Periodontology 2000, Vol. 73, 2017, 203–217 © 2016 John Wiley & Sons A/S.
y & Sons A/S. Published by John Wiley & Sons Ltd
Printed in Singapore. All rights reserved
Reliability of periodontal
diagnostic tools for monitoring
peri-implant health and disease

ONIQUE CHRISTIAENS, LARS SENNERBY &
P I E R L U I G I C O L I , V ER
HUGO DE BRUYN
The use of dental implants to restore compromised
oral function and esthetics as a result of tooth loss is a
well-established and well-proven treatment modality.
Since the first pioneer studies in the 1960s and 1970s,
overwhelming scientific evidence has been presented
regarding the safe use of dental implants. For full-
fixed implant-retained prostheses, the long-term clin-
ical survival of dental implants is described to be in
the range of 80–95% for up to 24 years of function (8,
9, 31, 63). For single-tooth crowns and short-span
bridges, treatment outcomes of 15–22 years of func-
tion have been in the order of 90–100% (10, 21, 29,
46). Moreover, as a result of modifications of implant
surface topography and design, a better biologic
understanding of the concept of osseointegration,
and improved surgical, as well as prosthetic treat-
ment protocols, even better long-term outcomes can
probably be foreseen with the modern implant sys-
tems used today (4).
The scientific community agrees that implant suc-
cess cannot be evaluated based on implant survival
alone, and should also take peri-implant conditions
and crestal bone-level stability into consideration.
This is logical because an implant with continuous
crestal bone loss is at risk for failure. In 1986, Albrek-
tsson et al. (3) stressed the importance of assess-
ments of crestal bone level when describing or
comparing dental implant systems. Their proposed
criteria of acceptable bone loss of 1.5 mm during the
first year of loading and thereafter of 0.2 mm yearly,
which were based on the early experiences with
machined surface implants and two-stage surgical
procedures, are still generally accepted by the scien-
tific community.
It is widely accepted that initial peri-implant bone
remodeling occurs as a consequence of biologic
adaptation of the peri-implant tissues, and thereafter
PERIODONTOLOGY 2000
a steady-state condition is to be expected. Long-term
clinical studies have, in general, shown crestal bone
loss to occur during the first year in function (69). The
initial crestal remodeling seems to be initiated by the
piercing of the mucosa with an abutment (83), and
the amount of bone loss is related to implant design
and/or surface properties (59). After this initial adap-
tation of the crestal bone, there seem to be rather
small average changes over time when following a
group of patients. However, when a frequency distri-
bution of bone loss for the same group of patients is
performed, it is obvious that some patients show
more bone loss during the first year than others.
Obviously, continuous crestal bone loss might consti-
tute a threat to implant survival and the longevity of
implant-supported prostheses. Furthermore, bone
loss might result in an unfavorable esthetic outcome
as a result of midfacial recessions or papilla retrac-
tion, or insufficient papilla fill, and these soft-tissue
changes may hamper patient satisfaction and lead to
discomfort. Hence, if possible, it is important to iden-
tify implants at risk for failure (i.e. showing continu-
ous bone loss).
Despite the documented long-term success rate of
implant treatment, alarming reports have been pub-
lished reporting of a high prevalence of periimplant
soft-tissue inflammation associated with peri-implant
bone loss (58, 62). It has been recommended that
implants showing signs of inflammation, as detected
by bleeding on probing and by probing pocket depth,
should be treated similarly to natural teeth affected
by periodontitis – either by nonsurgical or surgical
procedures – to prevent the future loss of the ‘af-
fected’ fixtures. Consequently, it seems as if well-
functioning dental implants would suddenly be in
need of nonsurgical, or possibly even surgical, treat-
ments following the detection of clinical signs of
203
Coli et al.
inflammation. The recommendation is based on the
assumption that periodontal indices, such as probing
pocket depth and bleeding on probing, are reliable
indicators of the condition of the peri-implant tissues
and that increased probing pocket depth with time
and the presence of bleeding on probing are good
predictors of future bone loss and implant failure.
The great danger of this approach is over-diagnosis
of peri-implant pathology, which results in patients
being subjected to unnecessary, and possibly iatro-
genic, treatment. Given the significant consequence
of this approach on a patient’s well-being and the lia-
bility consequences for health-care stakeholders,
such as dental insurance companies, public health
organizations and clinicians, it is imperative that it is
clearly validated in clinical studies that increasing
probing pocket depth over time, as well as the pres-
ence of bleeding on probing, are reliable predictors of
future bone loss, and that this bone loss leads to
implant failure as an end-stage.
The aims of this paper were: (i) to provide insights
into the histologic features of the peri-implant soft
tissue and the differences between it and the peri-
odontal soft tissues; (ii) to describe the clinical diag-
nosis of peri-implant diseases, such as peri-implant
mucositis and peri-implantitis; (iii) to review the evi-
dence-based knowledge on the use of periodontal
indices around dental implants, with special empha-
sis on peri-implant probing and provoked bleeding;
and (iv) to propose clinical guidelines regarding the
monitoring of peri-implant health.
Periodontal versus peri-implant
tissue complexes
After piercing the mucosal tissues with an artificial
structure, such as a transmucosal implant, an abut-
ment or restorative component, a soft-tissue barrier
is established. The structure of this peri-implant
mucosal attachment has been described in a number
of animal studies and also compared with the peri-
odontal tissues surrounding natural teeth (11–13, 17).
The soft-tissue attachments of teeth and of implants
have similarities, especially in the most coronal part.
A keratinized oral epithelium is continuous with a
nonkeratinized sulcular epithelium that is attached to
the surface of tooth and implant. Close to the bone, a
thin junctional epithelium connects to the implant or
tooth component. Around teeth, the periodontal liga-
ment connects the cementum of the tooth with the
bone, whereas the peri-implant connective tissue has
similarities to fibrous scar tissue in that it contains
204
high numbers of collagen fibers and low numbers of
fibroblasts and vessels. The collagen fibers run paral-
lel to the implant surface (17), in contrast to the per-
pendicular orientation at teeth. Because of the direct
bone-to-implant contact between implant and bone,
coined as osseointegration, the vascularity in the
mucosal tissues is different as a result of the lack of a
vascular plexus of the periodontal ligament (Fig. 1).
Compared to periodontal tissues, it is suggested
that peri-implant tissues are more susceptible to
inflammatory reactions, a phenomenon also con-
firmed immunohistochemically with an increase of
inflammatory infiltrate in comparison with teeth (25).
The chronic presence of this infiltrate at the implant–
abutment interface of two-piece implants has been
reported and has been attributed to the microgap
between the implant and the abutment (15, 16). In
contrast, the connective tissue surrounding one-piece
implants has been reported to be inflammation free,
possibly because of the absence of a microgap (17).
The dissimilarity of periodontitis and peri-implanti-
tis has been shown in a human biopsy study using
histologic and immunohistochemical analyses of the
respective lesions (20). In this study, peri-implantitis
lesions were defined based on probing pocket depths
of > 7 mm with bleeding on probing. In contrast to
periodontitis samples, peri-implantitis lesions were
more than twice as large and contained significantly
larger area proportions, numbers and densities of
plasma cells and macrophages. Peri-implantitis
lesions also extended to a position apical of the
pocket epithelium and were not surrounded by non-
infiltrated connective tissue. They further presented
with significantly larger densities of vascular
Fig. 1. Schematics showing morphological differences and
similarities between the dento–gingival complex (highly
specialized and differentiated tissues) and the implant sit-
uation (foreign-body reaction with scar tissues).
 Tools for monitoring peri-implant health

