You are on page 1of 6

J Clin Periodontol 2015; 42 (Suppl. 16): S152–S157 doi: 10.1111/jcpe.

12369

Primary prevention of peri- Søren Jepsen1, Tord Berglundh2,


Robert Genco3, Anne Merete Aass4,
Korkud Demirel5, Jan Derks2, Elena

implantitis: Managing Figuero6, Jean Louis Giovannoli7,


Moshe Goldstein8, France Lambert9,
Alberto Ortiz-Vigon6, Ioannis Polyz-

peri-implant mucositis ois10, Giovanni E. Salvi11, Frank Sch-


warz12, Giovanni Serino13, Cristiano
Tomasi2 and Nicola U. Zitzmann14
1
University of Bonn, Bonn, Germany;
2
University of Gothenburg, Gothenburg,
Jepsen S, Berglundh T, Genco R, Aass AM, Demirel K, Derks J, Figuero E,
Sweden; 3University at Buffalo, Buffalo, NY,
Giovannoli JL, Goldstein M, Lambert F, Ortiz-Vigon A, Polyzois I, Salvi GE, USA; 4University of Oslo, Oslo, Norway;
Schwarz F, Serino G, Tomasi C, Zitzmann NU. Primary prevention of peri- 5
Istanbul University, Istanbul, Turkey;
implantitis: managing peri-implant mucositis. J Clin Periodontol 2015; 42 (Suppl. 6
University of Complutense, Madrid, Spain;
16): S152–S157. doi: 10.1111/jcpe.12369. 7
Private Practice, Paris, France; 8Hadassah-
Hebrew University Medical Center,
Abstract Jerusalem, Israel; 9University of Liege, Liege,
Aims: Over the past decades, the placement of dental implants has become a rou- Belgium; 10Trinity College Dublin, Dublin,
tine procedure in the oral rehabilitation of fully and partially edentulous patients. Ireland; 11University of Bern, Bern,
However, the number of patients/implants affected by peri-implant diseases is Switzerland; 12Heinrich Heine University,
Du€sseldorf, Germany; 13Public Dental
increasing. As there are – in contrast to periodontitis – at present no established
Service Borås, Borås, Sweden; 14University
and predictable concepts for the treatment of peri-implantitis, primary prevention of Basel, Basel, Switzerland
is of key importance. The management of peri-implant mucositis is considered as
a preventive measure for the onset of peri-implantitis. Therefore, the remit of this
working group was to assess the prevalence of peri-implant diseases, as well as Sponsor representatives: Svetlana Farrell,
risks for peri-implant mucositis and to evaluate measures for the management of Proctor & Gamble, Mike Lynch, Johnson &
peri-implant mucositis. Johnson.
Methods: Discussions were informed by four systematic reviews on the current
epidemiology of peri-implant diseases, on potential risks contributing to the
development of peri-implant mucositis, and on the effect of patient and of profes-
sionally administered measures to manage peri-implant mucositis. This consensus
report is based on the outcomes of these systematic reviews and on the expert
opinion of the participants.
Results: Key findings included: (i) meta-analysis estimated a weighted mean prev-
alence for peri-implant mucositis of 43% (CI: 32–54%) and for peri-implantitis of
22% (CI: 14–30%); (ii) bleeding on probing is considered as key clinical measure
to distinguish between peri-implant health and disease; (iii) lack of regular sup-
portive therapy in patients with peri-implant mucositis was associated with
increased risk for onset of peri-implantitis; (iv) whereas plaque accumulation has
been established as aetiological factor, smoking was identified as modifiable
patient-related and excess cement as local risk indicator for the development of Key words: chemical plaque control;
peri-implant mucositis; (v) patient-administered mechanical plaque control (with mechanical plaque control; meta-analysis;
manual or powered toothbrushes) has been shown to be an effective preventive peri-implant mucositis; peri-implantitis;
primary prevention; secondary prevention;
measure; (vi) professional intervention comprising oral hygiene instructions and
systematic review
mechanical debridement revealed a reduction in clinical signs of inflammation;
(vii) adjunctive measures (antiseptics, local and systemic antibiotics, air-abrasive Accepted for publication 31 December 2014

