2010 John Wiley & Sons A/S
Periodontology 2000, Vol. 53, 2010, 167–181
Printed in Singapore. All rights reserved
PERIODONTOLOGY 2000
Comparative biology of chronic
and aggressive periodontitis vs.
peri-implantitis
L I S A J. A. H E I T Z -M A Y F I E L D & N I K L A U S P. L A N G
Peri-implant disease following successful integration
of an endosseous implant is the result of an
imbalance between the bacterial challenge and the
host response. Peri-implant diseases may affect the
peri-implant mucosa only (peri-implant mucositis)
or also involve the supporting bone (peri-implantitis) (112).
In the 6th European Workshop on Periodontology
in 2008, the definitions of peri-implant diseases were
revised as follows: peri-implant mucositis is the
presence of inflammation in the mucosa at an implant with no signs of loss of supporting bone; and
peri-implantitis, in addition to inflammation in the
mucosa, is characterized by the loss of supporting
bone (57).
For the purpose of this review, these two diseases
are compared with their counterparts around teeth
(i.e. gingivitis and periodontitis) without any consideration of the classification of periodontitis
(chronic and aggressive). The question therefore
arises: ÔAre periodontitis and peri-implantitis fundamentally different from the perspectives of etiological
aspects, pathogenesis aspects, risk assessment and
therapy?Õ
Etiological aspects (human studies)
Colonization (dynamics and surfaces)
In the late 1980s, the colonization of oral implants in
edentulous patients was studied using culture techniques. It was demonstrated that 1 week after
implant placement, a microbiota characterized
predominantly by gram-positive, facultative organ-
isms was established and maintained throughout the
duration of the study (6 months), with the exception
of one implant that showed suppuration after
3 months. At this particular site the subgingival
microbial community changed continuously within
the preceding months from a gram-positive
facultative microbiota to one rich in anaerobic
gram-negative bacteria (71).
In recent years, studies have focused on the
colonization of implants in partially edentulous
individuals (Figs. 1A–C). It was shown that bacterial
colonization occurred immediately following transmucosal implant placement (30 min) (29) and was
stable after 2 weeks (29, 82, 83). Moreover, the composition of the microbiota present after 3 months was
shown to be predictive for the colonization after
1 year (91). In addition, it was recognized that the
composition of the biofilms established on the implant surfaces corresponded closely to those identified from teeth surrounded by healthy tissues. Hence,
it can be anticipated that the microbiota present in
the oral cavity may have a substantial impact on
biofilm formation on newly placed implants.
Microbiota associated with healthy
peri-implant tissues
The microbiota associated with healthy peri-implant
tissues has been identified in many cross-sectional
studies that have generally characterized the
composition as being dominated by gram-positive
facultative cocci and rods (20, 29, 55). However,
gram-negative anaerobic rods may also be found in
small numbers and in low proportions at some implants.
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Heitz-Mayfield & Lang
A
B
C
Fig. 1. (A) Scanning electron micrograph of a titanium
abutment surface exposed to the oral cavity for 2 h,
illustrating attachment to the surface of single cocci on a
pellicle (fuzzy structure). Magnification: ·4500. (Figure
reproduced courtesy of Dr S. Abati, University of Milan,
Italy; unpublished.) (B) Scanning electron micrograph of a
titanium abutment surface exposed to the oral cavity for
1 week, illustrating early biofilm formation. Colonies of
cocci and rods in a glycocalyx matrix form an advancing
front attached to the surface. Magnification: ·1900. (Fig-
Microbiota associated with peri-implant
infections
Association studies have identified a microbiota
characterized by high counts and proportions of
gram-negative anaerobic bacteria around implants
with clinical signs of peri-implantitis. These studies
have found a high prevalence of pathogens associated with periodontitis (2, 9, 15, 16, 52, 66, 69, 71, 101,
104), which included members of the red complex
species (Porphyromonas gingivalis, Treponema denticola and Tannerella forsythia) and orange complex
species (Fusobacterium sp. and Prevotella intermedia), as defined by Socransky et al. (102). The presence of Aggregatibacter actinomycetemcomitans has
also been reported at peri-implantitis sites (39, 110).
A number of studies have also reported an association between the presence of Staphylococcus aureus,
enteric rods and Candida albicans, and periimplantitis (7, 15, 47, 55, 84, 90).
