J Clin Periodontol 2015; 42 (Suppl. 16): S172S186 doi: 10.1111/jcpe.

12346

Risk indicators for peri-implant Stefan Renvert1,2,3 and

Ioannis Polyzois3
1
Department of Health Sciences, Kristianstad

mucositis: a systematic literature University, Kristianstad, Sweden; 2Blekinge

Institute of Technology, Karlskrona, Sweden;
3
Dublin Dental University Hospital, Trinity

review College, Dublin, Ireland

Renvert S, Polyzois I. Risk indicators for peri-implant mucositis: a systematic

literature review. J Clin Periodontol 2015; 42 (Suppl. 16): S172S186. doi:
10.1111/jcpe.12346.

Abstract
Objectives: To examine the existing evidence in identifying risk indicators in the
aetiology of peri-implant mucositis.
Material and Methods: A search was performed in PubMed, Web of Science
(WOS) and The Cochrane Library databases for articles published until June 2014.
Results: This search gave 3135 results of which 15 studies fulfilled the inclusion cri-
teria. The current review revealed that only a few studies provided data on risk
indicators for the development of peri-implant mucositis. Based on the data avail-
able, there is evidence that plaque is a risk indicator for peri-implant mucositis.
Smoking has also been identified as an independent risk indicator whereas the over-
all evidence for surface roughness, residual cement, the dimension of the keratinized
tissue and time of implant in function is weak. There are limited data available to
support systemic conditions as risk indicators for peri-implant mucositis. Key words: peri-implant mucositis; plaque;
Conclusions: Plaque accumulation at implants will result in development of peri- risk indicators; smoking
implant mucositis. Smoking should also be considered as a risk indicator for the
development of peri-implant mucositis. Accepted for publication 27 November 2014

Peri-implant mucositis has been
defined as a reversible inflammatory
change in the peri-implant soft tissue
without bone loss (Albrektsson &
Isidor 1994) and it usually presents
as inflammation with erythema,
swelling and bleeding on probing
around the head of the dental
Conflict of interest and source of
funding statement
None of the authors declare a conflict
of interest. Kristianstad University
and Dublin Dental University Hospi-
tal, Trinity College, Dublin, Ireland
supported the study. The 11th Euro-
pean Workshop on Periodontology
was supported by an unrestricted edu-
cational grant from Procter & Gamble
and Johnson & Johnson.
S172
implant (Lindhe & Meyle 2008). A
more clinical based definition pre-
sented by Zitzmann & Berglundh
(2008) identified peri-implant muco-
sitis as the presence of inflamma-
tion in the mucosa at an implant
with no sign of loss of supporting
bone. Prevalence of peri-implant
mucositis has been reported in 80%
of subjects and 50% of implants
(Roos-Jans
aker et al. 2006a) and
there is currently some emerging evi-
dence to suggest that peri-implant
mucosititis is the precursor of peri-
implantitis (Costa et al. 2012).
Although there is only a small
number of studies available address-
ing risk indicators/factors in peri-
implant mucositis, smoking, residual
cement, bacterial micro-leakage
between the implant abutment inter-
face, implant surface characteristics,
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
type of the prosthetic supra-structure
and diabetes, have been proposed to
play a role in the aetiology of peri-
implant mucositis (Broggini et al.
2003, Ferreira et al. 2006, Pongnarisorn
et al. 2007, Karbach et al. 2009, Wil-
son 2009, Koutouzis et al. 2013). A
risk factor as defined by Genco et al.
(1996) is an environmental,
behavioural or biological factor that
if present directly increases the prob-
ability of a disease occurring and, if
absent or removed reduces that
probability.
A common finding in earlier
experimental studies was that patho-
genesis of peri-implant mucositis can
primarily be attributed to plaque
accumulation (Ericsson et al. 1992,
Leonhardt et al. 1992, Abrahamsson
et al. 1998, Zitzmann et al. 2002).
Most of the studies mentioned
 Risk indicators for peri-implant mucositis S173

above, employed a canine model and 2021 tles idened via PubMed
histological preparations of the peri-
925 tles idened through WOS
mucositis lesions to identify the Identification
inflammatory infiltrate. The inflam- 189 tles idened through The COCHRANE Library
mation was induced by termination No addional tles were idened through manual search
of the oral hygiene regimen. Human
studies further provided evidence
that the accumulation of plaque and
development of a biofilm contributes
to the initiation of inflammation
around the implants and if left
untreated, to the progression of Screening 3135 tles screened
peri-implant diseases (Leonhardt
et al. 1992, Pontoriero et al. 1994,
Augthun & Conrads 1997, Zitzmann
et al. 2001, Quirynen et al. 2006).
3028 tles were excluded and 79 abstracts were
Further evidence that poor oral
107 abstracts were screened excluded
hygiene is a significant risk factor
for the development of peri-implant
mucositis comes from a recent study
which demonstrated that peri-implant Eligibility 15 full text arcles were excluded 30 full text arcles
were assessed for
mucositis is reversible when treated (Reasons for exclusion in table 1) eligibility
(Salvi et al.2012). In addition,
mechanical therapy with or without
the adjunctive use of antiseptic rinses
has been proven to be effective in the
treatment of peri-implant mucositis
(Ciancio et al. 1995, Porras et al. 15 full text arcles were included
2002, Ji et al. 2014). Inclusion
The aim of this review was to (Tables 2-4)
examine the existing evidence in
identifying risk indicators in the aeti- Fig. 1. PRISMA flow diagram (Moher et al. 2009).
ology of peri-implant mucositis.

AND experimental peri-implant diseases

Materials and Methods
The Preferred Reporting Items for
Systematic Reviews and Meta-
Analyses (PRISMA) (Moher et al.
2009) was adopted for this system-
atic review. Two people were
involved in the search (S.R and I.P)
and the STROBE recommendations
(Appendix) were used as a guide for
the evaluation of the quality of exist-
ing research (von Elm et al. 2007). A
literature search was performed in
MEDLINE via PubMed database of
the US National Library of Medi-
cine, the Web of Science (WOS) and
the Cochrane library databases for
articles published until June 2014
using Medical Subject Heading
search terms + free text terms and in
different combinations:
PICO process for systematic search
Population (patients/animals with
implants): MeSH terms: dental
implant(s) OR dental implantation
OR
Text words: oral implants
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Intervention (exposure to risk
factors): MeSH terms: dental plaque
OR periodontal disease OR systemic
disease OR risk factor OR risk fac-
tors OR risk indicator OR genetic
OR dental cement OR risk OR
drugs OR pregnancy OR graft OR
medication
OR
Text words: cement excess OR
aetiology OR surface characteristics
OR smoking OR prosthesis OR
implant plaque OR surface rough-
ness OR surface hydrophobicity OR
soft tissue response OR keratinized
mucosa OR host response OR dental
abutment OR periodontal pathogens
AND/OR
Comparison (lack of plaque con-
trol): Text words: experimental
gingivitis OR experimental perimu-
cositis OR experimental peri-implant
mucositis OR experimental peri
implant mucositis OR experimental
periimplant disease OR experimental
peri-implant disease OR experimen-
tal peri implant disease OR experi-
mental peri implant diseases OR
OR experimental peri implant dis-
eases
AND
Outcome (development of peri-
implant mucositis): MeSH terms: mu-
cositis OR inflammation OR bleeding
OR
Text words: periimplant OR peri-
implant OR peri implant OR peri-
implant mucositis OR peri-implant
mucositis OR peri implant mucositis
OR periimplant disease OR peri-
implant disease OR peri implant dis-
ease OR peri implant diseases OR
peri-implant diseases OR peri
implant diseases OR peri-implant
health OR pathogenesis OR inflam-
mation OR infection.
Focused question
In subjects with dental implants,
exposure to which risk factors/indi-
cators can lead to the development
of peri-implant mucositis?
This search gave 3135 results. In
addition, the search was limited to
the English literature. After removal
S174 Renvert and Polyzois