Conflict of interest and source of funding


Funds for this workshop were provided by the European Federation of Periodontology in part through unrestricted educational
grants from Johnson & Johnson and Procter & Gamble. Workshop participants filed detailed disclosure of potential conflict of
interest relevant to the workshop topics and these are kept on file. Declared potential dual commitments included having
received research funding, consultant fees and speakers fee from: Colgate-Palmolive, Procter & Gamble, Johnson & Johnson,
Sunstar, Unilever, Philips, Dentaid, Ivoclar-Vivadent, Heraeus-Kulzer, Straumann.

S152 © 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Managing peri-implant mucositis S153

devices) were not found to improve the efficacy of professionally administered


plaque removal in reducing clinical signs of inflammation.
Conclusions: Consensus was reached on recommendations for patients with den-
tal implants and oral health care professionals with regard to the efficacy of mea-
sures to manage peri-implant mucositis. It was particularly emphasized that
implant placement and prosthetic reconstructions need to allow proper personal
cleaning, diagnosis by probing and professional plaque removal.

Dental implants supporting dental peri-implant mucositis is the precur- tis, and the effect of patient and pro-
restorations are part of the oral envir- sor to peri-implantitis, as is gingivitis fessionally administered measures to
onment of a significant proportion of for periodontitis, and that a contin- manage peri-implant mucositis. This
the population and thus, prevention uum exists from healthy peri-implant consensus report is based on four
of peri-implant diseases should be mucosa to peri-implant mucositis systematic reviews and on the expert
part of overall oral health care. There and to peri-implantitis. Therefore, opinion of the participants.
is great variation regarding the age of prevention of peri-implant diseases
patients treated with dental implants involves the prevention of peri-
Peri-implant Health and Disease –
and the type and extent of implant- implant mucositis and the prevention
Current Epidemiology
supported restorative procedures. of the conversion from peri-implant
Definitions of peri-implant dis- mucositis into peri-implantitis by In a systematic review, the preva-
eases were agreed upon at previous treatment of existing peri-implant lence, extent and severity of
European Workshops on Periodon- mucositis (Salvi & Zitzmann 2014). peri-implant diseases were assessed
tology (Lindhe & Meyle 2008, Lang The remit of this working group (Derks & Tomasi 2015).
& Berglundh 2011). The key parame- was to assess the current epidemiol- As case definitions varied, the
ter for diagnosis for peri-implant ogy of peri-implant diseases, poten- prevalence (based on subject-level)
mucositis is bleeding on gentle prob- tial risks contributing to the of peri-implant mucositis and peri-
ing (<0.25 N). It is assumed that development of peri-implant mucosi- implantitis ranged from 19 to 65%
© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
S154 Jepsen et al.