structures in the connective tissue area lateral to the Peri-implantitis

infiltrated connective tissue than within the infiltrate.
At the 6th European Workshop of Periodontology
This study suggests that lesions around implants and
consensus meeting, peri-implantitis was defined as
teeth may have critical histopathologic differences,
mucosal inflammation with loss of supporting bone
which contributes to the understanding of dissimilar-
(62), while at the 7th European Workshop of Peri-
ities in the onset and progression between the two
diseases. This is basically a confirmation of the sug- odontology meeting, it was defined as change of cre-
stal bone level with time and bleeding on probing,
gestion made by Lang & Berglundh (58), stating that
with or without deepening of probing pocket depth
structural differences between a periodontal lesion
(58). Hence, there was a slight change of the diagnosis
and a peri-implant lesion may influence the host
recommendations. In the consensus report from the
response and yield a histopathological difference.
Albrektsson et al. (5) elaborated further on this 6th European Workshop of Periodontology, diagnosis
of peri-implantitis required changes in probing
aspect and suggested that although the soft-tissue
pocket depth and/or in probing attachment level over
barrier around implants or implant abutments has
time that could be indicative of crestal bone loss (62).
morphologic similarities to gingiva around teeth,
It was stated that: (i) probing is essential for diagnosis
they represent two completely different entities as a
of peri-implant diseases; (ii) bleeding on probing
result of their origins. The periodontal complex is
indicates presence of inflammation in the peri-
the result of millions of years of evolution and con-
implant mucosa; (iii) bleeding on probing may be
sists of highly differentiated and specialized tissues,
used as a predictor for loss of tissue support; (iv) an
while the soft-tissue barrier around implants is scar
increase in probing depth over time is associated with
tissue. In essence, the authors propose that osseoin-
loss of attachment and supporting bone; (v) probing
tegration should be regarded as the result of a for-
eign-body reaction, which results in direct bone– pocket depth, bleeding on probing and suppuration
should be assessed regularly for the diagnosis of peri-
implant contact and the establishment of a soft-tis-
implant diseases; and (vi) radiographs are required to
sue scar. Based on these observations, it seems logi-
evaluate supporting bone levels around implants. The
cal to assume that the gingiva at teeth and the peri-
general conclusions from the workshop were that ‘in
implant mucosa at implants cannot be expected to
peri-implantitis the mucosal lesion is often associated
behave in a similar way when subjected to diagnos-
with suppuration and deepening of the pocket, but
tic tests (4).
always accompanied by loss of supporting marginal
bone’. Unfortunately, the workshop neither defined a
Definition and diagnosis of peri- threshold for unacceptable bone loss nor at which
time point this possible bone loss is not considered as
implant diseases
initial bone remodeling, the latter being known to
occur during establishment of the biologic width after
Peri-implant mucositis healing (69, 83).
The threshold levels of crestal bone loss and/or
Two decades ago, peri-implant mucositis was defined
probing pocket depth or attachment loss required to
as a reversible inflammation of the peri-implant soft
distinguish between reversible and irreversible condi-
tissue without signs of any loss of the supporting
tions has been a matter of debate since the early
bone. As with gingivitis, peri-implant mucositis can
1990s. Continuous revisions of criteria because of dis-
be a plaque-induced inflammation caused by bacte-
agreement in the scientific community have compli-
rial biofilm and is characterized by reddening, swel-
cated clinical and scientific evaluations. A literature
ling and bleeding on probing of the peri-implant soft
review revealed that nine different threshold levels for
tissue (51, 72, 85). Peri-implant mucositis can also be
radiographic bone loss have been used to diagnose
induced by extracoronal residual cement (64, 65). In
peri-implantitis (81).
the consensus report from the 6th European Work-
As discussed above, the definition of peri-implanti-
shop of Periodontology, peri-implant mucositis was
tis was modified from the 6th to the 7th European
defined as the presence of inflammation in the
European Workshop of Periodontology. The impor-
mucosa at an implant with no signs of loss of sup-
tance of baseline crestal bone level measurements
porting bone (85). At the 7th European Workshop of
was recognized in order to be able to evaluate bone
Periodontology consensus meeting, peri-implant
loss after initial remodeling following implant instal-
mucositis was diagnosed as bleeding on gentle prob-
lation (58). These baseline-recorded bone levels were
ing (< 0.25 N) (58).