of the duplicates, case reports, narra- Study Inclusion and exclusion criteria Results
tive reviews and screening of the To be included in the study, studies There was substantial heterogeneity
titles, 107 articles were selected from had to: between studies in terms of study
their title and abstracts were design. None of the selected studies
searched to find studies eligible for 1 Be written in English language
2 Be published in an International were either Randomized Controlled
the review. Seventy-nine full articles Clinical Trials (RCTs) or controlled
were excluded. Additional manual peer-reviewed journal
3 Describe attributes, exposures or clinical Trials (CCTs) so a meta-
search of reference lists in the papers analysis was not possible. An
selected as well as in a number of characteristics (risk indicators)
which can lead to peri-implant attempt was made to present a quali-
review articles was performed to tative report in both the tables and
source further relevant publications mucositis
4 Have a clear definition for peri- the conclusions.
(Fig. 1). Six of the studies selected were
Finally the following Journals implant mucositis or presence of
clinical data/assessed parameters experimental studies and employed
were searched manually between the canine model for assessing the
2000 and 2014: International journal which the reviewers could reliably
translate to peri-implant mucositis. pathogenesis of peri-implant mucosi-
of Oral and Maxillofacial Implants, tis (Ericsson et al. 1992, Leonhardt
European journal of Oral Implantolo- 5 For animal research studies have a
minimum of five animals and a et al. 1992, Abrahamsson et al. 1998,
gy, Journal of Oral Implantology, Zitzmann et al. 2002, Pongnarisorn
Implant Dentistry, Clinical Oral follow-up of at least 3 weeks.
6 For human research studies and et al. 2007, Schwarz et al. 2014). Five
Implants Research, Clinical Implant of them (Ericsson et al. 1992,
dentistry and Related Research, Jour- depending on the study design
have a minimum of 20 patients Leonhardt et al. 1992, Abrahamsson
nal of Periodontology, Journal of et al. 1998, Zitzmann et al. 2002,
Clinical Periodontology and Peri- overall or in each group examined
and a follow-up of at least Pongnarisorn et al. 2007) used the
odontology 2000. Two additional mandible and one used the Maxilla
articles was selected following the 3 weeks. As the number of avail-
able studies was small, we thought for implant insertion (Schwarz et al.
manual search. 2014). Four of these experimental
Finally, 30 full-text articles were it would be acceptable to apply
comparably less strict inclusion studies used five beagle dogs (Ericsson
assessed for eligibility and when dis- et al. 1992, Leonhardt et al. 1992,
agreements arose in the selection, criteria to previous reviews report-
ing on biological complications Abrahamsson et al. 1998, Zitzmann
they were resolved by discussion et al. 2002), one used six Foxhound
between the two reviewers. Fifteen around implants (Berglundh et al.
2002, Zitzmann & Berglundh dogs (Pongnarisorn et al. 2007) and
studies fulfilled the inclusion criteria one using eight greyhound dogs (Sch-
and 15 were excluded (Table 1). 2008).
warz et al. 2014). Two studies used 10
implants (Ericsson et al. 1992, Leon-
Table 1. Reasons for exclusion hardt et al. 1992), one used 20
Study Reason for exclusion implants (Zitzmann et al. 2002), one
30 implants (Abrahamsson et al. 1998),
Wennstr
om et al. (1994) No clear definition for peri-implant mucositis (Lack of one 48 implants (Schwarz et al. 2014)
radiographic evidence) and one 64 (Pongnarisorn et al.
Ericsson et al. (1995) No clear definition for peri-implant mucositis (No detailed 2007). One of these studies observed
clinical evaluation) the short (Leonhardt et al. 1992) and
Quirynen et al. (1996) Only six patients and no clear definition for peri-implant
one the long-term reaction of the soft
mucositis (Lack of radiographic evidence)
Zitzmann et al. (2001) Only 12 patients
tissues around teeth and implants (Er-
Wennerberg et al. (2003) Only nine patients icsson et al. 1992). One study investi-
Rene Schrott et al. (2009) No clear definition for peri-implant mucositis (Lack of gated the soft tissue response to
radiographic evidence) plaque formation at different implant
Taiyeb-Ali et al. (2009) No clear definition for peri-implant mucositis (Lack of systems (Abrahamsson et al. 1998)
radiographic evidence) and two at different surfaces
Vroom et al. (2009) Only 17 patients at 5 years and 13 in 12 years (Pongnarisorn et al. 2007, Schwarz
Rodriguez-Argueta No scores available for clinical and radiographic et al. 2014). All six studies took
et al. (2011) examinations. Just diagnosis biopsies of the lesions and performed
Salvi et al. (2012) Only 15 patients. No clear definition for peri-implant
mucositis (Lack of radiographic evidence)
histomorphometric analysis, five
Schwarz et al. (2012) 24 patients overall. Only eight patients in each group. No studies took clinical measurements
clear definition for peri-implant mucositis (Lack of (Ericsson et al. 1992, Leonhardt et al.
standardized radiographic evidence) 1992, Abrahamsson et al. 1998,
Ata-Ali et al. (2013) 34 patients but only 12 patients with peri-implant mucositis Pongnarisorn et al. 2007, Schwarz
Boynuegri et al. (2013) Only 15 patients. No acceptable definition for peri-implant et al. 2014) and two studies also took
mucositis (Lack of radiographic evidence) either immunological (Schwarz et al.
Koutouzis et al. (2013) Only eight patients in each group studied 2014) or microbiological measure-
Schwarz et al. (2014) 19 patients overall (two groups: nine patients in one and 10 in ments (Pongnarisorn et al. 2007).
the other) No clear definition for peri-implant mucositis
Finally, two studies (Pongnarisorn
(Lack of standardized radiographic evidence)
et al. 2007, Schwarz et al. 2014) used

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

one-piece implants, three studies used
two-piece (Ericsson et al. 1992, Leon-
hardt et al. 1992, Zitzmann et al.
2002) and one study used both types
(Abrahamsson et al. 1998).
Nine clinical studies were
included in this systematic review
(Pontoriero et al. 1994, Ferreira
et al. 2006, Roos-Jans
aker et al.
2006b, Maximo et al. 2008, Zigdon
& Machtei 2008, Karbach et al.
2009, Rinke et al. 2011, Casado
et al. 2013, Linkevicius et al. 2013).
They all assessed gingival inflamma-
tion using various indices and
depending on the risk indicators
investigated different tests were
employed to investigate possible
associations.
Aetiology of peri-implant mucositis
Pre-clinical studies
An experimental study performed in
1992 in the University of Gothen-
burg, used a canine model to study
the reaction of the peri-implant and
periodontal soft tissues to de novo
plaque formation (Table 2). The pre-
molar teeth from the left side of the
mandible were used for examination
and the premolars on the right side
were extracted to allow for future
implant installation. Following
implant abutment connection and 4-
months of plaque control, a clinical
examination and a block biopsy was
taken from one of the fixtures and
abutments together with adjacent
bone and masticatory mucosa in
each dog. Clinical examinations and
a block biopsy was also taken from
the contra-lateral tooth side. Plaque
control was terminated and the same
procedures were repeated 21 days
later. Clinical results, in combination
with data from the histomorphomet-
ric analysis, allowed the investigators
to conclude that termination of oral
hygiene measures and 3 weeks of
plaque accumulation was enough for
the soft tissues surrounding implants
and teeth to develop peri-mucositis/
gingivitis like symptoms (Leonhardt
et al. 1992). The same group of
researchers repeated the study, but
this time, the long-term effects
(90 days) of undisturbed plaque
accumulation were studied. They
observed that when the plaque was
allowed to stay longer in contact
with the peri-implant soft tissues the
inflammatory lesions progressed even
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Risk indicators for peri-implant mucositis
further apically to the gingival mar-
gin (Ericsson et al. 1992).
Clinical studies
In an early clinical study, patients
were requited from a private clinic
and had a history of periodontal dis-
ease. Following periodontal treat-
ment of all anterior teeth, two
implants were inserted in the poster-
ior edentulous area destined to sup-
port conventional fixed partial
dentures. Oral hygiene was rein-
forced and professional supportive
therapy was given to these patients
every 3 weeks. Baseline clinical and
microbiological examinations were
performed around the implants and
the teeth adjacent to them 2 months
following second stage surgery. Re-
examinations were performed at 3
and 6 months after baseline examin-
ations and patients were asked to
refrain from oral hygiene practices
for 3 weeks. At the end of the
3 weeks period, the same examina-
tions were repeated. Results showed
that inflammatory levels in the peri-
implant and periodontal tissues
stayed low during the 6-month
observation period and significantly
increased following the undisturbed
plaque accumulation (Pontoriero
et al. 1994).
Ferreira et al. (2006) examined
212 patients with three different
implant systems and diagnosed peri-
mucositis in 137 of them. All
implants were placed by postgradu-
ate students from five different den-
tal schools in Brazil and at the time
of examination all implants had been
in function for at least 6 months and
no more than 5 years. At an implant
level 362 of 578 implants were diag-
nosed with peri-implant mucositis.
The authors concluded that plaque
scores were statistically associated
with peri-implant mucositis and this
association was dose dependent.
In another human study, Roos-
Jans
aker et al. examined 218
patients with 999 implants. This
examination took place 914 years
following the placement of the
supra-structure. All the patients were
treated with the same implant sys-
tem. The effects of a number of
potential explanatory variables for
peri-implant mucositis on a patient
and on an implant level were analy-
sed. Both a single regression and a
multiple regression analysis were
S175
performed and plaque was explana-
tory on an implant level (p = 0.005
and p = 0.004 respectively) (Roos-
Jans