Intra-individual transmission of
pathogens
The similarity between the composition of the microbiota around teeth and implants within the same
subject has clearly been demonstrated (3, 46, 53, 70,
168
ure reproduced courtesy of Dr S. Abati, University of Milan, Italy; unpublished.) (C) Scanning electron micrograph
of a titanium implant abutment surface exposed to the
oral cavity for 2 weeks, illustrating a mature biofilm consisting of multiple layers (49–99) of coccoid bacteria in a
glycocalyx matrix. Cracks in the specimen are artefacts at
the bottom of which the titanium surface may be visible.
Magnification: ·2500. (Figure reproduced courtesy of Dr S.
Abati, University of Milan, Italy; unpublished.)
75, 80, 81, 83, 103, 105). Furthermore, longitudinal
studies have investigated the transmission of putative
periodontal pathogens from periodontal sites to implant sites. In a group of patients treated for periodontitis and undergoing a maintenance-care program,
the deepest periodontal site in each quadrant was
sampled before, and 3 and 6 months after, implant
placement. The same putative periodontal pathogens
were identified in residual periodontal pockets and
colonizing the implants after 3 and 6 months (70).
The transmission of bacteria from tooth to implant
sites was confirmed in studies investigating the
dynamics of colonization (20, 109). De Boever & De
Boever (20) identified the presence of periodontal
pathogens around implants 1, 3 and 6 months after
implant placement in partially dentate patients who
were successfully treated for aggressive periodontitis
and yielded plaque and bleeding scores of <20%.
Only 5 of the 22 patients were colonized with
putative periodontal pathogens, which had already
occurred by 14 days. This microbiota remained unchanged at the 6-month examination. Likewise, the
remainder of the patients displayed a microbiota at
6 months that had a composition very similar to that
encountered after 10 days. This underlines the
importance of eliminating potential reservoirs of
periodontal pathogens before implant placement and
Periodontal vs. peri-implant infections
the importance of maintaining periodontal health
in partially dentate patients with oral implants (70,
109).
Similarities and dissimilarities with
periodontal infections
Whilst the majority of studies show that the composition of the subgingival microbiota associated with
health and disease is similar around implants and
teeth (3, 46, 53, 70, 75, 80, 81, 83, 103, 105), there is
emerging evidence that differences may be present in
some of the peri-implant infections (87).
Biofilm formation is influenced by the properties of
the surface to be colonized, including chemical composition, surface roughness and surface free-energy
(107). In vitro studies have demonstrated an affinity of
S. aureus for titanium surfaces (34). A number of
clinical studies have identified high levels of S. aureus
at deep peri-implant pockets with the presence of
suppuration and bleeding on probing (85, 87). S.
aureus is not strongly associated with chronic periodontitis. However, it is well documented that S.
aureus can be associated with therapy-resistant
(refractory) cases of periodontitis (19, 27, 37, 84).
Pathogenesis aspects
Host response to biofilm formation
The host response to biofilm formation has been
studied using various animal models. Berglundh et
al. (13), in a dog model, evaluated clinical and histological characteristics following de novo plaque
formation around teeth and implants. The size and
extent of the subepithelial connective tissue infiltrate
was assessed after 3 weeks of undisturbed plaque
accumulation. Both of these parameters, as well as
the composition of the cellular infiltrate, were identical in the gingiva around teeth and in the mucosa
around osseointegrated implants. This suggested that
the early host response to the bacterial challenge
around the implanto-mucosal unit is of a similar
magnitude and intensity as the one that occurs at the
dentogingival unit.
The effect of biofilm formation on the development
of the inflammatory response was later studied
experimentally in humans (77) (Fig. 2). Twenty partially dentate patients received oral implants following successful completion of periodontal therapy.
After 6 months of closely supervised periodontal
conditions the patients were asked to refrain from
Fig. 2. Illustration of the similar pattern of biofilm formation (as expressed by increasing plaque indices; PlI)
and host response to biofilm formation [as expressed by
increased (sulcus) bleeding index; SBI] at implants and
teeth after 3 weeks of experimental undisturbed plaque
accumulation in humans (77), illustrating a cause–effect
relationship between biofilm formation and gingivitis on
teeth, as well as peri-implant mucositis on implants.
oral hygiene practices for a period of 3 weeks. At the
end of this period optimal plaque-control measures
were re-instituted. Comparing the accumulation of
biofilm and the host response expressed at gingival
and peri-implant mucosal tissues revealed no difference in the development of gingivitis and mucositis,
respectively. Hence, there is a similar cause-and-effect relationship between the accumulation of biofilm and the development of experimental gingivitis
and peri-implant mucositis (60). This cause-and-effect relationship has since been confirmed in another
group of partially dentate human volunteers (114). In
addition to confirming the development of clinical
parameters, the inflammatory response was also
characterized by the enumeration of the proportions
of T and B cells in both gingiva and peri-implant
mucosa. No statistically significant differences in the
host response of these two tissues could be demonstrated after 3 weeks.