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Coli et al.

described as ‘the reference from which the develop-

ment of peri-implant disease can be recognized and
followed in subsequent examinations.’ Hence, this
workshop clearly defined that peri-implantitis is char-
acterized by loss of crestal bone over time in conjunc-
tion with bleeding on probing, with or without
concomitant deepening of the peri-implant pockets
(58). In other words, it would appear that probing
pocket depth measurements would not be necessary
for a diagnosis of peri-implantitis. However, the same
paper stated, ‘when changes in the clinical parame-
ters indicate disease (bleeding on probing, increased
Fig. 2. Schematics showing probing in healthy and in peri-
probing depth), the clinician is encouraged to take a odontally diseased situations.
radiograph to evaluate possible bone loss.’ This was
also emphasized at the 8th European Workshop of
Periodontology consensus meeting (75), where a diagnosis of periodontitis is instead established for
more pragmatic definition of peri-implantitis was sites showing bleeding on probing and probing
introduced whenever baseline radiographs were pocket depth of ≥ 4 mm associated with radiographic
unavailable. A vertical distance of 2 mm from the ‘ex- evidence of bone loss (61).
pected’ crestal bone level following remodeling after
implant placement was suggested as an appropriate Probing pocket depth as assessment of
threshold level. Measurements of probing pocket peri-implant conditions
depth were still recommended as being among the
Animal studies
principal parameters for evaluation of peri-implanti-
tis treatment and as a secondary parameter for the Ericsson and Lindhe (33) showed that in healthy soft-
evaluation of healing after mucositis treatment. tissue conditions, probe penetration was more
advanced at implants than at teeth and concluded
that the differences between the attachment structure
Reliability of probing pocket depth of teeth and that of peri-implant mucosa make the
conditions for probing pocket depth measurements
at teeth and implants different (Fig. 3). In contrast to
Probing pocket depth as assessment of
the aforementioned study, Lang et al. (57) reported
periodontal conditions
that in healthy and mucositis sites, the probe tip was
Investigations from the 1970s have clearly shown that located at the most apical cell of the junctional
in the case of an inflamed periodontium, the tip of epithelium, whereas in the case of ligature-induced
the probe penetrates the epithelium into the connec- peri-implantitis sites the probe tip penetrated into
tive tissue, overestimating the depth of the histologi- the connective tissue. They concluded that probing
cal pocket. In the case of a healthy gingiva, the tip of around implants represents a good technique for
the probe fails to reach the most apical cell of the
epithelium because of the increased resistance of the
periodontal tissues to probing, thus underestimating
the depth of the histological pocket (Fig. 2). In other
words, probing pocket depth measurements around
teeth provide information on the ability of the peri-
odontium to withstand probe penetration as a mea-
sure of the inflammatory conditions of the tissues.
Therefore, a distinction should be made between the
histological pocket depth and the clinical pocket
depth (7, 66, 80). Because of the anatomy of the peri-
odontium, probing pocket depth values of less than
4 mm are considered as falling within normal ana-
tomic variations, and a diagnosis of gingivitis is estab- Fig. 3. Schematics showing probing at a healthy tooth and
lished for the sites showing bleeding on probing. A at an implant.