aker et al. 2006b).
Local risk indicators
Abutment surface characteristics
The mandibular premolar areas of
five beagle dogs were used by
Zitzmann et al. (2002) to examine
the soft tissue reactions of the peri-
implant mucosa to de novo plaque
formation on two implant abutments
with different surface topography
(Table 3a,b). Both the acid etched
and the turned abutment harboured
large amounts of plaque and calcu-
lus that resulted in significant inflam-
mation of the peri-implant tissues.
Clinical and histomorphometric
analysis failed to identify significant
differences between the two groups
regarding the amount of plaque
formed and the magnitude of the
inflammation developed due to this
plaque accumulation.
In another study, Pongnarisorn
and co-workers tried to determine
the nature of the inflammatory infil-
trate associated with four one-piece
implants, the transmucosal portion
of which had different surface char-
acteristics. These implants were
placed in the mandibular pre-molar
areas of eight greyhound dogs.
Despite the investigators attempt to
keep the abutments clean by carry-
ing out plaque control twice weekly
for 6 months, small amounts of den-
tal plaque was detected on each one
of the abutments leading to inflam-
matory lesions around them. The
different surface characteristics of
the transmucosal portion of these
implants did not seem to have an
effect on the nature of the infiltrate
or the peri-implant microbiota
(Pongnarisorn et al. 2007).
Recent experimental studies have
suggested that a chemically modified
hydrophilic surface can have a pre-
ventive effect either by slowing
down the biofilm formation or due
to better soft tissue adhesion (John
et al. 2013, Schwarz et al. 2013).
Schwarz and co-workers assessed
histologically and immunologically
experimental peri-mucositis at sur-
face enhanced titanium implants. In
a split-mouth design study, four
one-piece Straumann implants with
different surface characteristics were
 Table 2. Aetiology of peri-implant mucositis: pre/clinical and clinical studies
Study Number of Implant type Study description and Evaluation Results Comments Country/setting/
S176

animals/ methodology/parameters period funding

patients/implants assessed

Leonhardt Five beagle dogs Br

anemark An experimental study on
et al. (1992) 10 implants Nobelpharma dogs (mandible). To study
Experimental 7 mm 9 3.75 mm the reaction of the soft
tissues around teeth and
implants to de novo
plaque formation.
Clinical and
histomorphometric
21 days Both teeth and implants 21 days of undisturbed Sweden/University/
developed plaque accumulation is Institutional/
inflammatory lesions enough to initiate peri- industry
that fitted the profile implant inflammatory
of peri-implant lesion (ICT) extending
mucositis about 0.9 mm apical to
the gingival margin (in
both teeth and implants)
Renvert and Polyzois

observations and analysis

Ericsson et al. Five beagle dogs Br

anemark An experimental study on 90 days Following clinical and 90 days of undisturbed Sweden/University/
(1992) 10 implants Nobelpharma dogs (mandible). To study histomorphometric plaque accumulation Institutional/
Experimental the reaction of the soft analyses it was allows the peri-implant industry
tissues around teeth and observed that both inflammatory lesion (ICT)
implants to long-standing teeth and implants to progress to about
plaque accumulation developed 1.3 mm apical to the
inflammatory lesions gingival margin
that fitted the profile
of peri-implant
mucositis
Pontoriero 20 patients IMZ Clinical study 36 months The period of no oral Similar cause-effect Switzerland/Private
et al. (1994) 20 implants (longitudinal) compares re-evaluation hygiene demonstrated relationship was Practice/NR
Experimental the clinical and + 3 weeks a cause effect demonstrated between the
microbiological experimental relationship between accumulation of bacterial
parameters during the peri-implant the accumulation of plaque and the
development of mucositis/ bacterial plaque and development of gingivitis
experimentally induced gingivitis the development of in natural teeth
peri-implant mucositis peri-implant mucositis.
and gingivitis.
PlI, GI,SBI,PPD, Gingival
margin level, phase
contrast microscopy
Ferreira et al. 212 patients Nobel BioCare A cross-sectional study to 6 months The association Prevalence of peri-implant Brazil/University/
(2006) 578 Implants Intra-lock & 3i investigate the prevalence between plaque scores mucositis in subjects was NR
Observational and risk variables of peri- 5 years and peri-implant 64.6% (n = 137) and in
implant disease. disease was dose implants 62.6% (n = 362).
PPD, CAL, radiographic dependent Subjects with diabetes
measurements, mPLI, were more susceptible to
BOP, Supp develop peri-implant
mucositis. The association
between plaque scores
and peri-implant disease
was dose dependent

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
 Risk indicators for peri-implant mucositis S177

ICT, Infiltrated Connective Tissue; NR, Not Reported; PlI, Plaque Index; GI, GingivaI Index; SBI, Sulcus Bleeding Index; PPD, Probing Pocket Depth; mPLI, modified Plaque Index; Supp,
placed in the maxilla of six dogs and

Sweden/University/
Country/setting/
were allowed to accumulate plaque
for 16 weeks. Histomorphometric

funding

Institutional
and immunological analyses showed
that in all implants, the initiation
and progression of peri-implant mu-
cositis was comparable that the
severity of the inflammatory lesions

On a Patient level: smoking

was directly proportional to the level

have affected the results

and age were associated
of plaque present (Schwarz et al.

treatment, which might

supportive periodontal
There was no uniform
2014).
Comments

with peri-implant Abutment geometry/design

of this study
In 1998 a study was designed to
mucositis.

investigate the response of soft tissue

to plaque formation but also the
possibility that soft tissues around
implant transmucosal abutments
with different geometry respond dif-
presence of keratinized

peri-implant mucositis
were explanatory for

ferently. The investigators allowed

mucosa and plaque
On an implant level:

the outcome event

for 5 months of undisturbed plaque

Results

accumulation. Following clinical

observations and histomorphometric
measurements, it was observed that
the level of inflammation was
comparable at all three implants
investigated (Abrahamsson et al.
1998).
Evaluation

