Content uploaded by Craig W Barclay
Author content
All content in this area was uploaded by Craig W Barclay
Content may be subject to copyright.
October 2010 DentalUpdate 511
RestorativeDentistry
Peter Heasman
Peri-Implant Diseases
Abstract: Peri-implant diseases are inflammatory conditions that affect the soft and hard supporting tissues around implant fixtures.
Peri-implant mucositis usually responds to oral hygiene instructions, scaling and prophylaxis, but peri-implantitis, which involves bone
resorption, has less predictable treatment outcomes following non-surgical management. Adjunctive treatment for decontaminating sites
may include the use of antimicrobials and resistant cases may sometimes be managed with a surgical approach.
Clinical Relevance: As dental implant-retained prostheses become more popular the prevalence of peri-implant complications will also
increase. Dental practitioners and care professionals should appreciate their potential roles in the management of these conditions.
Dent Update 2010; 37: 511–516
Osseointegrated implant-retained
restorations and prostheses have become
a predictable treatment modality for
replacing missing teeth. An estimated
one million endosseous dental implants
are placed annually worldwide and
approximately 110 different manufacturers
now produce over 440 implant brands.1
Sales of dental implants and abutments
rise by 15% annually with a projected
worldwide market sale of $2 billion by
2010.2 In Europe, between 1995 and 2005,
21 million dental implants were placed
with the clinical need resulting from an
increasing population of older patients, an
estimated 770 million people missing one
or more teeth by the age of 65, around 20
million edentulous people and changing
patient preferences.3
The long-term success of
dental implants is dependent upon regular
follow-up and maintenance regimes
and, as dental implants become more
prevalent, the responsibility for providing
this maintenance care will fall increasingly
on the general dental practitioner. This
article aims to leave the practitioner better
informed about the potential problems
that may be encountered during follow-up
of patients with dental implants, how they
may be diagnosed, and the options for
clinical management.
Peri-implant disease
Dental implants, like natural
teeth, are susceptible to inflammatory
diseases that are predominantly driven by
the accumulation of dental plaque. These
conditions are categorized into those that
are limited to the peri-implant soft tissues
(peri-implant mucositis) and those that
also affect the alveolar bone support (peri-
implantitis).
Peri-implant mucositis
Peri-implant mucositis is a
reversible, inflammatory lesion affecting
the marginal soft tissues that surround
Peter Heasman, BDS, MDS, PhD,
FDS RCPS(Glasg), MRD RCS(Edin),
Professor of Periodontology, School of
Dental Sciences, Newcastle University,
Newcastle, NE2 4BW, Zaid Esmail, BDS,
MFDS RCS(Edin), General Professional
Trainee, Newcastle Dental Hospital,
NE2 4AZ and Craig Barclay, BDS, FDS
RCPS(Glasg), DRD RCS(Edin), MRD
RCS(Edin), MPhil, PhD, Consultant
in Restorative Dentistry, Associate
Postgraduate Dean for Specialist Training,
University Dental Hospital of Manchester,
Higher Cambridge Street, Manchester,
M15 6FH.
osseointegrated dental implants but
does not involve the resorption of the
supporting bone (Figure 1a). This condition
corresponds to gingivitis around natural
teeth and presents as redness and swelling
of the soft tissues. Bleeding on probing is
the clinical sign that confirms diagnosis
(Figure 1b).4,5 As with chronic gingivitis,
a necrotizing ulcerative condition may
develop when risk factors such as smoking
are present.
Peri-implantitis
Peri-implantitis is an
inflammatory lesion that affects the
supporting bone as well as the surrounding
soft tissues of a functioning implant.4-6
This condition broadly corresponds to
periodontitis around the natural teeth. In
addition to bleeding on probing, affected
sites may exude pus (Figure 1c) and are
always accompanied by marginal bone
loss (Figure 1d). To distinguish pathological
bone resorption from physiological
remodelling of the alveolar crest the loss of
bone height should involve ≥ 3 threads of
the implant fixture (1.8 mm) following the
first year in function.7
Prevalence
Although there are few long
term data on the prevalence of peri-implant
Zaid Esmail and Craig Barclay
RestorativeDentistry
512 DentalUpdate October 2010
diseases, those data that are available are
relatively consistent. Cross-sectional studies
of implants that have been in function for
9 years or more suggest that peri-implant
mucositis affects approximately 50%
of implants and 80% of patients;7 peri-
implantitis, again for implants that have
been in function for 9–11 years, affects
28–56% of patients and 12–43% of implant
sites.6-8 Whilst these data clearly indicate
a need for sustained supportive care, it is
reassuring to observe that overall survival
rate over the same period is around 96%.