206

assessing the status of peri-implant mucosal health or
disease. The difference in results between both stud-
ies was attributed to the lower probing force, of 0.2 N,
in the latter study (57) compared with 0.5 N in the
former study (33). From a clinical perspective, how-
ever, one should realise that force-controlled probing
is uncommon in daily practice. Mostly, hand probing
is used for diagnostic purposes. This is a major prob-
lem because the reliability of probing force is ques-
tionable. There is still no commercially available
instrument that resolves all of the inherent limitations
of clinical attachment measurements (71).
Human studies
Lekholm et al. (60) presented data from machined
surface implants placed in 20 partially edentulous
patients and with a mean follow-up time of 7.6 years.
Data on probing pocket depth, bleeding on probing,
radiographic bone-level measurements, microbiolo-
gical samples and soft-tissue biopsies were recorded.
The mean probing pocket depth was 3.8 mm, 45% of
the pockets measured 4–5 mm and 15% were
≥ 6 mm. Bleeding on probing was recorded at 80% of
sites, despite a limited mean bone loss of 0.07 mm
annually. The microflora was periodontally non-
pathogenic in nature in 94% of the samples, and the
soft-tissue biopsies showed a healthy mucosa in 95%
of cases. It was concluded that bleeding of peri-
implant tissues and deep pockets were not necessar-
ily related to crestal bone loss, the presence of a
pathogenic microflora or histologic changes indica-
tive for signs of periodontitis. Based on these findings,
Lekholm et al. (60) suggested that radiographic exam-
ination of marginal bone height changes, together
with fixture mobility tests, were preferable para-
meters to assess the prognosis of osseointegrated fix-
tures.
Serino et al. (79) examined the correlation between
the probing pocket depth at implants, before and
after removal of the prosthetic reconstructions, with
the amount of peri-implant bone loss measured dur-
ing peri-implant surgery. Twenty-nine patients with
89 implants with a diagnosis of peri-implantitis were
included in the study. The probing pocket-depth
measurements made after removal of the prosthetic
reconstruction (when good access to the implants
was made possible) had a high correlation with the
amount of bone loss assessed during surgery. The
findings therefore confirm the reports from animal
studies that the probe tip penetrates through the soft
tissues to a position close to the alveolar bone level.
On the other hand, probing pocket depth measure-
ments made before removal of the prosthetic
Tools for monitoring peri-implant health
reconstruction had a poor correlation with the
amount of bone loss and tended to overestimate the
peri-implant tissue loss. This study provided data
regarding the probe tip position in peri-implantitis
conditions only and not in healthy or peri-implant
mucositis conditions.
Is a probing pocket depth of 4mm or more a sign of
pathology?
The poor diagnostic value of probing depths to dis-
criminate bone loss and peri-implantitis, as presented
in the early studies, contradicts the recommendations
currently suggested by periodontal societies world-
wide (1, 58, 62) and as used in frequently cited studies
(73, 74). In similarity to periodontal disease, Roos-
Jansaker et al. (73, 74) used probing pocket depth
values of ≥ 4 mm in association with bleeding on
probing to establish a diagnosis of periimplantitis.
This is possibly based on the assumption that the
peri-implant anatomy and histology would be similar
to those of the periodontium. However, this assump-
tion has never been proven; in contrast, there are no
reports in the literature demonstrating that probing
pocket depth values of > 4 mm are outside the nor-
mal anatomic variations related to health or would
represent pathological alterations of the peri-implant
tissues. Furthermore, no investigations have shown
that a greater distance between the zone of osseointe-
gration and the oral cavity represents a pathological
pocket. Implants can be placed deep into bone, par-
ticularly in the esthetic zone, which leads to a long
soft-tissue tunnel compared with a tooth with a
healthy periodontium. Often, deeper probing pocket
depths are found at implant sites inserted in partially
edentulous ridges compared with totally edentulous
ridges. The differences in the mucosal thickness in
areas adjacent to the natural dentition compared
with more uniform underlying edentulous ridges can
explain these findings (79).
Kan et al. (49) studied the dimensions of healthy
peri-implant mucosa of 45 maxillary anterior single
implant crowns with a mean functional time of 3
(range: 1–6) years, and reported that the interproxi-
mal thickness of the mucosa was approximately
6  1.2 mm (mean  standard deviation). The
majority of implant patients are currently partially
edentulous. In some groups, single tooth replacement
is provided in more than 50% of all implant patients
(32). In these situations, the mesial and distal probing
pocket depths measured at implants are routinely
between 4 and 8 mm, depending how scalloped the
mucosa is (39). A recent 6-year study by Buser et al.
(19), on the esthetic appearance of single tooth
207
Coli et al.
implants, showed an average probing pocket depth of
4.2  0.5 mm associated with a low sulcus bleeding
index of 0.16 and a minimal crestal bone loss of
0.4 mm after 6 years of function.
The thickness of the healthy soft tissues surround-
ing implants was calculated in Beagle dogs as being,
on average, 3.8 mm with a standard deviation of
0.65 mm (11). These figures indicate that the mea-
surements, representing close to 97.7% of the popula-
tion, range from 1.85 to 5.75 mm. These animal data
were confirmed in a clinical study which obtained
values ranging from 0.85 to 6.85 mm for healthy soft-
tissue around implants. The authors observed papilla
regrowth when the contact point to the bone crest
was ≤ 5 mm, but even papillae of 7–9 mm were
observed (22).
Long-term investigations on humans have clearly
shown that the probing depth of healthy peri-implant
mucosa is not always < 4 mm (50) but, in fact, often
> 4 mm (60–63% of cases) (10, 60), and up to 6 mm
[15% in the study of Lekholm et al. (60)], and that
successful implants with over 18 years of function
might have a history of probing pocket depth of up to
9 mm (10).
In the light of all this compelling evidence from ani-
mal, as well as human, studies, it seems illogic and
unreliable to diagnose an implant as having peri-
implantitis because of a pre-established probing
pocket depth value, as probing pocket depth values
of 6–9 mm have been described as being in the upper
range of those found in association with successful
dental implants.
Is an increase in probing pocket depth a
sign of bone loss?
Animal studies
The scientific evidence provided to support the state-
ment from the 6th European Workshop of Periodon-
tology (44), that an increase in probing depth over
time would be associated with attachment and bone
loss, is based on three animal investigations. The first
study used four monkeys (56) and reported a continu-
ous increase in probing pocket depth and soft-tissue
indices, as well as radiographic bone loss, at sites (im-
plants or teeth) where silk ligatures were applied for
8 months. The two other investigations were based
on the same experimental materials, with eight
cynomolgus monkeys, aiming to compare the clinical
and radiographic manifestations (76), or the stereo-
logic and histologic manifestations (77), of ligature-
induced marginal inflammation related to osseointe-
grated implants with those around ankylosed and
208
normal control teeth. The clinical manifestations, as
expressed by plaque, gingival scores, probing depth
and attachment loss, were reported to be similar for
implants, ankylosed teeth and control teeth on which
ligatures were applied, whereas the radiographic fea-
tures differed. Significant loss of bone height was lim-
ited to implants and ankylosed teeth and did not
occur in relation to normal control teeth. Thus, it is
important to note that radiographic examination was
better than probing assessments at separating the
sites with bone loss (implants and ankylosed teeth)
from those without bone loss (control teeth).
In the same consensus report on peri-implant
probing, the study by Lang et al. (57) (previously
mentioned) was used, together with another animal
study (78), to provide evidence that periodontal prob-
ing is a reliable tool for diagnosing peri-implant
health and disease. A comparison was made of the
apical position of probe tips at implants and teeth of
eight cynomolgus monkeys in conditions of: (i)
healthy peri-implant mucosa/gingiva; (ii) mild
mucositis/gingivitis; (iii) severe mucositis/gingivitis;
or (iv) peri-implantitis/periodontitis (78). It was con-
cluded that the probing measurements around
implants and teeth were different and that even mild
marginal inflammation was associated with deeper
probe penetration around implants in comparison
with teeth. In other words, an increase in probing
depth around an implant did not necessarily mean
that bone loss had occurred, but it could have been
caused by a change in condition of the peri-implant
soft tissues, from healthy to only mildly inflamed.
Thus, an analysis of the data presented in most of the
investigations discussed above does not support con-
sensus statements claiming that an increase in prob-
ing depth over time would be associated with bone
loss (‘attachment loss’, according to the consensus
report).
Human studies
In a 5-year prospective study with 112 implants,
Weber et al. (84) evaluated the correlation between
bone-level changes and clinical parameters such as
suppuration, plaque and bleeding indices, probing
depth, attachment level and mobility. The authors
reported low levels of correlation between the indices
and their ability to predict future peri-implant bone
loss and concluded that these parameters, among
them probing pocket depth, are of limited clinical
value in assessing and predicting future peri-implant
bone loss. Similar findings were reported in another
clinical investigation, with a follow-up of 9 years,
using clinical, microbiologic and biochemical
 Tools for monitoring peri-implant health

parameters to assess 61 maxillary anterior implants. Bleeding on probing as assessment