914 years

Dimensions of keratinized tissue

period

Two recent studies in humans inves-

tigated the effect of keratinized
mucosa as a risk factor for develop-
ment of peri-implant mucositis
implant treatment and the

of remaining teeth before

threads not supported by

PPD, BOP, Supp, PS, %
methodology/parameters

(Roos-Jans
aker et al. 2006b, Zigdon

Study description and

implant placement with

factors associated with
914-year follow-up of

& Machtei 2008). Results from these

peri-implant lesions.

number of implant
bone loss 4 mm,

studies suggested that these dimen-

assessed

radiographically
bone measured

sions might have some effect on the

inflammatory state of the soft tissue
around dental implants but more as
an effect on plaque control than as a
direct correlation to soft tissue
health.
In a retrospective clinical trial
including 63 patients the aim was to
Implant type

Nobelpharma

investigate the association between

anemark

keratinized mucosa width and thick-

ness around implants with certain
clinical and immunological parame-
Br

ters. All patients included in the

study contributed with at least one
patients/implants

functioning dental implant, which

999 Implants
Number of

must have been in function for a

animals/

218 patients

minimum of 1 year. Smokers were

included and all implants had the
same surface topography. In addi-
Table 2. (Continued)

tion to the clinical examination, peri-

implant crevicular fluid samples were
Observational
aker
et al. (2006b)

collected for prostaglandin E2

Suppuration.
Roos-Jans

(PgE2) levels. Oral hygiene was gen-

erally good and overall, signs of
Study

peri-implant mucositis showed only

a minor correlation with the width
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
 S178

Table 3. Local risk indicators

Study Number of Implant type Study description and Evaluation Results Comments Country/setting/
animals/ methodology/parameters period funding
implants assessed

(a)
Abrahamsson 5 beagle dogs Nobel Biocare A comparative study in the 5 months Following clinical 90 days of undisturbed Sweden/University/
et al. (1998), 30 implants 7 mm 9 3.75 mm dog (mandible). To study observations and plaque accumulation Institutional/
Experimental Astra Tech the soft tissue response to histomorphometric allows the peri-implant industry
Renvert and Polyzois

8 mm 9 3.5 mm and plaque formation at
Straumann different implant systems
8 mm 9 4 mm
Zitzmann et al. 5 beagle dogs Biomet3i Osseotite An experimental study in 6 months
(2002), 20 implants 3.75 mm 9 8.5 mm dogs (mandible).
Experimental Reactions of the peri-
implant mucosa to plaque
accumulation at implant
abutments with different
surface topography
(Osseotite and Turned).
Histometric and
morphometric
measurements after
biopsies were obtained
containing the implant
and the surrounding
tissues
Pongnarisorn 8 greyhound Nobel Biocare An experimental study in
et al. (2007), dogs One-piece designed dogs (mandible).
Experimental 64 implants implants To determine the nature
Ti-Unite surface of the inflammatory
3.75 mm 9 7 mm infiltrate associated with
different transmucosal
implant surfaces in dogs.
Surfaces: Acid etched,
Standard Br
anemark
abutment, Machined with
groove, Mildly anodic
oxidized surface
analyses, it was observed inflammatory lesion (ICT)
that the progression of to progress to about 1.6
experimental mucositis 2 mm in the 3 different
was comparable at the systems investigated
implant systems
investigated
Soft tissue reaction to In all implants, Sweden/University/
plaque formation was quantitative and NR
similar at implants with qualitative differences
rough and smooth were identified between
abutment surfaces the plaque associated
lesion and the abutment/
fixture junction associated
lesion in the connective
tissue
6 months Following histological and Plaque control was carried Australia/
microbiological analysis, out twice weekly for University/Industry
it was concluded that 6 months. Despite
development of cleaning the abutments
inflammation associated regularly, inflammatory
with implants was lesions were detected.
independent of surface Clinically, all peri-implant
type. Furthermore, tissues did not look
different surfaces had no inflamed despite the fact
influence on the nature of that small amounts of
the infiltrate supra-gingival plaque
were detected on each
implant

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
 Table 3. (Continued)
Study Number of Implant type Study description and Evaluation Results Comments Country/setting/
animals/ methodology/parameters period funding
implants assessed

Schwarz et al. 6 foxhound Straumann, one-piece An experimental study in
(2014) dogs RN, standard plus, dogs (maxilla).
Experimental 48 implants 3.3 mm 9 8 mm To assess histologically and
immunologically
experimental peri-implant
mucositis at surface
enhanced modified
hydrophilic titanium
implants.
Surfaces: TiZr mod SLA,
TiZr mod MA, TiZr
Machined, Ti Machined
16 weeks Following In all implants, the Germany/
histomorphometric and establishment and severity University/
Immunological analyses, of peri-mucositis, was Institutional
it was observed that the directly correlated with
progression of the level of plaque
experimental mucositis formation
was comparable at all
implant surfaces
investigated

Study Number of Implant type Study Description and Evaluation Results Comments Country/setting/
patients/ Methodology/Parameters period funding
implants assessed

(b)

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Roos-Jans
aker 218 patients Br

anemark 914-year follow-up of 914 years On an implant level: On a Patient level: smoking Sweden/University/
et al. (2006b) 999 Implants Nobelpharma implant treatment and the presence of keratinized and age were associated Institutional
Observational factors associated with mucosa and plaque were with peri-implant
peri-implant lesions. explanatory for the mucositis.
PPD, BOP, Supp, PS, % outcome event peri- There was no uniform
of remaining teeth before implant mucositis supportive periodontal
implant placement with treatment, which might
bone loss 4 mm, have affected the results
number of implant of this study
threads not supported by
bone measured
radiographically
Zigdon & 32 patients 3i Osseotite A retrospective clinical trial At least No correlation between Keratinized mucosa width Israel/University/
Machtei 63 dental evaluating if the 1 year in keratinized mucosa width seems to affect other Institutional
(2008) implants dimensions of keratinized function and Bleeding on Probing clinical and
Observational mucosa around implants or gingival index but a immunological parameters
affect clinical and moderately positive
immunological correlation with Probing
parameters. Depth
KM width, MTh, MR, PD,
BOP, GI, PAL, presence/
Risk indicators for peri-implant mucositis

absence of plaque
S179
 S180 Renvert and Polyzois

and thickness of the keratinized Finally, Rinke et al. (2011) con-

GI, gingival index; NR, not reported; PPD, probing pocket depth; BOP, bleeding on probing; mPLI, modified Plaque Index; Supp, suppuration; KM, keratinized mucosa; MR, mucosal
mucosa (Zigdon & Machtei 2008). ducted a retrospective cross-sectional

Lithuania/Latvia/
Pr.practice/NR
Country/setting/

Roos-Jans
aker et al. (2006b), study, which also identified smoking

after exploring a number of poten- as a risk indicator for peri-implant
tially explanatory variables for the mucositis.
funding

outcome event peri-implant mucosi-

tis, concluded that on the implant
level and both in single regression
and multiple regression analysis the
presence of keratinized mucosa was
significantly less in the
Radiation therapy
Karbach et al. (2009), in the study
that was described above, identified
radiation therapy as a significant risk

a significant risk indicator (p = 0.02 indicator for developing peri-implant

Complications were

and p = 0.008 respectively). In this mucositis both on the single and

study, peri-implant mucositis was multiple regression analysis.
control group

defined as probing depth 4 mm and

Diabetes
Comments

BOP so the authors suggested that

shallower pockets would be more
common in areas with less kerati-
nized mucosa.
be more prone to develop
peri-implant disease when
In the study by Ferreira et al.
(2006), where they examined 212
patients and diagnosed with peri-mu-
cositis 137 of the subjects, a possible