Of the implants that are lost, the majority
fail early, either before placement of the
suprastructure, or within the first year of
loading.9
Identifying patients at risk
For patients with periodontal
diseases it is crucial that associated
risk factors are identified, modified or
eliminated if the benefit of treatment is to
be maximized. The same strategy applies
to patients with peri-implant diseases and,
although it might be anticipated that risk
factors are addressed adequately before the
placement of implants, this may not always
be the case. Patients who are unable to
achieve a good standard of plaque control
are at increased risk of peri-implant disease
with an odds ratio of 2.9 for peri-implant
mucositis and 14.3 for peri-implantitis,10
and the association between plaque and
disease is ‘dose-dependent’. The ability of
patients to clean effectively around implant
fixtures, however, may not be assumed
from their ability to achieve a high standard
of plaque control around the natural
dentition.11 Therefore careful instruction in
plaque control measures around implants
in the immediate post-placement period is
essential.
There is also an increased
prevalence of peri-implantitis in
patients with a history of periodontitis
when compared to non-periodontitis
patients,12,13 although the extent to which
this might impact on overall implant
survival in the long-term is unclear.14,15
A history of periodontitis does not
preclude the placement of implants, but
the disease should be stabilized with
high level maintenance to minimize the
opportunity for periodontal pathogens
from periodontally-active sites to colonize
peri-implant tissues.16 It is important to
appreciate, however, that the risk for
peri-implant infection is still present even
when implants are placed in edentulous
patients; an implant will still provide a
favourable ecological niche for colonization
by commensal oral bacteria.17 Indeed,
a number of bacterial species such as
Peptostreptococcus stomatitis, Mycoplasma
salivarium and Pseudoramibacter
alactolyticus, that are not linked with
healthy implant sites or periodontal disease,
have been identified at sites of peri-
implantitis.18
Smoking is a known risk factor
for periodontal diseases and there is a
substantial evidence base of long-term
studies that implicate the habit as a risk
factor for peri-mucositis, peri-implantitis
and total implant failure.12,19,20 These
associations have been substantiated
unequivocally by systematic review and
meta-analysis20 and, whilst there are few
data to suggest otherwise, it must be
assumed that cigarette smoking will impact
negatively on attempts both to prevent and
manage peri-implant disease in the long-
term.
Diagnosis of peri-implant
disease
Clinical assessment
Visual assessment alone will
reveal an inflamed gingival cuff, although
scar reactions in the soft tissues, for
example after bone grafting and tissue
manipulation, may mask inflammatory
reactions of the mucosa. Probing is essential
and may be undertaken circumferentially
or at four sites around an implant fixture. A
plastic (TPS or WHO 621) probe has greater
flexibility than a metal counterpart, may
cause less contamination and damage
to the implant surface, and is potentially
more accurate as it can adapt more readily
to the abutment-suprastructure junction
(Figure 2). A light probing force of around
0.15–0.2N is recommended;21 the absence
of gingival connective tissue fibres attached
to the implant surface means that there
is minimal resistance to probing. In the
presence of peri-implantitis there is an
extensive, unencapsulated neutrophil
infiltrate and the periodontal probe is
likely to penetrate the entire depth of the
a
b
c
d
Figure 1. (a) Peri-implant mucositis: gingival
inflammation and enlargement around two
mandibular implants. (b) Clinical appearance of
peri-implantitis with circumferential inflammation
around the implant at the LR3 site. (c) Clinical
appearance of peri-implantitis with suppuration
at the mesial buccal site after gentle probing with
TPS plastic probe. Note how the flexibility of the
probe allows it to follow closely the contour of
the crown and the long axis of the implant fixture.