The study showed poor correlation between probing
of periodontal conditions
pocket-depth changes and bone-level changes as
bone stability and healthy peri-implant soft tissues
A series of investigations in the late 1980s and early
were detected in sites with increased probing pocket
1990s provided scientific evidence for the use of bleed-
depth values (41).
ing on probing as a tool for assessing periodontal condi-
One important aspect to be considered is the rele-
tions and as a diagnostic test for predicting future
vance of different types of investigations in providing
periodontal attachment loss (53–55). Lang et al. (54) fol-
clinical guidelines. The relevance of different investi-
lowed 41 periodontally treated patients (3807 sites) in a
gations to the clinical situations varies hugely,
maintenance care program for 2.5 years. The recall
depending on the type of study, and is often referred
intervals were 2–6 months, and bleeding on probing,
to as the ‘evidence pyramid’. At the base of the pyra-
probing pocket depth and probing attachment level
mid are ideas or laboratory research. These ideas are
were measured at every recall. Based on the data col-
then tested in laboratory models, then in animals and
lected, the diagnostic utility of bleeding on probing in
finally in humans. As you move up the pyramid, the
identifying sites with disease progression was evaluated.
relevance of the investigation to the clinical setting
A periodontal site was defined as diseased if a loss of
increases (Fig. 4). ‘In vitro’ and animal studies are at
probing attachment level of 2 mm or more was
the lowest level of scientific relevance to clinical situa-
detected between the baseline measurement and the
tions. Investigations in humans increase the rele-
final probing attachment level measurement. The test
vance, moving from case reports to case series, case–
was defined as positive for the sites showing an inci-
control studies, cohort studies, randomized control
dence of bleeding on probing of five or six times out of
studies, randomized controlled double-blind studies,
the total of six assessments during the 2.5 years. Thus, a
systematic reviews and meta-analyses.
periodontal site that showed bleeding on probing at five
It is important to note that of the few studies claim-
or six of the six assessments was judged to be positive
ing to provide evidence for the use of probing pocket
to the test and therefore would have been expected to
depth around implants, all are exclusively based on
show a probing attachment level loss of at least 2 mm.
the use of animal models. Furthermore, these investi-
The strength of a diagnostic test is judged on its
gations (56, 57, 76–78) rely on the ligature model,
ability to identify diseased subjects within a given
which clearly represents a ‘foreign body on another
population. Therefore, the strength is defined by its
foreign body (the implant)’, as recently discussed by
sensitivity (the ability of the test to identify correctly
Albrektsson et al. (5), and elicits a stronger foreign
the diseased subjects) and its specificity (the ability
body reaction to the one already present around the
to identify correctly those subjects that do not have
dental implant. The relevance of this model to the
the disease) (6). In Lang’s study, bleeding on prob-
clinical reality can be strongly questioned (35). Based
ing (as a diagnostic test), was proven to have a low
on the data and investigations discussed above, it can
sensitivity (29%) and a relatively high specificity
be concluded that probing pocket depth assessment
(88%). In other words, the presence of bleeding on
around implants appears to be a poor diagnostic tool.
probing at a periodontal site was a poor predictor of
future disease progression, but absence of bleeding
on probing at a site was a good predictor of future
stability (Fig. 5). For this reason, the use of bleeding
on probing in daily practice was recommended.
A very important parameter affecting the efficacy of
a diagnostic test is the prevalence of the disease in a
given population to which the test is applied (6). The
prevalence is defined as the number of cases of a dis-
ease that is present in a population at a specific time
point (68). As an example, a diagnostic test with a good
sensitivity (95%) and specificity (95%), applied to a
population with a disease prevalence of 10%, would
result in a 68% probability that a person with a positive
test result has the disease. Thus, a person with a posi-
Fig. 4. The evidence pyramid. RCTs, randomized control tive test result would have a 32% probability of not
trials.

209
Coli et al.

Fig. 5. Evaluation of a diagnostic test. BoP, bleeding on probing; PAL, probing attachment level.

having the disease (52). In a population in which the Bleeding on probing as assessment
disease prevalence is 1%, a person with a positive test
of peri-implant conditions
result has a 16% probability of having the disease and
a 84% probability of being healthy. With decreasing
In the 6th consensus report of the European Work-
disease prevalence, the more likely it becomes that a
shop of Periodontology (44), and maintained in the
person with a positive test result does not have the dis-
following European Workshops of Periodontology (58,
ease. In other words, with a low disease prevalence,
75), bleeding on probing is claimed to indicate the
the probability of a person (or, in the case of periodon-
presence of inflammation in the peri-implant mucosa
titis, of a site) to have the disease when the test is posi-
and to be a predictor for future loss of tissue support.
tive is very low (Table 1).
Therefore, it is recommended for bleeding on probing
As previously discussed, bleeding on probing
to be included in routine inspection of dental
showed low strength as a diagnostic test for the pro-
implants. The previously mentioned investigation of
gression of periodontitis, with sensitivity and speci-
Ericsson & Lindhe (33), in Beagle dogs, showed that
ficity values much lower than 95%. Therefore, if
the tip of the probe penetrates the junctional epithe-
bleeding on probing was applied to the general popu-
lium and results in bleeding on probing for the major-
lation, the probability that a periodontal site would be
ity of healthy implant sites. On the other hand, Lang
affected by periodontitis when found to be positive to
et al. (57) reported that bleeding on probing in Beagle
bleeding on probing would be low, resulting in exten-
dogs was detected in 0% of healthy sites, in 67% of
sive over-diagnosis and over-treatment of sites and
mucositis sites and in 91% of peri-implantitis sites.
patients. This is the reason why bleeding on probing
Only two clinical investigations are cited in the
can only be used as a diagnostic tool and as an indica-
Consensus report (44) and provide rather poor scien-
tor for treatment in patients where a diagnosis of peri-
tific support for the use of bleeding on probing as a
odontitis is (or can be) established in association with
predictor of loss of tissue support. In the first study
other diagnostic signs such as probing pocket depth
cited, Jepsen et al. (48) included 25 patients with
of ≥ 4 mm and radiographic detection of bone loss.
overdentures. Clinical parameters and crevicular fluid
samples were assessed at baseline and again
Table 1. Effect of disease prevalence on the positive
predictive value of a test with 95% sensitivity and 95% 6 months later. A site was defined as having progres-
specificity sive peri-implant tissue breakdown in case of 1 mm
probing attachment loss between the two assess-
Prevalence (%) Positive predictive value (%)
ments. No statistically significant difference in bleed-
0.1 1.9 ing on probing at the baseline examination was
detected between sites showing progressive peri-
1 16
implantitis and stable sites (40 vs. 34%). Hence, the
10 68 predictive value of bleeding on probing for bone loss
20 83 was not proven. The authors also pointed out that
peri-implant probing may provoke a nonspecific
50 95
bleeding that is unrelated to the amount of