Residual Cement
Patients with a history of
periodontal disease may

association of peri-mucositis with

tissues get exposed to

A recent retrospective study by diabetes was investigated. Smokers

Linkevicius et al. (2013) tried to and former smokers were excluded
residual cement

determine if residual cement in from this study. The authors also

patients with a previous history of factored a number of demographic,
periodontitis is a risk indicator for behavioural and biological risk vari-
Results

developing peri-implant diseases. ables into their analysis and when a

Although patients with a history of single regression statistical analysis
periodontal disease were more at was used, the results demonstrated
risk, patients without this character- that patients with diabetes were
to the diagnosis
of complication
6 months from

the restoration
the delivery of

istic were also affected. more susceptible to develop peri-mu-

cositis. Interestingly, when a multi-
Evaluation

More than

Systemic risk indicators nomial logistic regression analysis

period

was used to investigate the degree of

Smoking
association, diabetes was not associ-
Karbach et al. (2009) compared five ated with peri-mucositis.
parameters as risks factors for peri-
patients with a history of
Methodology/Parameters

development of cement-

implant mucositis and examined for Patient related risk indicators

aiming to determine a
Study Description and

periodontitis and the

relationship between
A retrospective study

specific periodontal pathogens as

related peri-implant

Function time of Implant

they tried to identify possible corre-
lations (Table 4). A hundred patients In an attempt to evaluate prevalence
recession; PAL, periodontal attachment levels; Mth, Mucosa thickness.

were examined with a minimum fol- of peri-implant diseases around

low-up of 1 year and a maximum of Br
anemark implants and the possible
disease
assessed

19 years following fitting of the res- relationship with time of loading,

toration. The parameters evaluated
were roughness of implant surface,
smoking, augmented implant site,
Bio-Horizons
Implant type
periodontal bone loss, certain sys-
temic conditions and a general
demographic profile, 113 subjects

presence of residual teeth and radia-
tion therapy. For patients that had
more than one implant, the one with
the deepest pocket was selected for
microbiological analysis. Results
(screw retained)
treated with at least one machined
Br
anemark implant were recruited
by M aximo et al. (2008) (Table 4).
The implants were clinically and
radiographically examined. Results

showed that smoking was a signifi- demonstrated that there was a weak
Test: 77 Patients
129 Implants

238 Implants
restorations)

cant risk indicator for developing correlation between peri-implant mu-

66 Patients
(cemented
Number of

peri-implant mucositis. cositis and increased time of loading

patients/
implants

(r = 0.44; p = 0.0058) but no other

Control:

Roos-Jans
aker et al. (2006b) after

exploring a number of potentially risk indicators were identified.
Table 3. (Continued)

explanatory variables for the out- In the study by Ferreira et al.

come event peri-mucositis, concluded (2006), one of the risk indicators
Observational

that on the patient level and both in that was associated with peri-implant
et al. (2013)
Linkevicius

single and multiple regression analy- mucositis was time of implant load-
sis smoking was a significant risk ing but this same independent
Study

indicator (p = 0.009 and p = 0.02 variable, failed to demonstrate an

respectively). association in an adjusted model.
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
 Table 4. Systemic risk indicators and patient-related risk indicators
Study Number of Implant type Study Description and Evaluation Results Comments Country/setting/
patients/implants Methodology/Parameters period funding
assessed

Ferreira et al. (2006) 212 patients Nobel BioCare A cross-sectional study to 6 months Male patients were Prevalence of peri-implant Brazil/University/
Observational 578 Implants Intra-lock & 3i investigate the prevalence 5 years more susceptible to mucositis in subjects was NR
and risk variables of peri- peri-implant 64.6% (n = 137) and in
implant disease. mucositis Implants 62.6% (n = 362).
PPD, CAL, radiographic Subjects with diabetes were
measurements, mPLI, BOP, more susceptible to develop
Supp peri-implant mucositis. The
association between plaque
scores and peri-implant
disease was dose dependent
Roos-Jans
aker 218 patients Br

anemark 914-year follow-up of 914 years On a Patient level: On an implant level: Sweden/University/
et al. (2006b) 999 Implants Nobelpharma implant treatment and the smoking and age presence of keratinized Institutional
Observational factors associated with peri- were associated with mucosa and plaque were
implant lesions peri-implant explanatory for the
PPD, BOP, Supp, PS, % of mucositis outcome event peri-implant
remaining teeth before mucositis.

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
implant placement with There was no uniform
bone loss 4 mm, number supportive periodontal
of implant threads not treatment, which might
supported by bone have affected the results of
measured radiographically this study
Karbach et al. (2009) 100 patients Not reported A study identifying risk Minimum Smoking is an The type of dentition seems Germany/
Observational factors for the development follow-up important risk to influence the periodontal University/NR
of clinical signs of peri- of 1 year and indicator in the microflora at the implant
implant mucositis. Maximum formation of peri- site
PI, BOP,PPD, Microbiologic 19 years implant mucositis
analysis
Maximo et al. (2008) 113 patients Machined A casecontrol study Minimum Statistically significant Peri-implant mucositis may Brazil/University/
Observational 41 Patients with Br

anemark evaluating the possible follow-up of positive correlations be associated with the NR
peri-mucositis relationship of peri-implant 1 year. Mean were found in increasing time of loading
diseases with periodontal follow-up implants with
bone loss, systemic 3.4 years mucositis in relation
condition and demographic to time of loading
profile.
BOP, Supp, PD, GI,
radiographic examination
Risk indicators for peri-implant mucositis
S181
S182 Renvert and Polyzois

Country/setting/ Genetics

Brazil/University/
Germany/Private
funding
Casado et al. (2013), investigated the

Practice/NR
association between interleukin 6 (IL-
6) G174C polymorphism and suscep-

NR
tibility to peri-implant disease as well
as susceptibility to chronic periodon-
titis. Although the results demon-

identified as risk indicators

both Chronic periodontitis

strated that the frequency of the

common risk indicator for

implants per patient, and
periodontal disease, age

for peri-implant mucositis

and Peri-implant diseases

The independent variables

PPD, probing depth; BOP, bleeding on probing; Supp, suppuration; GI, gingival index; NR, not reported; mPLI, modified Plaque Iindex; PI, modified plaque index.
genotype IL-6 174GG and allele G
placement, follow-up

compliance were not

This genotype may be a

gender, history of

period, number of
was different between healthy and
Comments

at time of implant

diseased patients, these results should

be interpreted with caution due to the
very small number of patients
(n = 20) included in this study.
Gender
Ferreira et al. (2006) demonstrated
that the male gender could be con-
174GG and allele G
The frequency of the

sidered as a risk indicator for peri-

formation of peri-

indicator for peri-

implant mucositis

implant mucositis
indicator in the

mucositis both in the single and the

important risk

genotype IL-6
Results

may be a risk
Smoking is an

multiple regression analysis.

Maintenance visits
Development of peri-implant mucosi-
tis was not found to be associated with
the frequency of visits to the dentist
24.8 months.

follow-up of
Evaluation

\dental hygienist (Ferreira et al. 2006,

1 year and
follow-up
period

Maximum
5.7 years

Minimum

Roos-Jans
aker et al. 2006b).