and from 1 to 47% respectively. of bone loss in peri-implantitis. function time of implants as a risk
Meta-analysis estimated a weighted Considerations should be given to indicator for peri-implant mucositis.
mean prevalence of peri-implant mu- the value of such severity indices.
cositis of 43% (CI: 32–54%) in 1196 Extent of disease must include pro- What are the local risk indicators for the
patients and 4209 implants. The portions of affected implants per development of peri-implant mucositis?
weighted mean prevalence of peri- patient in the presence of multiple
implantitis was 22% (CI: 14–30%), implants. Results from pre-clinical in vivo stud-
estimated in 2131 patients and 8893 ies failed to demonstrate an effect of
implants. Studies were performed in design and surface characteristics of
What is the risk for conversion from peri-
eight different countries in Europe, the trans-mucosal portion of implants
implant mucositis to peri-implantitis?
South and North America. on the development of peri-implant
The proportion of patients and There is emerging evidence on the soft tissue inflammation. The effect of
implants with healthy peri-implant patient level from a retrospective the dimensions of keratinized tissues
mucosa was not reported and could study that the lack of annual sup- (distance between peri-implant muco-
not be estimated from the presented portive therapy in patients diagnosed sal margin and the muco-gingival
data. Data on extent and severity of with peri-implant mucositis was junction) on the development of peri-
disease were rarely presented. Analy- associated with increased risk for implant mucositis is inconclusive.
sis in the review also revealed a posi- conversion of mucositis to peri-im- Some evidence exists indicating
tive relationship between prevalence plantitis (Costa et al. 2012). After that excess cement is a risk indicator
of peri-implantitis and function time 5 years, 18% of the patients comply- for peri-implant mucositis.
and a negative relationship between ing with supportive therapy pre-
prevalence of peri-implantitis and sented with peri-implantitis, while
the corresponding proportion in Efficacy of Measures to Manage Peri-
threshold for bone loss (i.e. smaller
patients who did not adhere to sup- implant Mucositis
prevalence data resulted when greater
bone loss was set as threshold). portive therapy was 43.9%. It is understood that patient-
The systematic review identified a administered measures are usually per-
number of shortcomings in the formed in conjunction with profes-
included studies. Case definitions Risk Indicators for Peri-implant sionally administered plaque removal
varied significantly. All studies were Mucositis procedures. For the purpose of this
based upon convenience samples of A risk factor is defined as “an envi- workshop, two systematic reviews
limited sample size and a variation ronmental, behavioural or biological were performed to evaluate the two
of follow-up. Estimates of prevalence factor that if present directly increases procedures separately. One study eval-
and incidence should ideally be made the probability of a disease occurring uated the efficacy of patient-adminis-
on randomly selected patient sam- and, if absent or removed reduces tered (Salvi & Ramseier 2015), and
ples of sufficient size and follow-up that probability” (Genco 1996). In another one the efficacy of profession-
time to ensure accuracy. the absence of studies fulfilling the ally administered measures (Schwarz
demands in the assessment of risk fac- et al. 2015) for plaque control in
tors, a systematic review evaluated patients with peri-implant mucositis.
What is the best clinical measure to
distinguish between peri-implant health
risk indicators for peri-implant muco-
and disease? sitis based on cross-sectional and pre-
What are effective ways to prevent peri-
clinical in vivo studies (Renvert & implant mucositis – “primary
Although bleeding on probing was a Polyzois 2015). Addressing aetiology, prevention”?
consistently used parameter in the seven experimental and two cross-
studies included in the systematic sectional studies demonstrated that At present, there are no studies
review, case definitions frequently plaque accumulation on implants available for the primary prevention
applied other parameters (e.g. prob- resulted in peri-implant mucositis. of peri-implant mucositis. This is in
ing depth) resulting in inconsistent The review assessed systemic/patient- contrast to the primary prevention
distinction between health and dis- related and local risk indicators for of gingivitis, in which documentation
ease. As bleeding on probing is an peri-implant mucositis. exists for frequency of complete pla-
indicator for inflammation in the que removal required to maintain
peri-implant mucosa, standardized gingival health (Lang et al. 1973).
sulcular or pocket probing assess- What are the systemic/patient-related risk
indicators for the development of peri-
ment should be considered as the
implant mucositis? What are effective ways of patient-
current clinical measure to distin-
performed plaque control in the
guish between peri-implant health Smoking was identified as an inde-
management of peri-implant mucositis?
and disease. pendent risk indicator for peri-
implant mucositis. A single study of In the systematic review on the effi-
limited size indicated that exposure cacy of patient-administered mea-
Is there a need for defining severity and
to radiation therapy was associated sures, eleven RCTs with a follow-up
extent of peri-implant disease?
with mucositis. One study identified from 3 to 24 months were included
The present review identified few diabetes as well as gender to be (Salvi & Ramseier 2015). Three
reports that presented information risk indicators for mucositis, while major groups of treatment were iden-
on frequencies of different degrees two cross-sectional studies described tified, i.e. mechanical plaque removal
© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Managing peri-implant mucositis S155