Host response with established biofilms
In an experimental dog study, 3 months of biofilm
accumulation with respect to the host response was
analyzed using both clinical and histological parameters, comparing gingival tissues with peri-implant
mucosal tissues (21). After 90 days of undisturbed
biofilm formation, the dogs had accumulated large
amounts of biofilm and the soft tissues around implants and teeth bled on gentle probing. The histological examination of the two types of inflamed soft
tissues revealed that (i) both gingiva and peri-implant
mucosa contained an inflammatory cell infiltrate
within the apical extension of the junctional epithelium and (ii) the composition of these infiltrates was
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Heitz-Mayfield & Lang
Fig. 3. Illustration of the host response of an inflammatory infiltrate subjacent to the junctional epithelium in
response to a biofilm challenge of 3 weeks (13) and
3 months (21). The initial response after 3 weeks is identical for the dento–gingival and the implanto–mucosal
unit. However, after persistent biofilm accumulation for
3 months, the inflammatory infiltrate in the implanto–
mucosal unit is almost threefold greater than that in the
dento–gingival unit.
similar in both gingiva and peri-implant mucosa,
showing a substantial loss of collagen and a significant increase in the numbers of inflammatory cells.
However, the apical extension of the inflammatory
infiltrate in the mucosa, as well as the size of the
lesion, was significantly greater (almost threefold
higher) than that in the gingiva (Fig. 3). This, in turn,
meant that the host response to the bacterial challenge after a period of 3 months was more pronounced in the peri-implant mucosa than in the
gingiva. It is, however, unknown whether this fact will
render the peri-implant mucosal tissue more prone
to the loss of supporting bone (i.e. peri-implantitis).
The host response to the bacterial challenge has been
demonstrated to develop irrespective of the implant
system used (1) (Figs. 4A and B).
Host response with advancing infections
For obvious ethical reasons, sequential studies on the
pathogenesis of periodontitis and peri-implantitis
can only be performed in animals. The ligature model
for biofilm formation has been used both in dogs (56)
and in monkeys (49, 96) to study the transition from
peri-implant mucositis to peri-implantitis and to
make comparisons with the pathogenesis of ligatureinduced periodontitis.
In the monkey model, plaque and gingival indices,
increasing probing depths and loss of attachment
were identical at ligated teeth and ligated implants
during the course of an 8-month plaque-accumulation study. Nonligated implants, however, only
developed mucositis and minimal bone loss within
170
Fig. 4. Experimental plaque accumulation in three different implant systems: Astra Tech; Brånemark; and
Straumann. (A) Following implant placement and meticulous plaque control, healthy peri-implant mucosal tissues
are evident around all three systems. Figure reproduced
courtesy of Clinical Oral Implants Research (1). (B) Following 5 months of biofilm accumulation, plaque deposits
are clearly visible on all three implant systems, resulting in
peri-implant mucositis. Figure reproduced courtesy of
Clinical Oral Implants Research (1).
the same period of time. It was concluded that
massive plaque accumulation generated by ligature
placement would result in similar tissue responses
for gingival and peri-implant tissues (49). In the dog
study, the progression of the inflammatory lesion was
found to extend into the bone marrow at peri-implantitis sites and hence to progress to a greater extent than the periodontitis lesion (56).
Another study, in monkeys (96), compared the
inflammatory response and the loss of supporting
bone at ligature-induced peri-implantitis and ligature-induced periodontitis for both ankylosed teeth
and normal control teeth. The histologic observations
supported a greater extent of bone loss and inflammatory infiltrate around implants and ankylosed
teeth compared with control teeth. It may therefore
be speculated that the absence of the periodontal
ligament could have a lesion-promoting effect in the
pathogenesis of peri-implantitis (96).
Following ligature removal, some of the lesions will
go into remission, while the majority of the sites will
experience further bone loss. In about 25% of the
cases it was demonstrated that rapid progressive
Periodontal vs. peri-implant infections
bone loss occurred within a period of 1 year after
removal of the ligatures (113). This, in turn, means
that peri-implant infections, once established, will
probably continue to progress, even though arrest of
the progression may be encountered in about 20% of
cases. The spontaneous progression of peri-implantitis may be influenced by exposed roughness and
topography of implant surfaces (5, 6, 12) favoring the
colonization with specific pathogens. There is conflicting evidence, however, regarding the effect of the
implant surface in the pathogenesis of peri-implantitis in humans (10, 111).