(d) Radiographic appearance of fixture seen in
(b). There is extensive bone loss on the mesial
and distal surfaces of the fixture. In situ, the bone
involvement affected the entire circumference of
the fixture.
RestorativeDentistry
514 DentalUpdate October 2010
soft tissues and extend to the level of the
alveolar bone.22
Bleeding following gentle
probing is the characteristic sign for
peri-implant mucositis and suppuration
following probing is indicative of peri-
implantitis. Probing depth may be
influenced by the implant system and the
suprastructure used: a gingival cuff with
a probing depth of 5 mm but with no
bleeding on probing may be consistent
with health. If initial probing depths are
recorded about one month after implant
placement, then future measurements,
recorded for example on an annual basis,
can be compared to the baseline record.
Any mobility within a year of
placing an implant and/or its suprastructure
is more likely to be a sign of lack of
osseointegration, fracture of the implant or
mobility and fracture of the suprastructure
rather than an early sign of peri-implantitis.
The only reliable method for assessing
mobility (other than for a single tooth
implant) is to dismantle the suprastructure
so that the implant fixture(s) can be
assessed independently. Late mobility of a
successfully integrated implant, however,
may be an additional sign of advanced or
progressing peri-implantitis.
Radiographic assessment
High quality, long cone
periapical radiographs are the films of
choice for assessing implant fixtures. The
ideal exposure will reveal the external
configuration of the implant and the thread
profile is likely to be visible unless there
is a vertical discrepancy of ≥ 15° from the
perpendicular between the beam and the
film surface.23 The normal bone density
around osseointegrated fixtures was
described originally as having perifixtural
trabeculations radiating from the implant
surface24 and radiographic evidence of
a bone trough extending apically to the
first thread may be consistent with health
being a manifestation of bone remodelling
and re-establishment of the biologic width
of peri-implant tissues. A radiographic
observation of bone resorption mesial and
distal to the implant of ≥ 3 threads will
confirm a diagnosis of peri-implantitis.7 If
a ‘baseline’ radiograph is taken at the time
of placement of the suprastructure, then
further films can be exposed at 6 and 12
months at the time of greatest remodelling
of bone and when complications are most
prevalent, and then at 2-3 year intervals
thereafter. More frequent exposures on
an annual basis are indicated when there
are persistent clinical signs of peri-implant
disease and when there is an increased risk
of complications, such as when implants
are placed in a patient with a history of
periodontal disease. It must, however,
always be remembered that this type of
radiography is purely two dimensional
and therefore gives no indication as to any
potential buccal bone loss that may have
occurred.
Treatment of peri-implant
disease
Comprehensive reviews25,26 of
the treatment of peri-implant diseases have
made important conclusions:
n That mechanical, non-surgical therapy
may be effective in the treatment of peri-
implant mucositis and that the adjunctive
use of antimicrobial mouthrinses may
enhance the clinical outcomes;
n That non-surgical therapy for peri-
implantitis is not a predictable treatment
even with adjunctive chlorhexidine
mouthrinse. Adjunctive local or systemic
antibiotics , however, may be effective in
reducing probing depths and resolving
bleeding on probing;
n Adjunctive Listerine mouthrinse can
reduce dental plaque and marginal
bleeding and may provide some benefit in
the management of peri-implant mucositis.
The relatively superficial
nature of peri-implant mucositis is the
most likely reason that this condition
responds favourably to intensive oral
hygiene instruction, scaling, prophylaxis
and mouthrinsing with chlorhexidine.