by means of manual or powered Professional intervention mainly level of the available scientific evi-
toothbrushes, chemical plaque con- comprised oral hygiene instructions, dence, but rather facilitate its under-
trol by means of adjunctive delivery mechanical debridement applying a standing. Recommendations (e.g.
of antimicrobials and triclosan-con- variety of different hand or powered PRISMA, MOOSE) for systematic
taining toothpastes. According to the instruments and/or polishing tools reviews including meta-analysis
consensus report of the VIII Euro- and revealed a reduction in clinical should be carefully considered.
pean Workshop (Sanz & Chapple signs of inflammation, while resolu- The reviews identified some limita-
2012), the endpoint of therapy and tion of BoP on the subject level was tions of the included studies. For epi-
primary outcome should be the reso- not achieved. demiological studies as well as studies
lution of peri-implant mucosal Adjunctive measures (antiseptics, on intervention, the main issues were
inflammation (frequency distribution local and systemic antibiotics, air- (i) the variation in case definition, (ii)
of resolved lesions) as determined by abrasive devices) were not found to the variation in sampling and sample
the absence of BoP. Although com- improve the efficacy of profession- size and (iii) the limited follow-up
plete resolution following patient- ally administered plaque removal in time. In addition, studies included in
administered measures was not reducing clinical signs of inflamma- the two reviews on management of
always reported, a reduction of clini- tion. peri-implant mucositis showed varying
cal signs of inflammation as second- risks of bias (according to the Cochra-
ary outcome was evident in all ne checklist). A lack of standard con-
studies. One study reported the per- Is Resolution of Peri-implant trol treatment for mucositis was
Mucositis Achievable?
centage of implants with complete apparent. Included studies assessed
resolution of peri-implant mucositis. Both systematic reviews demonstrated efficacy of interventions in highly con-
Manual brushing with or without that resolution of peri-implant mucosi- trolled clinical settings. Such studies
adjunctive chlorhexidine gel was tis is possible. However, current data may not allow the evaluation of effec-
investigated over 3 months and 38% also indicate that resolution of inflam- tiveness in general populations. Com-
of the patients/implants were found mation was not achieved in all patients. parisons of dichotomous and ordinal
with complete resolution of peri- Experimental peri-implant mucositis outcome variables were often based on
implant mucositis (Heitz-Mayfield was significantly reversed by profes- group averages rather than analysis of
et al. 2011). sionally administered plaque removal frequency distributions.
There were a variety of control and reinstitution of oral hygiene prac-
treatments that had been used for tices conducted over 3 weeks (Salvi Recommendations for Research
comparison indicating that there is a et al. 2012).
lack of an accepted standard of In a previous consensus report focus-
care. All studies were designed as ing on quality of reporting (Sanz &
What is the current standard of care for
parallel arm RCTs and six of 11 Chapple 2012) recommendations for
patient- and professionally administered
had an observation time of 6 plaque control for the management of
future research on epidemiology and
months, which is in line with the peri-implant mucositis? prevention of peri-implant diseases
recommendations given in a previ- were given. The present working
ous consensus (Sanz & Chapple Patient-administered mechanical pla- group strongly supports these previ-
2012). Study quality was analysed que control is an effective preventive ous recommendations. For epidemio-
according to the Cochrane collabo- measure. Chemical plaque control logical studies, establishment of
ration tool for assessing the risk of either by oral rinses or a dentifrice national/regional implant databases
bias, and only four of the 11 studies tested to date had limited adjunctive was advocated. Studies should be
achieved at least 80% of positive effect. Patient-administered mechani- adequately powered, randomly sam-
answers. Thus the results should be cal plaque control alone (with man- pled and consider sufficient follow-
interpreted with caution. ual or powered toothbrush) should up. Risk assessments should include a
be considered the current standard multiple-step process and aim at
of care. establishing causality by addressing
What are effective ways of professional
Professionally administered pla- criteria such as those proposed by
plaque control in the management of peri-
implant mucositis?
que control procedures should include Hill (1965).
regular (based on the individual The working group identified the
In the systematic review on the effi- needs) oral hygiene instructions and need for defining and reporting
cacy of professionally administered mechanical debridement employing peri-implant health (e.g. absence of
plaque removal, seven RCTs were different hand or powered instru- bleeding on probing) and incidence
included (48.6% revealing high risk ments with or without polishing tools. of disease from prospective cohort
of bias) mainly employing a parallel studies.
group design, and BoP reduction For intervention trials, appropriate
Limitations of Available Research
was defined as the primary outcome. endpoints, i.e. resolution of inflamma-
The definition of peri-implant muco- Meta-analysis was applied in two of tion at the given site, as well as the lack
sitis was heterogeneous among stud- the reviews presented in this working of standard control treatment were
ies but commonly included positive group (Derks & Tomasi 2015, Sch- identified as critical issues. Therapeutic
BoP at the respective sites. Case defi- warz et al. 2015). The group high- measures demonstrating efficacy in
nitions were not reported in two of lighted that meta-analytic methods properly designed RCT studies should
the studies evaluated. per se do not always strengthen the be evaluated in field studies. The com-
© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
S156 Jepsen et al.