Similarities and dissimilarities with
periodontal infections
Human case series reporting histopathological data
at sites with peri-implantitis have described inflammatory lesions with high proportions of B cells and
plasma cells, suggesting that the peri-implantitis lesion has features similar to those of both aggressive
periodontitis and chronic periodontitis (11, 22, 32).
The peri-implantitis lesion may progress from an
existing mucositis with a greater infiltrate predominated by plasma cells that extends apically to the
position of the pocket epithelium (11).
From overwhelming evidence in the literature, it
appears that the development of periodontitis and
peri-implantitis lesions follows a similar sequence of
events. However, the dynamics of these pathological
processes may not be identical at all times. One
difference may be that the periodontitis lesion is
always walled off by an intact supracrestal connective tissue fibre compartment (100). Therefore, the
inflammatory cell infiltrates generally do not penetrate into the alveolar bone marrow. By contrast, a
peri-implantitis lesion may progress without the
presence of a healthy connective tissue fibre compartment walling off the lesion from the alveolar
bone. Consequently, it appears that the infection
may progress into the bone marrow in some instances (5, 6, 56, 61). Hence, from a clinical point of
view, some peri-implantitis lesions can be expected
to progress rapidly. This suggests that a peri-implant
site diagnosed with peri-implantitis should be treated without delay.
determined following cross-sectional analyses to
identify factors associated with disease.
The known risk factors for periodontitis development and progression are as follows (35):
• poor oral hygiene;
• gingivitis;
• tobacco consumption; and
• diabetes mellitus.
By far the most important risk factor for both the
development and the progression of periodontitis is
poor oral hygiene practices (72). This, in turn, results
in persistent gingivitis that has been identified as a
risk factor both for disease progression and for tooth
loss (93).
Tobacco consumption, in a dose-dependent manner, represents the third risk factor for the progression of periodontal disease. Heavy smokers should be
considered as individuals at high risk for disease
progression (14).
Finally, studies indicate that diabetes patients with
poor glycemic control have an increased risk for periodontal disease and disease progression (73). Regarding the risk evaluation of patients to develop peri-implantitis, the literature is less conclusive. Therefore,
only proposed risk indicators can be addressed.
A recent review evaluated risk indicators for periimplantitis (36). Cross-sectional analyses of the
studies in that review included the following patientbased risk indicators:
• poor oral hygiene;
• history of periodontitis;
• tobacco consumption;
• diabetes mellitus;
• alcohol consumption; and
• genetic traits.
Poor oral hygiene
There is substantial evidence that poor oral hygiene,
as expressed by median full-mouth plaque scores of
>2, was highly associated with peri-implantitis with
an odds ratio of 14.3 and a 95% confidence interval
of 9.1–28.7 (26). Furthermore, a prospective study
reported an association between poor oral hygiene
and peri-implant bone loss after 10 years (59). A
recent study identified inaccessibility for oral hygiene measures around implants in partially dentate
patients as a risk for peri-implantitis (99).
Risk evaluation (human studies)
Identification of true risk factors for disease requires
longitudinal studies with a prospective design to be
carried out in humans. A risk indicator can be
History of periodontitis
As in cases of periodontitis, peri-implant infections
may take years to develop. It is logical to assume that
171
Heitz-Mayfield & Lang
the susceptibility to periodontitis, characterized by
loss of attachment and alveolar bone loss, may
translate to susceptibility to peri-implantitis. In recent years, eight systematic reviews have addressed a
history of treated periodontitis as a risk indicator for
implant outcomes (4, 43, 45, 74, 79, 94, 98, 108).
Three studies reporting on the occurrence of periimplantitis found a statistically significantly greater
risk of peri-implantitis in patients with a history of
treated periodontitis compared to those without a
history of periodontitis (26, 44, 88). Reported odds
ratios ranged from 3.1 to 4.7.
Tobacco consumption
Besides poor oral hygiene, tobacco consumption has
been propagated as the second most important risk
factor for disease progression for both teeth and oral
implants. An association between smoking and periimplantitis has been found in five cohort studies (31,
33, 48, 63, 88). A higher risk was found for smokers
compared with nonsmokers, with odds ratios ranging
from 3.6 to 4.6. Smoking has also been identified as
an aggravating factor to poor oral hygiene (59);
hence, all the studies mentioned above have adjusted
for poor oral hygiene practices when evaluating the
contribution of tobacco consumption.