210

inflammation in peri-implant tissues. Evaluation of
the diagnostic tests revealed that both bleeding on
probing and crevicular fluid test results were of lim-
ited value in the site-specific diagnosis when exam-
ined as positive predictors for peri-implant
attachment loss. However, both tests demonstrated
high negative predictive values. An important draw-
back of this study is that the definition applied for
peri-implantitis did not fulfil the definition of peri-
implantitis as an inflammation with loss of support-
ing bone. Owing to the absence of radiographs, the
authors never evaluated or reported on changes in
crestal bone levels. Also, as discussed previously,
probing depth around implants may be affected by
the temporary inflammatory conditions of the soft
tissues and is poorly correlated to real changes in
bone level. Furthermore, based on the known errors
of probing in periodontal research (43), it is strongly
questionable whether 1 mm probing attachment loss
can be applied as a threshold for progression of dis-
ease.
In the second investigation cited, Luterbacher et al.
(67) evaluated the diagnostic value of bleeding on
probing and of microbiological testing in identifying
sites with progressive peri-implantitis. Nineteen
patients, with a known history of periodontitis before
implant treatment and under supportive periodontal
therapy, were selected. The tooth–implant and
implant-supported restorations had been in function
for 3 years before collection of baseline data for the
investigation. The study was terminated at the 5-year
follow-up appointment from implant placement.
During the 2 years of the study period (the fourth and
fifth years of the follow-up period), diagnostic tests
were performed (under five to eight recall visits in
total) at one implant site and at one tooth site for
each patient. Disease progression was defined as an
increase in probing pocket depth of 2.5 mm over
5 years (0.5 mm annually) or as reduction in bone
density between year 1 and year 5, as detected by
computer-assisted digital image analysis. According
to the definition of disease progression, eight of 19
tooth sites and 10/19 implant sites showed loss of
periodontal or peri-implant support, respectively. In
addition, 11/19 tooth sites and nine of 19 implants
were reported to be stable. The diagnostic character-
istics of bleeding on probing using various thresholds
for a positive test outcome were presented. Any peri-
implant site bleeding at more than half of the recall
visits over the 2-year period showed disease progres-
sion at the end of the 2 years. Thus, the positive pre-
dictive value (of bleeding on probing > 50%) was
found to be 100%. It was concluded that ‘bleeding on
Tools for monitoring peri-implant health
probing is a useful clinical parameter for predicting
peri-implant and periodontal attachment loss’. The
continuous use of bleeding on probing, using a light
standardized probing force (0.2–0.25 N), was recom-
mended to monitor periodontal and peri-implant sta-
tus. Unfortunately, this investigation does not present
the data regarding the potential presence of bleeding
on probing in stable sites or the statistical compar-
ison between stable and diseased sites for bleeding
on probing. Being critical, one could suggest that per-
haps most of the implants were positive for bleeding
on probing, as shown in other studies. This study,
often quoted in consensus reports, appears to have
some serious drawbacks. An increase of probing
pocket depth over a certain threshold was used as a
definition of a site with peri-implantitis, which again
is not in agreement with the definition of peri-
implantitis that requires evidence of bone loss, with
or without increase of probing pocket depth. Further-
more, probing pocket depth measurements were not
collected at the start (baseline) of the investigation,
but only after 1 year of function and at the 5-year
examination. As the definition of disease progression
in this study could be based on changes in probing
pocket depth only, it would have been more relevant
to have the probing pocket depth measurements
taken at the start of the study (at the start of the last
2-year follow-up). A positive bleeding on probing
result could have been the consequence of probing in
a deeper pocket, now stable, rather than an indica-
tion of disease progression. It should also be noted
that in four of the 19 patients, the radiographic docu-
mentation could not be used and that again the dis-
ease progression was defined solely on the basis of
their changes in probing attachment level. Consider-
ing the incomplete data set and the statistically
underpowered study, the evidence to recommend
bleeding on probing as a useful clinical parameter for
predicting future peri-implant attachment loss is
rather poor. As previously discussed, Lekholm et al.
(60) reported that the indications of bleeding on
probing and deep pockets at the clinical examination
were not found to be accompanied by accelerated
marginal bone loss, or by microflora or histologic
changes indicative of peri-implantitis.
Prevalence of peri-implant disease
As discussed above, independently of sensitivity and
specificity, the ability to use bleeding on probing as a
diagnostic tool is dependent on the prevalence of
peri-implantitis in the general population. Fransson
211
Coli et al.
et al. (38) established a diagnosis of peri-implantitis
for any implant site showing bleeding on probing and
any bone loss occuring between the 1-year and the
5-year (up to the 23-year) follow-up examinations.
Based on this peri-implantitis definition, Fransson
et al. (38) suggested a peri-implantitis prevalence of
28%. This value has been seriously questioned in a
follow-up study by Jemt et al. (47) on the same
patient material. Interestingly, in Fransson’s study
(38), bleeding on probing was detected in 93.9% of
the implants with ‘progressive’ bone loss and in
90.9% of the implants with a stable bone level.
Roos-Jans aker et al. (73) reported that peri-implant
mucositis, diagnosed by bleeding on probing, was
detected in approximately 70% of functioning
implants after 9–14 years. Bone levels ranging from
one to five implant threads below the abutment–im-
plant interface were found in 33% of the implants.
The prevalence of peri-implantitis, defined as bone
loss of at least 1.8 mm following the first year of func-
tion, combined with bleeding on probing and/or pus,
was 16% at patient level and 6.6% at implant level. It
is worth pointing out that 42.2% of the implants had
stable bone levels and still showed bleeding on prob-
ing or suppuration, and 8.4% of the implants showed
bone-level gain, even in the presence of bleeding on
probing or suppuration.
In the Consensus of the 6th European Workshop of
Periodontology, Zitzmann & Berglundh (85) con-
cluded, in their review of these data, that peri-implant
mucositis has a prevalence of 80% at subject level and
a prevalence of 50% at implant level. The prevalence
of peri-implantitis was reported to be between 28%
up to 77% at subject level and between 12% up to
43% at implant-site level. The interpretation of these
data to achieve such a high prevalence of disease
should really be questioned. If peri-implant mucositis
and peri-implantitis were indeed widespread with
such high prevalences, and if bleeding on probing
alone or bone loss combined with bleeding on prob-
ing would indeed jeopardize the long-term survival of
the implants, the prevalence of implant loss would be
expected somehow to mirror the prevalence of peri-
implantitis in long-term investigations. Fortunately,
this is not the case and clinical long-term studies
show that peri-implantitis has a low prevalence and a
minimal impact in implant failures. In fact, long-term
studies on machined surface implants up to 22 years
of function show an implant-survival rate ranging
from 87 to 99.2%. Mean bone loss ranges from 0.03 to
0.05 mm/year. These investigations all report a poor
correlation between probing pocket depth and bone
loss (9, 10, 29), between bleeding on probing and
212
bone loss (29) and of a prevalence of peri-implantitis
(bone loss and bleeding on probing) ranging from 2.4
to 5% (8, 29). In one investigation, despite stable con-
ditions, bleeding on probing was detected at 81.4% of
implants and was more prevalent in deeper pockets,
although this was not correlated to bone-level mea-
surements (29).
The suggestion that the modern micro-rough
implant surfaces could result in an increase in peri-
implantitis (2, 14), compared with the machined
implant surfaces used in the above cited long-term
studies, is not sustained in recent papers. Many long-
term studies (over 10 years), on sandblasted or acid-
etched implant surfaces, report implant success rates
similar to or better than those for the turned implant
surfaces (95–99.2%) and a very low prevalence of
peri-implantitis, ranging from 1.8 to 4.1% (18, 36, 70),
despite a high prevalence of bleeding on probing in
up to 87% of the implants (36). A review including 10
different studies on three brands of moderately rough
surfaces, with follow up of 10 years or longer,
assessed that more than 95% of all implants had a
highly predictable and successful outcome (4). Fur-
thermore, it was pointed out that estimates of bleed-
ing on probing and probing pocket depth had no
known correlation to marginal bone loss around oral
implants. Thus, long-term clinical studies, of up to
20 years, on machined implant surfaces, and more
recent long-term studies, of up to 10 years, on mod-
ern micro-rough implant surfaces, are indicative of a
low prevalence of peri-implantitis and implant losses
because of peri-implantitis (2–5%).
It seems that peri-implantitis, as presently defined,
is not a major threat for the long-term success of
implant restorations (45). For instance, a follow-up
study based on the population described by Fransson
et al. (37, 38) showed that 9 years after the diagnosis
of peri-implantitis, 31% of the patients presented with
implants with bone loss of > 2 mm/year or with
implant failures, whereas 69% showed no problems
with their implants (47). Moreover, 91.4% of the
implants in the patients diagnosed with peri-implan-
titis showed either no annual bone loss or annual
bone loss of < 0.2 mm during the 9 years from the
diagnosis. The authors reported a low prevalence of
obvious bone loss at implants (> 0.2 mm/year) with a
comparable distribution between ‘affected’ and ‘not
affected’ implants. Hence, the definition of peri-
implantitis used in the Fransson study (38), namely
bone loss associated with bleeding on probing, was
shown to be a poor predictor of future bone loss and
implant failure and consequently a poor indicator of
treatment needs.