5 years
68.2 

Mean

Discussion
The early experimental studies by
palpation for inflammation,
interleukin-6 (IL-6) G174C

implant disease (PID) and/

Methodology/Parameters

Leonhardt et al. (1992), Ericsson

Study Description and

radiographic assessment.
or chronic periodontitis.
A study investigating the

and oedema, PD, BOP,

evaluate the prevalence
The primary aim was to

periimplantitis and the

identify risk indicators

Length Polymorphism

et al. (1992), Abrahamsson et al.

secondary aim was to

susceptibility to peri-

Restriction fragment
Visual inspection and
rates of periimplant

association between

polymorphism and

(1998), were the ones that demon-

assessed

implant mobility,

strated for the first time that there is

percussion test,
mucositis and

an association between bacterial pla-

que biofilm formation and peri-
implant diseases. As canines show a
natural susceptibility to periodontal
disease, the above series of studies
gave also the first indication that the
Dentsply Friadent

clinical and histological characteris-

Implant type

tics of the experimentally induced

Not reported

lesions have many features in com-

Ankylos,

mon with naturally occurring lesions

(Weinberg & Bral 1999, Schwarz
et al. 2012). The cross-sectional stud-
ies by Ferreira et al. (2006) and
40 Patients with

20 patients with
patients/implants

Roos-Jans
aker et al. (2006b) and the

Peri-mucositis
peri-mucositis
Number of

prospective study by Pontoriero

103 patients
89 patients

et al. (1994), validated the above-

mentioned claims of a cause-effect
relationship between the presence of
bacterial plaque and the develop-
ment of peri-implant mucositis. Fur-
Table 4. (Continued)

Casado et al. (2013)

Rinke et al. (2011)

thermore Pontoriero et al. (1994)