parison of clinical parameters should mucosal margin to allow meticu- current epidemiology. J Clin Periodontol 2015;
42 (Suppl. 16): S158–S171.
be based on changes rather than abso- lous removal of excess cement.

Genco, R. J. (1996) Current view of risk factors
lute values. Data management should Clinicians have to be aware that for periodontal diseases. Journal of Periodontol-
consider multiple and multi-level logis- implant placement at a submuco- ogy 67, 1041–1049.
tic regression models to correctly sal level (to hide crown margins) Heitz-Mayfield, L. J., Salvi, G. E., Botticelli, D.,
address binary and ordinal data. may carry a higher risk for peri- Mombelli, A., Faddy, M., Lang, N. P. Implant
complication research group. (2011) Anti-infec-
Areas of interest for future implant diseases. tive treatment of peri-implant mucositis: a
research are as follows: • To facilitate personal oral randomised controlled clinical trial. Clinical
hygiene, clinicians should con- Oral Implants Research 22, 237–241.
• Primary prevention of peri- sider having keratinized attached Hill, A. B. (1965) The environment and disease:
association or causation? Proceedings of the
implant mucositis and unmovable tissue surround- Royal Society of Medicine 58, 295–300.
• Risk assessment ing the transmucosal implant Lang, N. P., Cumming, B. R. & L€ oe, H. (1973)
• Importance of attached/kerati- portion already during implant Toothbrushing frequency as it relates to plaque
development and gingival health. Journal of
nized tissue placement (for one-stage implant
• Efficacy of interproximal cleaning placement) or during abutment Periodontology 44, 396–405.


Lang, N. P., Berglundh, T. & Working Group 4
Further evaluation of adjunctive connection (for two-stage implant of Seventh European Workshop on P. Periim-
measures placement). plant diseases: where are we now? Consensus
• Individualized supportive therapy • Since infection control is essential of the Seventh European Workshop on Peri-
odontology. Journal of Clinical Periodontology
in the prevention of peri-implant
2011;38 (Suppl 11):178–181.
diseases, patients have to be Lindhe, J., Meyle, J. & Group D EWoP. Peri-
instructed on their personal oral implant diseases: Consensus Report of the Sixth
Recommendations for Dental
hygiene with regular monitoring European Workshop on Periodontology. Jour-
Professionals nal of Clinical Periodontology 2008;35:282–285.
and reinforcement.
According to the present data, peri- • Implant position should be
Renvert, S. & Polyzois, I. (2015) Risk indicators
for peri-implant mucositis. A systematic litera-
implant diseases are very common. selected and suprastructures ture review. J Clin Periodontol 2015; 42 (Suppl.
Therefore, it is imperative for the cli- should be designed in a way 16): S172–S186.
nician to examine and evaluate facilitating sufficient access for Salvi, G. E., Aglietta, M., Eick, S., Sculean, A.,
Lang, N. P. & Ramseier, C. A. (2012) Reversibil-
patients who have been provided regular diagnosis by probing as ity of experimental peri-implant mucositis com-
with implant-supported restorations well as for personal and profes- pared with experimental gingivitis in humans.
on a regular basis. The following sional oral hygiene measures. Clinical Oral Implants Research 23, 182–190.
aspects are recommended for the • Professional supportive care Salvi, G. E. & Zitzmann, N. U. (2014) The effects
of anti-infective preventive measures on the
clinical routine: should be established according occurrence of biologic implant complications
to the individual needs of the and implant loss: a systematic review. Interna-
• When implant treatment is consid- patient (e.g. 3-, 6- or 12-month tional Journal of Oral & Maxillofacial Implants
ered, patients should be informed recall intervals) and their compli- 29 (Suppl), 292–307.
Salvi, G. & Ramseier, C. (2015) Efficacy of patient-
on the risks for biological compli- ance has to be confirmed.