As lesions develop, however, their local
anatomy, the complex morphology of
the exposed fixture and the profile of
suprastructure-implant fixture design will
inevitably compromise the ability of the
clinician to debride the site effectively and
the ability of the patient to maintain the
area free from dental biofilm (Figure 3).27
Mechanical, non-surgical treatment (using
specifically designed titanium curettes
and the Vector ultrasonic system with tips
designed for treatment around dental
implants) is effective in reducing dental
plaque deposits and soft tissue bleeding,
although the effects on probing depths and
the pathogenic subgingival microflora are
limited.27 Titanium curettes are less likely
than conventional instruments to alter
or damage the implant surface, but their
restricted ability to ‘work’ horizontally and
circumferentially between the threads on
the part of a fixture exposed through peri-
implantitis will limit effectiveness. Similarly,
Figure 2. Plastic TPS probe that can be used for
probing around dental implants. The flexibility of
the probe may enable more precise probing of
irregular defects than would a metal probe.
Figure 3 (a) Gross deposits of plaque and calculus
on an implant-retained bar. (b) The resultant
inflammation and massive gingival overgrowth
caused by the inability of the patient to clean the
suprastructure effectively.
a
b
October 2010 DentalUpdate 515
RestorativeDentistry
plastic manual instruments which may
be useful for scaling in the supragingival
environment may be less effective when
attempting to remove deposits from
between the threads (Figure 4).
Because of the problem with
access to the affected part of the fixture,
the Implantic Debrider™ has been recently
introduced (Figure 5a). This rotatory
instrument cleans down to the titanium
surface between the threads of the exposed
fixture at 400 rpm with copious water
cooling, but the suprastructure must be
dismantled to allow access (Figure 5b).
Er-YAG Lasers have also been
used for decontaminating peri-implantitis
affected implant surfaces,28,29 but again,
access has proven challenging and the
outcome data from relatively small studies
have yet to demonstrate significant
benefit when compared to conventional
mechanical therapy.25 Ultrasonic
instruments with plastic tips (SoftTip™,
Dentsply PA, USA) are also conceptually
attractive for use on implant surfaces
and, although their efficacy in removing
deposits from affected surfaces has yet
to be determined, there is evidence to
suggest that they inflict far less damage on
the titanium surface than do conventional
metal ultrasonic instruments (Figure 6).30
The objective of treatment of
peri-implantitis is to reduce or eliminate the
bacterial load and so allow healing to occur.
When there is evidence of bone cratering
and thread exposure, and when mechanical
therapy alone may be effective, then
adjunctive antimicrobial therapy may be an
option. Minocycline microspheres (Arestin®,
Orapharma, Johnson and Johnson) adhere
to the walls of peri-implant pockets and are
retained in high enough concentrations to
be effective against biofilm. They appear
to be a valuable adjunct to mechanical
debridement in patients with peri-
implantitis.31,32
When peri-implantitis sites
appear to be unresponsive to non-surgical
management, pockets continue to bleed
or suppurate and there is bone loss of
≥2mm (involving 3 or more threads of the
implant fixture), then referral to a specialist
may be indicated for consideration of a
surgical approach to achieve better access
for decontamination, and perhaps consider
regenerative procedures in the longer term.
Peri-implant supportive care
It is crucial that any patient with
an implant-retained prosthesis is enrolled
into an individually-tailored programme of
supportive care, with the emphasis being
on a preventive approach to potential
peri-implant problems and early diagnosis
of developing peri-implant disease.
Risk assessment should be ongoing, for
example to establish smoking status (has
an ex-smoker relapsed?) and the overall
maintenance of patients who have a
history of periodontal disease. The design
of suprastructures should facilitate oral
hygiene practices and the use of soft bristle
toothbrushes (manual or powered) should
be reviewed. Single-tufted, interspace
brushes, and interdental tape and brushes
with plastic-coated wire hubs are essential
for cleaning around fixtures and beneath
the suprastructure. Scaling and prophylaxis
should be undertaken with plastic manual
or ultrasonic instruments with a view
to minimizing the deposit of calculus,
disrupting and removing biofilm and
ensuring an environment that is consistent
with peri-implant health.
Conclusion
Peri-implant diseases are
likely to become more prevalent as the
popularity of implant-retained prostheses
continues to increase. Prevention is the
optimal strategy but early identification of
peri-implant complications is essential if
inflammation in the supporting soft tissues
is to be resolved. Peri-implantitis, however,
is a more challenging condition and
Figure 4. Plastic scaling instruments are effective
supragingivally but may be less effective in
removing hard deposits from within exposed
threads of implants.