The definition of peri-implantitis as any loss of
marginal bone and bleeding on probing appears to be
inappropriate because several long-term investiga-
tions have shown that up to 90% of implants with
stable bone conditions bleed on probing. Thus,
bleeding on probing is not a characteristic only of
inflamed/diseased peri-implant soft tissues, but also
of the majority of healthy tissues. Therefore, bleeding
on probing cannot be reasonably used to distinguish
between healthy and diseased sites.
Considering the effect of low disease prevalence on
the efficacy of a diagnostic test to distinguish between
disease and healthy conditions, even with a strong
diagnostic test, the use of probing around implants
for bleeding on probing and probing pocket depth
assessment in a general population does not appear
to be justified. Their use would result in a high false-
positive value and the consequence would be over-
treatment of the majority of healthy sites. This is of
no benefit to patients and clinicians. From the long-
term longitudinal studies it appears that the majority
of implants with a diagnosis of peri-implantitis (based
on the actual definition of peri-implantitis) would not
need treatment because an annual bone loss of 0.1–
0.2 mm and bleeding on probing do not seem to
affect the longevity and the success rate of implants
and of their related restorations.
A systematic review of peri-implantitis therapy
showed that probing pocket depth, bleeding on
probing and clinical attachment level were the sur-
rogate markers most frequently reported for impor-
tant clinical events, such as implant failure, despite
the fact that these surrogate markers/end points
have not yet been validated (34). The authors
pointed out that surgical/nonsurgical treatments
aiming to improve probing pocket depth, bleeding
on probing and clinical attachment level around
dental implants do not necessarily improve the
long-term survival of the implants. This is because
these surrogate end points might not capture the
long-term true outcome in the form of implant fail-
ure as other factors might be more important in
maintaining/saving the implants. In other words,
studies that make the assumption that the goal of
peri-implantitis treatment should be a reduction in
probing pocket depth, bleeding on probing and clin-
ical attachment level (because these parameters
would be directly related to overall implant survival)
have no evidence for this assumption. It has already
been reported in the medical literature that in some
situations the use of nonvalidated end points may
be more harmful than beneficial (23). Indications
for treatment and assessment of the ‘real effect’ of a
Tools for monitoring peri-implant health
therapy should be based on strong and validated
end points (true or surrogate). This is particularly
important when complex interventions and expen-
sive materials are used. For example, a patient
receiving treatment for peri-implantitis with bone
substitutes plus membranes (guided bone regenera-
tion) should be clearly informed that the potential
additional gain in millimetres of surrogate end
points, such as probing pocket depth and clinical
attachment level, will not guarantee long-term
implant maintenance compared with no treatment
or nonsurgical treatment (30, 34). If true end points,
such as implant loss, are to be replaced with surro-
gate end points, such as probing pocket depth and
bleeding on probing, in providing indications for
potentially expensive treatment and for measuring
treatment outcomes, it is obviously very important
that these surrogate end points are thoroughly vali-
dated. Probing pocket depth and/or bone-loss val-
ues, associated with bleeding on probing, for the
definition of peri-implantitis (and the associated
extensive treatment needs), arbitrarily established in
investigations or by Consensus meetings, need to be
strongly tested and validated to avoid the risk of
epidemic over-treatments. For instance, in the
much-cited investigations of Fransson and cowork-
ers (37, 38), the arbitrary choice of a defined bone
loss in association with bleeding on probing (surro-
gate end points) for the definition of peri-implanti-
tis, resulting in a prevalence of peri-implantitis of
28%, did not capture the long-term true outcome
(end point) in the form of implant failure and could
have resulted in massive over-treatment of implant
patients, as discussed above. In fact, patients treated
by oral hygienists and/or who had experienced peri-
implantitis surgery did not show any more favorable
progression of bone loss compared with nontreated
patients (47).
Another example is the alarmistic editorial by Gian-
nobile & Lang (40), in which it is claimed that peri-
implant mucositis and peri-implantitis are common
biologic complications potentially jeopardizing the
longevity of reconstructions on implants and ques-
tioning the long-term success rates of implant treat-
ment, on the basis of yet another epidemiological
study using bleeding on probing and a defined
threshold for bone loss for the diagnosis of peri-
implant diseases (26, 27). The epidemiologic study in
question, based on a heterogeneous Swedish popula-
tion, treated by a mix of general dentists and special-
ists in private, as well public, settings, showed that
over 90% of the patients were satisfied with the
implant treatment and that only 2% of the implants
213
Coli et al.