Diabetes mellitus and alcohol
consumption
There is limited evidence that diabetes mellitus and
alcohol consumption are associated with periimplant diseases, although diabetes mellitus has
been associated with increased implant loss. Only
one study in nonsmoking individuals with poor
metabolic control has shown an increased risk for
peri-implantitis (26). Similarly, only one study suggested that alcohol consumption of >10 g daily
resulted in significantly greater marginal bone
loss, even exceeding the amount identified in
smokers (30).
Genetic traits
As identified in a systematic review on the role of the
composite interleukin-1alpha and interleukin-1beta
polymorphisms and their natural specific inhibitor,
interleukin-1 receptor antagonists, with respect to the
development of periodontitis and periodontal therapy (41), no conclusive evidence can be attributed to
the genetic traits. Moreover, a recent systematic review on the role of the composite interleukin-1
172
polymorphisms for the development of peri-implantitis has identified two retrospective cohort studies
(25, 31) with conflicting and limited evidence (42).
Hence, from a clinical point of view, the identification of genetic traits does not appear to be justified at
this time.
Similarities and dissimilarities with
periodontal infections
As both periodontitis and peri-implantitis are
opportunistic infections with a similar etiology and
similar clinical outcomes it is reasonable to assume
that risk evaluation should follow similar pathways.
In fact, the three major risk factors for periodontitis
have also been shown to represent risk indicators
for peri-implantitis. In addition, a history of periodontitis indicating susceptibility to this infection
may be the most important risk factor for periimplantitis.
Diagnosis
In determining the severity and extent of periodontitis, the diagnostic process encompasses at least (i)
an assessment of the inflammatory changes and (ii)
an assessment of the damage to the periodontal tissues, as expressed by probing depth and loss of
clinical attachment. These probing measurements
are highly sensitive, while a radiographic documentation of bone loss represents a specific test with
which to document the sequelae of periodontitis.
This disease may only be diagnosed properly if
inflammation occurs concomitantly with pocket
development (increasing probing depth). In the absence of inflammation and deepened pockets, loss of
attachment represents a previous history of periodontitis or recession.
Because the pathogenesis of peri-implantitis closely resembles that of periodontitis, it is imperative to
use the same diagnostic criteria for the detection of
peri-implantitis and for monitoring the progression
of lesions over time (50).
It has clearly been demonstrated that any disruption in the soft tissue–implant interface caused by
probing the peri-implant sulcus will be followed by
the formation of a new epithelial attachment within
5 days (23). This is also the case when probing the
periodontal sulcus (106) (Figs. 5A–C). The application
of a light probing force (0.2–0.3 N) will also provide
reliable assessments of probing depth around
implants (51, 97). In peri-implantitis, however, the
Periodontal vs. peri-implant infections
A
B
C
2
1.8
1.6
1.4
1.2
1
0.8
0.6
0.4
0.2
0
Day 0
Day 1
Day 2
Fig. 5. Repair of the junctional epithelium at an implant
surface following probing (23). (A) Standardized probing
applying a pressure of 0.25 N along a defined groove in a
prototype abutment for reproducible probing location at
the implant surface. Figure reproduced courtesy of Clinical Oral Implants Research (23). (B) Adherence of new
junctional epithelium over 1 week as shown by the
A
B
Day 3
Day 5
Day 7
increasing distance (mm) of the apical-most cell to the
coronal-most cell of the junctional epithelium adhering to
the implant surface. (C) A baseline histologic section
(magnification · 40), immediately following probing (day
0), showing complete separation of the junctional epithelium from the implant. Figure reproduced courtesy of
Clinical Oral Implants Research (23).
C
Fig. 6. Histologic probe penetration in healthy, mucositis
and peri-implantitis sites (51). (A) Histologic probe penetration in peri-implant mucositis, identifying the attachment level of the junctional epithelium within 0.2 mm of
the supracrestal fibres that are densely arranged around
the implant abutment, hindering penetration of the probe
following application of a standardized force of 0.2 N.
Figure reproduced courtesy of Clinical Oral Implants Research (51). (B) Probing error in identifying the histologic
location of the apical-most cell of the junctional epithelium in peri-implant health or mucositis. Identification of
the epithelial attachment by applying a probing pressure
of 0.2 N resulted in a very small probing error (histologic
attachment level-histologic pocket depth). In peri-implantitis most probes penetrate into the connective tissue,
resulting in a probing error of up to 1.6 mm for location of
the epithelial attachment. (C) Histologic probe penetration in peri-implantitis by applying a pressure of 0.2 N to
inflamed mucosa, illustrating probe penetration to the
alveolar bone. Figure reproduced courtesy of Clinical Oral
Implants Research (51).
probe may penetrate into the connective tissue and
only be stopped in its penetration by the alveolar
bone (Figs. 6A–C).
In a maintenance program for the long-term care
of implants, probing-depth measurements should be
compared with baseline assessments of probing
depth obtained after the placement of the reconstruction. In the light of the desirability of more
apical placements of implants allowing for an optimal emergence profile of the crown, initial probing
depth measurements may exceed the 3–4 mm depth
usually encountered. Consequently, the development
of disease will be associated with increasing probing
depth from the baseline value. Nevertheless, a 6 mm
peri-implant pocket has been found to be indicative
of peri-implantitis (28).
In cases where there has been an increase in
probing depth with the presence of bleeding on
probing, supplemental radiographs should be
obtained to further evaluate the progression of
peri-implantitis. These will probably reveal an
implant-specific saucer-shaped intraosseous lesion
173
Heitz-Mayfield & Lang
as opposed to the diagnostic site-specific characteristics, confirming probing measurements in
periodontitis.
A very specific characteristic of implant failure,
representing the total loss of osseointegration, is
implant mobility. This highly specific parameter,
however, is completely useless for the diagnosis of
peri-implant mucositis or peri-implantitis.
A dynamic assessment of bone-to-implant contact
reflecting implant stability would be desirable to assess the events during healing. Recently, noninvasive
diagnostic methods have been advocated to specifically monitor the implant stability (8). Resonance
frequency analysis is believed to yield the degree of
bone-to-implant contact during the early phases of
healing (64, 65). Consequently, resonance frequency
analysis has been evaluated in relation to jaw bone
characteristics and during early healing following
implant installation (40). However, there was no
evidence that resonance frequency analysis would
reliably reveal loss of stability in advance of the
clinically evident implant failure. When resonance
frequency analysis records implant stability quotient
values within the range of 57–70, implant stability can
be assumed. No predictive value for losing implant
stability could be attributed to resonance frequency
analysis and hence the routine use of this diagnostic
methodology may be questioned (40).
In conclusion, probing peri-implant sulci or
pockets is an essential criterion for the diagnosis of
peri-implant infections as is also true in cases of
periodontitis. It is important that only light probing
forces, preferably between 0.2 and 0.3 N, should be
used. To monitor the inflammatory component for
peri-implant mucositis and peri-implantitis, bleeding
on probing, again using a light force, should be
evaluated. Obviously the presence of pus represents
the sign of ongoing infection that often accompanies
the progression of peri-implantitis (89). As found in
cases of periodontitis, loss of supporting bone, as
revealed by radiographs, is a confirmatory test for the
diagnosis of peri-implantitis.
Therapy
Similarities with periodontal therapy
Because the etiologies of periodontitis and peri-implant infections are almost identical it is obvious that
all therapeutic approaches should be anti-infective.
In the treatment of periodontitis, this consists of
detailed instruction to improve oral hygiene practices
174
concomitant with a thorough mechanical debridement of the contaminated root surfaces. This will
result in a healing of the debrided wound area with a
junctional epithelium closely adhering to the previously exposed root surface. The patientÕs supragingival plaque control subsequently slows re-infection
of the subgingival environment with pathogens. In
conjunction with appropriate, professionally administered periodontal maintenance therapy, the clinical
outcome of such treatment has been demonstrated to
be excellent in the long-term (38, 58). In deep periodontal defects, nonsurgical mechanical debridement
may result in both inadequate biofilm removal and
pocket reduction. In such situations it may be
necessary to obtain access to the contaminated root
surface by reflecting mucoperiosteal flaps. Such
access flaps may also be used in specific cases to
attempt regeneration of periodontal tissues that have
been destroyed by the periodontal infection. Similar
therapeutic principles govern the treatment of periimplantitis because poor oral hygiene is the most
pertinent risk factor for the development of infection
in the oral cavity. Instruction in oral hygiene practices represents a prerequisite for successful treatment outcomes. Owing to the fact that existing
periodontitis lesions may act as reservoirs of pathogens to colonize implant surfaces, it is imperative
that periodontitis be successfully treated and
controlled, preferably before implant placement.
However, if peri-implantitis is found in patients with
untreated periodontitis, treatment of periodontitis
must be given concurrently with the treatment of
peri-implantitis. If satisfactory treatment outcomes
are to be expected, mechanical debridement of
contaminated root and implant surfaces must be
performed. However, mechanical debridement is difficult to perform on implant surfaces because the use
of steel curettes should be avoided in this situation
(62). Furthermore, implant and supported reconstruction designs may often hinder access to the contaminated implant surfaces for thorough mechanical
debridement. It may therefore be desirable to apply
antimicrobial agents with proven efficacy, either to the
peri-implant sulci and ⁄ or as a mouthrinse, to deplete
the supragingival and supramucosal plaque reservoirs.