Figure 5. (a) The Implantic Debrider™ designed
to remove deposits from exposed threads of
implants affected by peri-implantitis. Reproduced
by kind permission of Dr Jan Nilsson, Implantic.
www.implantic.com (b) The Implantic Debrider™
in vivo. (Reproduced by kind permission of Dr Jan
Nilsson, Implantic. www.implantic.com)
a
b
Figure 6. Ultrasonic handpiece with SoftTip™
plastic tips which are an attractive option to hand
instruments for scaling around dental implants.
(Reproduced by kind permission of Dentsply
PA, USA.)
RestorativeDentistry
516 DentalUpdate October 2010
treatment success may be unpredictable.
Nevertheless, a conventional, non-surgical
approach should be attempted.
References
1. Barclay CW, Michelinakis G. Implant
recognition system. Int Dent J 2006; 56:
1–6. Also at: http://www.whichimplant.
com [Accessed 23.08.10].
2. Implant-Based Dental Reconstruction.
The Worldwide Dental Implant
and Bone Graft Market. Kalorama
Information. Available at: http://
www.medicalnewstoday.com/
articles/29693.php [Accessed 03.08.10].
3. Millennium 2005 DF estimates. Personal
communication, Dentsply UK Ltd,
Addlestone, UK.
4. Lindhe J, Meyle J. Peri-implant diseases:
Consensus Report of the Sixth European
Workshop on Periodontology. J Clin
Periodontol 2008; 35: 282–285.
5. Albrektsson T, Isidor F. Implant therapy.
In: Proceedings of the First European
Workshop of Periodontology. Lang NP,
Karring T, eds. Berlin: Quintessence,
1994; pp.365–369.
6. Zitzmann NU, Berglundh T. Definition
and prevalence of peri-implant diseases.
J Clin Periodontol 2008; 35: 286–291.
7. Roos-Jansåker A-M, Lindahl C,
Renvert H, Renvert S. Nine- to fourteen-
year follow-up of implant treatment.
Part II: Presence of peri-implant lesions.
J Clin Periodontol 2006; 33: 290–295.
8. Fransson C, Lekholm U, Jemt T,
Berglundh T. Prevalence of subjects with
progressive bone loss at implants. Clin
Oral Implant Res 2005; 16: 440–446.
9. Roos-Jansåker A-M, Lindahl C, Renvert H,
Renvert S. Nine- to fourteen-year follow-
up of implant treatment. Part I: Implant
loss and associations to various factors.
J Clin Periodontol 2006; 33: 283–289.
10. Ferreira SD, Silva GMN, Cortelli JR,
Costa FO. Prevalence and risk variables
for peri-implant disease in Brazilian
subjects. J Clin Periodontol 2006; 33:
929–935.
11. Serino G, Ström C. Peri-implantitis
in partially edentulous patients:
association with inadequate plaque
control. Clin Oral Implant Res 2009; 20:
179–174.
12. Roos-Jansåker A-M, Renvert H, Lindahl C,
Renvert S. Nine- to fourteen-year follow-
up of implant treatment. Part III: Factors
associated with peri-implant lesions. J
Clin Periodontol 2006; 33: 296–301.
13. Schou S. Implant treatment in
periodontitis-susceptible patients: a
systematic review. J Oral Rehabil 2008;
35: 9–22.
14. Karoussis IK, Salvi GE, Heitz-Mayfield LIA,
Brägger U, Hämmerle CHF, Lang NP.
Long-term implant prognosis in patients
with and without a history of chronic
periodontitis: a 10-year prospective
cohort study of the ITI dental implant
system. Clin Oral Implant Res 2003; 14:
329–339.
15. Schou S, Holmstrup P, Worthington HV,
Esposito M. Outcome of implant therapy
in patients with previous tooth loss due
to periodontitis. Clin Oral Implant Res
2006; 17: 104–123.
16. van Winkelhoff AJ, Goené RJ,
Benschop C, Folmer T. Early colonisation
of dental implants by putative
periodontal pathogens in partially
edentulous patients. Clin Oral Implant
Res 2000; 11: 511–520.
17. Renvert S, Roos-Jansåker A-M, Lindahl
C, Renvert H, Persson GR. Infection at
titanium implants with or without a
clinical diagnosis of inflammation. Clin
Oral Implant Res 2007; 18: 509–516.
18. Koyanagi T, Sakamoto M, Takeuchi Y,
Ohkuma M, Izumi Y. Analysis of the
microbiota associated with peri-
implantitis. Available at: http://
iadr.confex.com/iadr/2010barce/
webprogram/Paper138742.html
[Accessed 03.08.10].
19. Lindquist LW, Carlsson GE, Jemt T.
Association between marginal bone loss
around osseointegrated mandibular
implants and smoking habits. J Dent Res
1997; 76: 1667–1674.
20. Strietzel FP, Reichart PA, Kale A,
Kulkarni M, Wegner B, Küchler I.
Smoking interferes with the prognosis
of dental implant treatment: a
systematic review and meta-analysis.
J Clin Periodontol 2007; 34: 523–544.
21. Gerber J, Tan W, Balmer T, Salvi G,
Lang NP. Bleeding on probing (BOP)
and pocket probing depth in relation to
probing pressure and mucosal health
around implants. Clin Oral Implant Res
2009; 20: 75–78.
22. Schou S, Holmstrup P, Stoltze K,
Hjørting-Hansen E, Fiehn N-E,
Skoygaard LT. Probing around implants
and teeth with healthy or inflamed peri-
implant mucosa/gingiva: a histologic
comparison in cynomolgus monkeys
(Macaca fascicularis). Clin Oral Implant
Res 2002; 13: 113–126.
23. Sewerin IP.
Comparison of radiographic
image characteristics of Brånemark and
IMZ implants. Clin Oral Implant Res 1991;
2: 151–156.
24. Brånemark P-I, Zarb G, Albrektsson T.
In: Tissue Integrated Prostheses:
Osseointegration in Clinical Dentistry.
Chicago: Quintessence Publishing, 1985.
25. Renvert S, Roos-Jansåker A-M, Claffey, N.
Non-surgical treatment of peri-implant
mucositis and peri-implantitis: a
literature review. J Clin Periodontol 2008;
35: 305–315.
26. Roos-Jansaker A-M, Renvert S,
Egelberg J. Treatment of peri-implant
infections: a literature review. J Clin
Periodontol 2003; 30: 467–485.
27. Renvert S, Samuelsson E, Lindahl C,
Persson GR. Mechanical non-surgical
treatment of peri-implantitis: a double-
blind randomized longitudinal clinical
study. I: Clinical results. J Clin Periodontol
2009; 36: 604–609.
28. Schwartz F, Bieling K, Bonsmann M,
Latz T, Becker J. Nonsurgical treatment
of moderate and advanced peri-
implantitis lesions: a controlled clinical
study. Clin Oral Invest 2006; 10: 279–288.
29. Schwartz F, Bieling K, Nuesry E,
Sculean A, Becker J. Clinical and
histological healing pattern of peri-
implantitis lesions following non-
surgical treatment with an Er:YAG Laser.
Lasers Surg Med 2006; 38: 663–671.
30. Mann M, Walmsley AD, Lea S. Analysis
of implant surface damage due to
ultrasonic scaler instrumentation.
Available at: http://iadr.confex.
com/iadr/2010barce/webprogram/
Paper40516.html [Accessed 03.08.10].
31. Renvert S, Lessem J, Dahlén G, Renvert
H, Lindahl C. Mechanical and repeated
antimicrobial therapy using a local drug
delivery system in the treatment of peri-
implantitis – a randomized clinical trial.
J Periodontol 2008; 79: 836–844.
32. Salvi G, Persson R, Heitz-Mayfield LIA,
Lang NP. Adjunctive local antibiotic
therapy in treatment of peri-implantitis.
II: Clinical and radiographic outcomes.
Clin Oral Implant Res 2007; 18: 281–285.