administered mechanical and/or chemical pla-
cations (peri-implant diseases) and Particularly in patients with a que control protocols in the management of
the need for preventive care. history of treated aggressive peri-implant mucositis. A systematic review. J
• An individual risk assessment periodontitis indicating an incre- Clin Periodontol 2015; 42 (Suppl. 16): S187–
S201.
including systemic and local risk ased susceptibility for periodontal
Sanz, M., Chapple, I. L. & Working Group 4 of
indicators should be performed and peri-implant diseases, shorter the VIII European Workshop on Periodontol-
and modifiable risk factors, such recall intervals should be ogy. Clinical research on peri-implant diseases:
as residual increased probing considered. consensus report of Working Group 4. Journal
pocket depth in the remaining • During recall peri-implant tissues of Clinical Periodontology 2012;39 (Suppl 12):
202–206.
dentition or smoking, should be must be regularly examined Schwarz, F., Becker, K. & Sager, M. (2015) Effi-
eliminated. Hence, treatment of including probing assessments cacy of professionally-administered plaque
periodontal disease aiming for with special emphasis on bleeding removal with or without adjunctive measures
elimination of residual pockets on probing. for the treatment of peri-implant mucositis. A
systematic review and meta-analysis. J Clin
with bleeding on probing and Periodontol 2015; 42 (Suppl. 16): S201–S212.
smoking cessation should precede
implant placement References
• The correct fit of implant compo- Costa, F. O., Takenaka-Martinez, S., Cota, L. O.,
Address:
Søren Jepsen
nents and the suprastructure has Ferreira, S. D., Silva, G. L. & Costa, J. E.
(2012) Peri-implant disease in subjects with and Department of Periodontology, Operative
to be ensured to avoid additional and Preventive Dentistry
without preventive maintenance: a 5-year follow-
niches for biofilm adherence. If up. Journal of Clinical Periodontology 39, 173– University of Bonn
cemented implant restorations 183. Welschnonnenstr. 17, 53111 Bonn, Germany
have been selected, the restoration Derks, J. & Tomasi, C. (2015) Peri-implant E-mail: jepsen@uni-bonn.de
margins should be located at the Health and Disease. A systematic review of

© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Managing peri-implant mucositis S157

Clinical relevance Plaque accumulation is an aetiologi- Conclusions: Successful manage-


Background: In the absence of estab- cal factor and smoking and excess ment of peri-implant mucositis
lished and predictable treatment cement are modifiable risk indictors should comprise proper diagnosis
concepts for peri-implantitis, pre- for the development of peri-implant by regular probing as well as effec-
vention is of uppermost importance. mucositis. Both patient- and profes- tive self-performed and supportive
Principal findings: Peri-implant dis- sionally administered mechanical professional plaque removal.
eases are highly prevalent. Bleeding measures for plaque removal are
on probing can distinguish between effective for the reduction of inflam-
peri-implant health and disease. mation in the peri-implant mucosa.

© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

You might also like