showed that the soft tissues around
Observational

Observational

teeth and implants, respond similarly

to bacterial plaque.
In an article by Heitz-Mayfield
Study

(2008), it was suggested that true risk

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

factors can only be identified by pro-
spective longitudinal studies. Four
years later, in a consensus report
from the VIII European Workshop
in Periodontology the evidence neces-
sary and the process required for
defining risk factors, in terms of
study design, were discussed (Sanz &
Chapple 2012, Tomasi & Derks
2012). It was discussed that initially,
cross-sectional studies or casecontrol
studies and a single regression statisti-
cal analysis can identify putative risk
factors. Additional employment of a
multiple regression analysis in the
above-mentioned type of studies can
be useful in identifying potential con-
founding factors. Validating these
putative risk factors, requires the use
of prospective Cohort studies whose
results are reproducible in different
populations (Sanz & Chapple 2012,
Tomasi & Derks 2012).
Some of the most important
problems identified in the VIII
Workshop and in the review herein
were that the available studies were
not adequately powered and the
samples were not representative of
the population. A number of pro-
spective studies which could have
contributed greatly to the existing
evidence had to be excluded due to
their lack of power (Vroom et al.
2009, Boynuegri et al. 2013, Sch-
warz et al. 2014). In addition, most
of the studies were not originally
designed to specifically assess the
impact of an exposure, attribute or
characteristic on the development of
peri-implant mucositis. This later
characteristic of some of the pub-
lished articles complicated interpre-
tation of the results as it was left
up to reviewers to decide if they
could reliably extract the informa-
tion needed to diagnose peri-muco-
sitis from the parameters assessed in
each article.
Conclusions
It is clearly demonstrated that
plaque accumulation results in
peri-implant mucositis around
osseointegrated dental implants
(seven experimental, and two
cross-sectional studies). Good
strength of evidence exists and
two studies (Ferreira et al. 2006,
Roos-Jans
aker et al. 2006b) used
multiple logistic regression analy-
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Risk indicators for peri-implant mucositis
sis to provide estimates of the
relative risk after being appropri-
ately adjusted for particular con-
founders.
Smoking has also been high-
lighted as a risk indicator for
peri-implant mucositis. Three
studies provided evidence (Roos-
Jans
aker et al. 2006b, Karbach
et al. 2009, Rinke et al. 2011),
and again all three used multiple
logistic regression analysis to pro-
vide estimates of the relative risk
after being appropriately adjusted
for particular confounders.
Although three experimental
studies indicated that there is a
possibility that different abutment
surface characteristics may play a
role in the quality or quantity of
plaque accumulated at the trans-
mucosal section of the implant,
the overall evidence should be
considered weak. (Zitzmann et al.
2002, Pongnarisorn et al. 2007,
Schwarz et al. 2014).
Radiation therapy has been
highlighted as a significant risk
indicator for developing peri-
implant mucositis (Karbach et al.
2009).
There is an indication from a
cross-sectional (Roos-Jans
aker
et al. 2006b) and a retrospective
clinical trial (Zigdon & Machtei
2008) that the role of keratinized
tissue as a risk indicator for peri-
implant mucositis should be con-
sidered for further investigation.
Current evidence is weak.
There is weak evidence from two
cross-sectional studies (Ferreira
et al. 2006, Roos-Jans
aker et al.
2006b) to support the role of
Diabetes as a risk indicator for
peri-implant mucositis.
There is weak evidence from one
casecontrol study (Casado et al.
2013) to support the role of
Genetics in the development of
peri-implant mucositis.
There is weak evidence from one
cross-sectional study (Ferreira
et al. 2006) to support the role of
gender as a risk indicator in the
development of peri-implant mu-
cositis.
There is weak evidence from two
studies to support the role of
function time of implants as a
risk indicator for peri-implant
mucositis (Ferreira et al. 2006,
M aximo et al. 2008).
S183
There is some evidence from a
retrospective study (Linkevicius
et al. 2013) to support the role of
residual cement as a risk indica-
tor for peri-implant mucositis.
Overall, peri-implant mucositis
does not seem to be a condition
related to implant system, surface
topography or width of kerati-
nized tissue but more to the
amount of plaque accumulation
and patient susceptibility.
Controversial data are available in
the literature about the risk vari-
ables and individuals who present
a higher risk of developing peri-
implant mucositis. There is a need
for more adequately powered pro-
spective longitudinal studies to try
and identify the potential effects
that certain biological, demo-
graphic and behavioural variables
have on the initiation of the
inflammatory processes affecting
peri-implant tissues.
References
Abrahamsson, I., Berglundh, T. & Lindhe, J.
(1998) Soft tissue response to plaque formation
at different implant systems. A comparative
study in the dog. Clinical Oral Implants
Research 9, 7379.
Albrektsson, T. & Isidor, F. (1994) Consensus
report of session IV. In: Lang, N. P. &
Karring, T. (eds). Proceedings of the First
European Workshop on Periodontology.
London: Quintessence pp. 365369.
Ata-Ali, J., Flichy-Fern an ez, J., Ata-Ali, F.,
Penarroch-Diago, M. & Pe narroch-Diago, M.
(2013) Clinical Microbiologic and host response
characteristics in patients with peri-implant mu-
cositis. International Journal of Oral and Maxil-
lofacial Implants 28, 830890.
Augthun, M. & Conrads, G. (1997) Microbial
findings of deep peri-implant bone defects.
International Journal of Oral and Maxillofacial
Implants 12, 106112.
Berglundh, T., Persson, L. & Klinge, B. (2002) A
systematic review of the incidence of biological
and technical complications in implant den-
tistry reported in prospective longitudinal stud-
ies of at least 5 years. Journal of Clinical
Periodontology 29, 197212.
Boynue gri, D., Nemli, S. K. & Kasko, Y. A.
(2013) Significance of keratinized mucosa
around dental implants: a prospective compar-
ative study. Clinical Oral Implants Research 24,
928933.
Broggini, N., McManus, L. M., Hermann, J. S.,
Medina, R. U., Oates, T. W., Schenk, R. K.,
Buser, D., Mellonig, J. T. & Cochran, D. L.
(2003) Persistent acute inflammation at the
implant-abutment interface. Journal of Dental
Research 82, 232237.
Casado, P. L., Villas-Boas, R., de Mello, W.,
Duarte, M. E. & Granjeiro, J. M. (2013) Peri-
implant disease and chronic periodontitis: is
interleukin-6 gene promoter polymorphism the
common risk factor in a Brazilian population?
S184 Renvert and Polyzois
International Journal of Oral and Maxillofacial
Implants 28, 3543.
Ciancio, S. G., Lauciello, F., Shibly, O., Vitello,
M. & Mather, M. (1995) The effect of an anti-
septic mouthrinse on implant maintenance: pla-
que and peri-implant gingival tissues. Journal
of Periodontology 66, 962965.
Costa, F. O., Takenaka-Martinez, S. & Cota, L. O.
M. (2012) Peri-implant disease in subjects with
and without preventive maintenance: a 5-year
follow up. Journal of Periodontology 39, 173181.
von Elm, E., Altman, D. G., Egger, M., Pocock,
S. J., Gotzsche, P. C. & Vandenbroucke, J. P.
(2007) The strengthening of reporting of obser-
vational studies in epidemiology (STROBE)
Statement: guidelines for reporting observa-
tional studies. Bulletin of the World Health
Organization 85, 867872.
Ericsson, I., Berglundh, T., Marinello, C.,
Liljenberg, B. & Lindhe, J. (1992) Long-standing
plaque and gingivitis at implants and teeth in the
dog. Clinical Oral Implants Research 3, 99103.
Ericsson, I., Persson, L. G., Berglundh, T.,
Marinello, C., Lindhe, J. & Klinge, B. (1995)
Different types of inflammatory reactions in
peri-implant soft tissues. Journal of Clinical
Periodontology 22, 255261.
Ferreira, S. D., Silva, G. L. M., Cortelli, J. R.,
Costa, J. E. & Costa, F. O. (2006) Prevalence
and risk variables for peri-implant disease in
Brazilian subjects. Journal of Clinical Periodon-
tology 33, 929935.
Genco, R. J., Jeffocat, M., Cton, J., Papapanou,
P., Armitagwe, G. C., Grossi, S., Johnson, N.,
Lamster, I., Lang, N. P., Robertson, P. &
Sanz, M. (1996) Consensus report. Periodontal
diseases: epidemiology and diagnosis. Annals
Periodontology 1, 216222.
Heitz-Mayfield, L. J. A. (2008) Peri-implant dis-
eases: diagnosis and risk indicators. Clinical
Oral Implants Research 35, 214222.
Ji, Y. J., Tang, Z. H., Wang, R., Cao, J., Cao, C.
F. & Jin, L. J. (2014) Effect of glycine powder
air-polishing as an adjunct in the treatment of
peri-implant mucositis: a pilot clinical trial.
Clinical Oral Implants Research 25, 683689.
John, G., Becker, J. & Schwarz, F. (2013) Modi-
fied implant surface with slower and less initial
biofilm formation. Clinical Implant Dentistry
and Related Research [e-pub ahead of print.]
Karbach, J., Callaway, A., Kwon, Y. D.,
dHoedt, B. & Al-Nawas, B. (2009) Compari-
son of five parameters as risk factors for peri-
mucositis. International Journal of Oral Maxil-
lofacial Implants 24, 491496.
Koutouzis, T., Koutouzis, G., Gadalla, H. & Nei-
va, R. (2013) The effect of healing abutment
reconnection and disconnection on soft and hard
peri-implant tissues: a short-term randomized
controlled clinical trial. International Journal of
Oral and Maxillofacial Implants 28, 807814.
Leonhardt, A.,
Berglundh, T., Ericsson, I. &
Dahlen, G. (1992) Putative periodontal patho-
gens on titanium implants and teeth in experi-
mental gingivitis and periodontitis in beagle dogs.
Clinical Oral Implants Research 3, 112119.
Lindhe, J. & Meyle, J. (2008) Peri-implant dis-
eases: consensus report of the sixth European
workshop on periodontology. Journal of Clini-
cal Periodontology 35 (Suppl. 8), 282285.
Linkevicius, T., Puisys, A., Vindasiute, E., Linke-
viciene, L. & Apse, P. (2013) Does residual
cement around implant-supported restorations
cause peri-implant disease? A retrospective case
analysis. Clinical Oral Implants Research 24,
11791184.
Maximo, M. B., de Mendonca, A. C., Alves, J.
F., Cortelli, S. C., Peruzzo, D. C. & Duarte, P.
M. (2008) Peri-implant diseases may be associ-
ated with increased time loading and general-
ized periodontal bone loss: preliminary results.
Journal of Oral Implantology 34, 268273.
Moher, D., Liberati, A., Tetzlaff, J. & Altman,
D. G. & the PRISMA Group (2009) Preferred
reporting items for systematic reviews and
meta-analyses: the PRISMA statement. PLoS
Medicine 6, e1000097.
Pongnarisorn, N. J., Gemmell, E., Tan, A. E.,
Henry, P. J., Marshall, R. I. & Seymour, G. J.
(2007) Inflammation associated with implants
with different surface types. Clinical Oral
Implants Research 18, 114125.
Pontoriero, R., Tonelli, M. P., Carnevale, G.,
Mombelli, A., Nyman, S. R. & Lang, N. P.
(1994) Experimentally induced peri-implant
mucositis. A clinical study in humans. Clinical
Oral Implants Research 5, 254259.
Porras, R., Anderson, G. B., Caffesse, R., Naren-
dran, S. & Trejo, P. M. (2002) Clinical
response to two different therapeutic regimes to
treat peri-implant mucositis. Journal of Peri-
odontology 73, 11181125.
Quirynen, M., Bollen, M. L., Papaioannou, W.,
Van Eldere, J. & van Steenberghe, D. (1996)
The influence of titanium abutment surface
roughness on plaque accumulation and gingivi-
tis: short-term observations. International Jour-
nal of Oral and Maxillofacial Implants 2, 168
178.
Quirynen, M., Vogels, R., Peeters, W., van
Steenberghe, D., Naert, I. & Haffajee, A.
(2006) Dynamics of initial subgingival coloniza-
tion of pristine peri-implant pockets. Clinical
Oral Implants Research 17, 2537.
Rinke, S., Ohl, S., Ziebolz, D., Lange, K. &
Eickholz, P. (2011) Prevalence of periimplant
disease in partially edentulous patients: a
practice- based cross-sectional study. Clinical
Oral Implants Research 22, 826833.
Rodriguez-Argueta, O. F., Figueiredo, R., Valma-
seda Castellon, E. & Gay-Escoda, C. (2011)
Postoperative complications in smoking
patients treated with implants: a retrospective
study. Journal of Oral and Maxillofacial Sur-
gery 69, 21522157.
Roos-Jans
aker, A. M., Lindahl, C., Renvert, H.
& Renvert, S. (2006a) Nine- to fourteen-year
follow-up of implant treatment. Part II: pres-
ence of peri-implant lesions. Journal of Clinical
Periodontology 33, 290295.
Roos-Jans
aker, A. M., Renvert, H., Lindahl, C.
& Renvert, S. (2006b) Nine- to fourteen-year
follow-up of implant treatment. Part III: fac-
tors associated with peri-implant lesions. Jour-
nal of Clinical Periodontology 33, 296301.
Salvi, G. E., Aglietta, M., Eick, S., Sculean, A.,
Lang, N. P. & Ramseier, C. A. (2012) Revers-
ibility of experimental peri-implant mucositis
compared with experimental gingivitis in
humans. Clinical Oral Implants Research 23,
182190.
Sanz, M. & Chapple, I. L. (2012) Clinical
Research on peri-implant diseases: consensus
report of Working Group 4. Journal of Clinical
Periodontology. 39 (Suppl. 12), 202206.
Schrott, R. A., Jimenez, M., Hwang, J. W., Fio-
rellini, J. & Weber, H. P. (2009) Five year eval-
uation of the influence of keritinized mucosa
on peri-implant soft tissue health and stability
around implants supporting full arch mandibu-
lar fixed prostheses. Clinical Oral Implants
Research 20, 11701177.
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Schwarz, F., Iglhaut, G. & Becker, J. (2012) Qual-
ity assessment of reporting of animal studies
on pathogenesis and treatment of peri-implant
mucositis and peri-implantitis. A systematic
review using the ARRIVE guidelines. Journal
of Clinical Periodontology 39, 6372.
Schwarz, F., Mihatovic, I., Becker, J., Bormann,
K. H., Keeve, P. L. & Friedmann, A. (2013)
Histological evaluation of different abutments
in the posterior maxilla and mandible. An
experimental study in humans. Journal of Clini-
cal Periodontology 40, 807815.
Schwarz, F., Mihatovic, I., Golubovic, V., Eick,
S., Iglhaut, T. & Becker, J. (2014) Experimental
peri-implant mucositis at different implant sur-
faces. Journal of Clinical Periodontology 41,
513520.
Taiyeb-Ali, T. B., Toh, G. C., Huat Siar, C. H.,
Seiz, D. & Ong, S. T. (2009) Influence of abut-
ment design on clinical status of peri-implant
tissues. Implant Dentistry 18, 438441.
Tomasi, C. & Derks, J. (2012) Clinical research of
peri-implant diseases-quality of reporting, case
definitions and methods to study incidence,
prevalence and risk factors of peri-implant dis-
eases. Journal of Clinical Periodontology 39
(Suppl. 12), 207223.
Vroom, M. G., Sipos, P., de Lange, G. L.,
Gr undemann, L. J., Timmerman n, M. F., Loos,
B. G. & van der Velden, U. (2009) Effect of sur-
face topography of screw-shaped titanium
implants in humans on clinical and radiographic
parameters: a 12-year prospective study. Clinical
Oral Implants Research 20, 12311239.
Weinberg, M. A. & Bral, M. (1999) Laboratory
animal models in periodontology. Journal of
Clinical Periodontology 26, 335340.
Wennerberg, A., Sennerby, L., Kultje, C. & Lek-
holm, U. (2003) Some soft tissue characteristics
at implant abutments with different surface
topography. A study in humans. Journal of
Clinical Periodontology 30, 8894.
Wennstr om, J. L., Bengazi, F. & Lekhom, U.
(1994) The influence of the masticatory mucosa
on the peri-implant soft tissue condition. Clini-
cal Oral Implants Research 5, 18.
Wilson, T. G. (2009) The Positive relationship
between excess cement and peri-implant dis-
ease: a prospective clinical endoscopic study.
Journal of Periodontology 80, 13881392.
Zigdon, H. & Machtei, E. E. (2008) The dimen-
sions of keratinized mucosa around implants
affect clinical and immunological parameters.
Clinical Oral Implants Research 19, 387392.
Zitzmann, N. U., Abrahamsson, I., Berglundh, T.
& Lindhe, J. (2002) Soft tissue reactions to pla-
que formation at implant abutments with dif-
ferent surface topography. An experimental
study in dogs. Journal of Clinical Periodontol-
ogy 29, 456461.
Zitzmann, N. U. & Berglundh, T. (2008) Defini-
tion and prevalence of peri-implant diseases.
Journal of Clinical Periodontology 35 (Suppl.
8), 286291.
Zitzmann, N. U., Berglundh, T., Marinello, C. P.
& Lindhe, J. (2001) Experimental peri-implant
mucositis in man. Journal of Clinical Periodon-
tology 28, 517523.
Address:
Stefan Renvert
Kristianstad University
291 88 Kristianstad, Sweden
E-mail: stefan.renvert@hkr.se
 Risk indicators for peri-implant mucositis S185