Table 2. Estimated frequencies of peri-implant diagnoses when applying the Association of Dental Implantology
guidelines (82) on four published 10-year follow-up studies in relation to the true frequencies of peri-implantitis as
reported by the respective authors

Study Diagnosis according to Association of Dental Implantology guidelines Diagnosis according

to authors

Healthy implant Mucositis Peri-implantitis Peri-implantitis Peri-implantitis

Probing pocket Probing pocket Probing pocket Probing pocket
depth < 3 mm depth < 3 mm depth > 3 mm depth > 3 mm
No bleeding Bleeding on Bleeding on Bleeding on
on probing probing + plaque probing + plaque probing + plaque
No clinical No clinical bone Clinical bone Clinical bone
bone loss loss loss < 2 mm loss > 2 mm

€
Ostman 22.6 66.1 11.3 1.9
et al. (70)

Fischer 4.9–27.1 68–87 4.9–8.1 2.1

et al. (36)

Gotfredsen 2.5–35.5 62 2.5 2.5

et al. (42)

Buser 11.3 34.9–49.5 4.4 1.8

et al. (18)
Values are given as %.
Note the large number of implants that are regarded as unhealthy, according to the Association of Dental Implantology guidelines, and thus require surgical or non-
surgical treatment in spite of good function, as reported by the respective authors.

(in 4.2% of the subjects) were lost during 9 years of
function. In contrast to the authors’ interpretation of
the data, leading to the conclusion that ‘implant fail-
ure is not an uncommon event’, one could in fact
rejoice the brilliant result of 98% of the implants
being in function after 9 years, with over 90% of the
treated patients reporting to be satisfied or highly sat-
isfied with the regained esthetics and function (26–
28). Thus, the application of nonvalidated surrogate
end points might lead to incorrect diagnoses and
unjustified treatment recommendations, which do
not seem to be of benefit for the patient. The poten-
tial problems arising can be well pictured in Table 2,
in which several 10-year follow-up studies with sur-
vival rates between 95.1 and 99.2% (using true end
points such as implant survival) and minimal soft-tis-
sue complications, show a prevalence of peri-implan-
titis and consequent treatment needs between 34.9
and 87% if the Association of Dental Implantology
guidelines were applied (82).
Conclusions
 Probing depth at a healthy peri-implant mucosa
can be far deeper than 4 mm. Therefore, probing
pocket depth values of > 4 mm at dental implants
cannot be seen as a sign of pathology or an
alarming signal regarding the conditions of the
peri-implant tissues.
 An increase of probing pocket depth values over
time is not necessarily associated with loss of sup-
porting bone around dental implants. Therefore,
probing does not appear to be a reliable tool for
the assessment of peri-implant marginal soft- and
hard-tissue conditions.
 From a biomaterials science point of view,
osseointegration is a foreign-body reaction. As a
consequence, bleeding on probing does not
always indicate the presence of acute inflamma-
tion in the peri-implant mucosa, but may rather
reflect the nature of the scar tissue–implant inter-
face. Therefore, bleeding on probing does not
appear to be a predictor for future loss of tissue
support. Similarly, absence of bleeding on probing
does not appear to be a predictor of future stabil-
ity. Hence, probing pocket depth and bleeding on
probing cannot be considered to be reliable tools
for monitoring peri-implant health and disease.
 Radiographic evaluation of crestal bone levels
over time seems to be the most reliable tool to
identify those implants undergoing continuous
bone loss and therefore in need of treatment
(24).
 A single episode of bone loss does not necessarily
call for treatment unless associated with clear signs

214

of inflammation, such as profuse bleeding/suppu-
ration and discomfort at pressure/palpation.
Proposed clinical approach to peri-
implant complications
The authors of the present review believe that good
oral hygiene and maintenance is a prerequisite for
good long-term outcomes with dental implants. We
also believe that peri-implantitis, irrespective of the
cause, is a clinical complication that needs to be
properly treated and may pose a risk for survival of
the implant. However, the concern we want to
address in this paper is that periodontal indices, such
as probing pocket depth and bleeding on probing, are
not sensitive for identification of peri-implant disease
and future risk for peri-implant crestal bone loss,
when used as standard diagnostic measures in clini-
cal routine. The long-term experiences and evidence
presented in the literature indicate that a zero-toler-
ance approach to bleeding, pocket formation and cre-
stal bone loss at implants is not justifiable. Instead,
these seem to reflect, in most instances, normal con-
ditions of well-functioning implant restorations, bear-
ing in mind that osseointegration is a biologically
abnormal situation. Therefore, the use of probing
pocket depth and bleeding on probing assessments
lead to over-diagnosis and over-treatment of
assumed peri-implantitis lesions.
It is the opinion of the authors of the present
review that, based on the current degree of knowl-
edge, the only justifiable approach to peri-implant
disease is to deal with it when it is a clinical problem
based on patient’s symptoms (discomfort, pain, etc.),
presence of swelling, redness and pus and significant
crestal bone loss over time, as verified with radiogra-
phy. The treatment should aim at resolving the infec-
tion, which could include removal of the implant.
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