However, only three controlled clinical trials have
evaluated the efficacy of such combined mechanical
and antiseptic debridement protocols (18, 24, 78).
These measures of mechanical and adjunctive antiseptic debridement are, in most cases, sufficient to
treat peri-implant mucositis.
Cases of peri-implantitis characterized by deepened probing depths, concomitant bone loss and
Periodontal vs. peri-implant infections
A
C
B
D
E
Fig. 7. Treatment of advanced peri-implantitis with antiinfective therapy. Figure reproduced courtesy of Dr B.
Schmid (Belp, Switzerland). (A) Two Straumann hollow
screw implants (no longer available) of 12 mm with a titanium plasma sprayed surface were installed in 1991. (B)
Two years following loading of the implants a radiograph
revealed advanced peri-implant bone loss in one implant
and initial peri-implant bone loss at the other implant. (C)
Following nonsurgical mechanical debridement concomitant with daily rinsing with 0.2% chlorhexidine solution
and weekly irrigation with 0.5% chlorhexidine in the
pocket for 1 month, surgical access was obtained and the
implant was rinsed with copious amounts of chlorhexi-
dine. The patient was prescribed 500 mg of ornidazole
(Tiberal), twice daily for 10 days. The radiograph taken
in 1997 shows bone repair. At this time some inflammation was still present and a tetracycline fibre (Actisite, no
longer available) was applied for 10 days in conjunction
with additional mechanical debridement and irrigation
with chlorhexidine. (D) Further bone repair was documented in 1999 as a result of regular maintenance and
optimal plaque control by the patient. (E) Stable periimplant bone levels 5 years after the second active antiinfective peri-implantitis therapy. This case report clearly
demonstrates the importance of anti-infective therapy for
peri-implant disease control.
bleeding on probing cannot usually be treated by
nonsurgical mechanical and antiseptic debridement
alone. However, plaque control and submucosal
debridement are a prerequisite before further steps
are taken in the treatment of peri-implantitis (e.g.
administration of systemic or local antibiotics and ⁄
or surgical debridement). In studies dealing with the
treatment of peri-implantitis, desirable outcomes
have included resolution of inflammation, reduction
in probing depths and a substantial reduction in the
number of putative pathogens. These satisfactory
outcomes have been reported when systemic or local
antibiotics are adjunctively used for the management
of sites with deepened pockets of ‡6 mm (17, 67, 68,
86, 92) (Figs. 7A–E).
Owing to the lack of randomized controlled clinical
trials, the benefits of antibiotics adjunctive to
debridement, before or concomitant with surgical
debridement, may be debated. However, the often
rapid progression of peri-implantitis and the
proposed differences observed in advancing periimplantitis lesions compared with periodontitis
lesions may justify the use of antibiotics directed
against the recognized putative pathogens.
In a variety of situations, surgical access to the
contaminated implant surface may be required.
Because the main goal of the open-flap procedure is
access to the contaminated surface, the typical
saucer-shaped and deep peri-implantitis lesions can
only be decontaminated effectively by surgical access (Figs. 8A–E). However, to date, only one study
has evaluated the long-term (5 years) outcome of
peri-implantitis treated with surgical access including the use of antibiotics (54). Out of the 27 implants with peri-implantitis placed in nine patients
at baseline, 25% of the implants were lost in four
patients during the follow-up period despite a significant reduction in the presence of plaque and
mucosal bleeding. Four implants continued to lose
bone, while in six sites bone formation was observed. Therefore, it appears that surgical treatment
does not guarantee the long-term stability without
re-infection and hence the outcomes should be
considered unpredictable.
175
Heitz-Mayfield & Lang
A
B
C
D
E
Fig. 8. Treatment of advanced peri-implantitis with antiinfective therapy in a high-risk patient. (A) Radiograph of
three osseointegrated implants (Nobel Biocare, TiUnite
surface) replacing three missing teeth. The patient had a
history of treated periodontitis and was a heavy smoker
(20 cigarettes per day for more than 20 years). (B) Photograph illustrating clinical signs of peri-implantitis:
bleeding on probing, suppuration and deep pockets (7–
9 mm) 5 years after implant placement. (C) Radiograph
confirming peri-implantitis, illustrating advanced periimplant bone loss at two implants and moderate bone loss
at the implant in the premolar region. Following an antiinfective treatment protocol including nonsurgical
mechanical debridement and oral hygiene instructions,
supplemented by application of chlorhexidine gel (0.5%)
for 4 weeks and smoking-cessation counselling, inflammation and deep pockets were still present at re-evaluation. Consequently, access surgery was scheduled. (D)
Circumferential intraosseous (saucer shaped) peri-implant bone defects following surgical access and decontamination of the implant surface using physiologic sterile
saline. The patient was prescribed adjunctive systemic
antibiotics [metronidazole (400 mg) and amoxicillin
(500 mg) three times daily, for 1 week]. After surgery the
patient rinsed with chlorhexidine mouthrinse (0.2%)
twice daily for a 4-week period. Maintenance care was
then provided every 3 months. (E) Resolution of the
inflammation 6 months after treatment. Decreased probing depths and mucosal recession, and no bleeding or
suppuration on probing, were observed.
Surgical procedures are often advocated to gain
access for regenerative procedures. However, there is
no evidence to date that such procedures reveal
additional benefits or secure treatment outcomes in
the long term.
implant surfaces. As indicated above, the inability to
access microbial habitats in the subgingival ⁄ submucosal region may often result in less than optimal
treatment outcomes. Irrespective of surface roughness and configuration, decontamination of the titanium surface poses inherent problems and can
probably not be achieved by mechanical debridement alone. It can be speculated that irrigation with
antiseptic solutions and ⁄ or physiologic saline might
dilute the bacterial load, thereby allowing innate and
adaptive host responses to control the infection.
Exception to the rule
While periodontal treatment involves the debridement of contaminated tooth surfaces, treatment of
peri-implantitis focuses on the decontamination of
176
Periodontal vs. peri-implant infections
Animal studies have demonstrated that there is no
superiority of one decontamination protocol vs. another (95). Even the application of carbon dioxide
laser has not been shown to be superior to simple
decontamination with saline, when applying the
microbiological dilution principle (76). It is apparent
that the decontamination of the implant surface located either in a submucosal region or under surgical
access represents the most pertinent challenge for
predictable treatment outcomes.
Summary and conclusions
This review was undertaken to address the similarities and dissimilarities between the two disease
entities of periodontitis and peri-implantitis. The
overall analysis of the literature on the etiology and
pathogenesis of periodontitis and peri-implantitis
provided an impression that these two diseases have
more similarities than differences. First, the initiation
of the two diseases is dependent on the presence of a
biofilm containing pathogens. While the microbiota
associated with periodontitis is rich in gram-negative
bacteria, a similar composition has been identified in
peri-implant diseases. However, increasing evidence
suggests that S. aureus may be an important pathogen in the initiation of some cases of peri-implantitis.
Further research into the role of this gram-positive
facultative coccus, and other putative pathogens, in
the development of peri-implantitis is indicated.
While the initial host response to the bacterial challenge in peri-implant mucositis appears to be identical to that encountered in gingivitis, persistent
biofilm accumulation may elicit a more pronounced
inflammatory response in peri-implant mucosal tissues than in the dentogingival unit. This may be a
result of structural differences (such as vascularity
and fibroblast-to-collagen ratios).
When periodontitis and peri-implantitis were produced experimentally by applying plaque-retaining
ligatures, the progression of mucositis to peri-implantitis followed a very similar sequence of events as
the development of gingivitis to periodontitis. However, some of the peri-implantitis lesions appeared to
have periods of rapid progression, in which the
infective lesion reached the alveolar bone marrow. It
is therefore reasonable to assume that peri-implantitis in humans may also display periods of accelerated destruction that are more pronounced than that
observed in cases of chronic periodontitis.
From a clinical point of view the identified and
confirmed risk factors for periodontitis may be
considered as identical to those for peri-implantitis.
In addition, patients susceptible to periodontitis appear to be more susceptible to peri-implantitis than
patients without a history of periodontitis.
As both periodontitis and peri-implantitis are
opportunistic infections, their therapy must be antiinfective in nature. The same clinical principles apply
to debridement of the lesions and the maintenance of
an infection-free oral cavity. However, in daily practice, such principles may occasionally be difficult to
apply in peri-implantitis treatment. Owing to implant
surface characteristics and limited access to the
microbial habitats, surgical access may be required
more frequently, and at an earlier stage, in periimplantitis treatment than in periodontal therapy.
In conclusion, it is evident that periodontitis and
peri-implantitis are not fundamentally different
from the perspectives of etiology, pathogenesis, risk
assessment, diagnosis and therapy. Nevertheless,
some difference in the host response to these two infections may explain the occasional rapid progression
of peri-implantitis lesions. Consequently, a diagnosed
peri-implantitis should be treated without delay.
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