Clinical Relevance development of peri-implant mucosi- to design RCTs for identification

Scientific rationale for the study:
Evidence of risk indicators in the
aetiology of peri-implant mucositis
is scarce.
Principal findings: There is enough
evidence to suggest that plaque accu-
mulation at implants will result in
tis. Although evidence is weak, it
could be suggested that smoking can
lead to the development of peri-
implant mucositis. Peri-implant muco-
sitis was heterogeneously defined.
Principal implications: Due to ethical
and technical reasons, it is difficult
of certain risk factors. There is a
need for more adequately powered
prospective longitudinal studies to
identify biological, demographic
and behavioural variables which
may have an effect on the initiation
of peri-implant mucositis.

Appendix. STROBE Statement checklist of items that should be included in reports of observational studies
Item No Recommendation

Title and abstract 1 (a) Indicate the studys design with a commonly used term in the title or the abstract
(b) Provide in the abstract an informative and balanced summary of what was carried out and what
was found
Introduction
Background/rationale 2 Explain the scientific background and rationale for the investigation being reported
Objectives 3 State specific objectives, including any pre-specified hypotheses
Methods
Study design 4 Present key elements of study design early in the study
Setting 5 Describe the setting, locations and relevant dates, including periods of recruitment, exposure,
follow-up and data collection
Participants 6 (a) Cohort study Give the eligibility criteria, and the sources and methods of selection of
participants. Describe methods of follow-up
Casecontrol study Give the eligibility criteria, and the sources and methods of case
ascertainment and control selection. Give the rationale for the choice of cases and controls
Cross-sectional study Give the eligibility criteria, and the sources and methods of selection of
participants
(b) Cohort study For matched studies, give matching criteria and number of exposed and
unexposed
Casecontrol study For matched studies, give matching criteria and the number of controls per
case
Variables 7 Clearly define all outcomes, exposures, predictors, potential confounders and effect modifiers. Give
diagnostic criteria, if applicable
Data sources/ measurement 8* For each variable of interest, give sources of data and details of methods of assessment
(measurement). Describe comparability of assessment methods if there is more than one group
Bias 9 Describe any efforts to address potential sources of bias
Study size 10 Explain how the study size was arrived at
Quantitative variables 11 Explain how quantitative variables were handled in the analyses. If applicable, describe which
groupings were chosen and why
Statistical methods 12 (a) Describe all statistical methods, including those used to control for confounding
(b) Describe any methods used to examine subgroups and interactions
(c) Explain how missing data were addressed
(d) Cohort study If applicable, explain how loss to follow-up was addressed
Casecontrol study If applicable, explain how matching of cases and controls was addressed
Cross-sectional study If applicable, describe analytical methods taking account of sampling
strategy
(e) Describe any sensitivity analyses
Results
Participants 13* (a) Report numbers of individuals at each stage of study e.g. numbers potentially eligible,
examined for eligibility, confirmed eligible, included in the study, completing follow-up, and
analysed
(b) Give reasons for non-participation at each stage
(c) Consider use of a flow diagram
Descriptive data 14* (a) Give characteristics of study participants (e.g. demographic, clinical, social) and information
on exposures and potential confounders
(b) Indicate number of participants with missing data for each variable of interest
(c) Cohort study Summarize follow-up time (e.g. average and total amount)
Outcome data 15* Cohort study Report numbers of outcome events or summary measures over time
Casecontrol study Report numbers in each exposure category, or summary measures of
exposure
Cross-sectional study Report numbers of outcome events or summary measures

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
S186 Renvert and Polyzois

Appendix. (Continued)
Item No Recommendation

Main results 16 (a) Give unadjusted estimates and, if applicable, confounder-adjusted estimates and their precision
(e.g., 95% confidence interval). Make clear which confounders were adjusted for and why they
were included
(b) Report category boundaries when continuous variables were categorized
(c) If relevant, consider translating estimates of relative risk into absolute risk for a meaningful
time period
Other analyses 17 Report other analyses done e.g. analyses of subgroups and interactions, and sensitivity analyses
Discussion
Key results 18 Summarize key results with reference to study objectives
Limitations 19 Discuss limitations of the study, taking into account sources of potential bias or imprecision.
Discuss both direction and magnitude of any potential bias
Interpretation 20 Give a cautious overall interpretation of results considering objectives, limitations, multiplicity of
analyses, results from similar studies and other relevant evidence
Generalizability 21 Discuss the generalizability (external validity) of the study results
Other information
Funding 22 Give the source of funding and the role of the flinders for this study and, if applicable, for the
original study on which the present article is based
*
Give information separately for cases and controls in casecontrol studies and, if applicable, for exposed and unexposed groups in cohort
and cross-sectional studies.
An Explanation and Elaboration article discusses each checklist item and gives methodological background and published examples of trans-
parent reporting. The STROBE checklist is best used in conjunction with this article (freely available on the Web sites of PLoS Medicine at
http://www.plosmedicine.org/, Annals of Internal Medicine at http://www.annals.org/, and Epidemiology at http://www.epidem.com/). Infor-
mation on the STROBE Initiative is available at www.strobe-statement.org.

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd