Braz J Oral Sci.

12(2):95-99
Original Article Braz J Oral Sci.
April | June 2013 - Volume 12, Number 2
Is bleeding on probing a differential diagnosis
between periimplant health and disease?
Priscila Ladeira Casado
1
, Ricardo Villas-Bas
2
, Luana Cristine Leo da Silva
3
,
Cristiana Farias de Carvalho Andrade
3
, Letcia Ladeira Bonato
4
, Jos Mauro Granjeiro
5
1
Area of Morphology, Cell Therapy Center - Clinical Research Unit and Biology Institute, Fluminense Federal University Niteri, RJ, Brazil and
Orthopedics and Traumatology National Institute, Rio de Janeiro, RJ, Brazil
2
Area of Dentistry, Veiga de Almeida University, Rio de Janeiro, RJ, Brazil
3
Dentist, Veiga de Almeida University, Rio de Janeiro, RJ, Brazil
4
Dentist, Juiz de Fora Federal University, Juiz de Fora, MG, Brazil
5
Area of Chemistry, Cell Therapy Center - Clinical Research Unit and Biology Institute - Fluminense Federal University - Niteri, RJ, Brazil and
National Institute of Metrology - Rio de Janeiro, RJ, Brazil
Correspondence to:
Priscila Ladeira Casado
Ncleo de Terapia Celular
Unidade de Pesquisa Clinica
Rua Marques de Paran 303, 40 andar,
CEP: 24033-900 - Centro, Niteri, RJ, Brasil
Phone / Fax: +55 21 26299255
E-mail: [email protected]
Abstract
As far as the periimplant anatomy is considered, the question raised is whether or not healthy
periimplant tissues present bleeding on probing (BOP). Aim: To assess if the criterion BOP is
strictly related to periimplant disease (PID). Methods: 134 patients were included in this study. All
periimplant regions were clinically and radiographically evaluated. Patients were assigned to 3
groups based on radiographic and clinical aspects in the periimplant region: Group A (healthy-
sites) - no signs of mucosal inflammation or bone loss; Group B (mucositis) - red and swollen
mucosa, but no radiographic bone loss; Group C (periimplantitis) - radiographically confirmed
pathological bone loss. After this classification, all periimplant sulci were probed at 4 sites (mesial,
distal, buccal, lingual/palatal). Patients mean age was 51.712.4 years, 77 women and 57 men,
with a total of 486 osseointegrated endosseous implants. Results: Groups A and C showed
significant difference in age and implant region distribution (p=0.009 and p=0.008, respectively).
After initial clinical and radiographic diagnosis of periimplant status, 33 (20.1%) regions showed
BOP in group A. All regions in Group B presented BOP. In Group C, 41 (19.9%) regions showed
no BOP. All groups differed significantly considering BOP as diagnosis parameter (p<0.0001).
Conclusions: BOP was always present in inflamed mucosa, but it was not always absent in
healthy mucosa. Not all periimplantitis regions showed BOP. Clinical and radiographic aspects
must always be considered together for diagnosis of PID, even if BOP is absent.
Keywords: inflammation, periimplantitis, diagnosis.
Introduction
The soft and hard tissues around endosseous implants share some similarities
with the periodontium. However, differences such as the absence of cementum
and periodontal ligament in the periimplant region, orientation of the collagen
fibers in the periimplant soft tissue, which is parallel to the implant surface and
not inserted in the implant surface and periimplant vascularization must be taken
into consideration to provide reliable prognosis
1
.
In natural dentition, the junctional epithelium provides sealing on the base
Received for publication: February 21, 2013
Accepted: June 11, 2013
96 96 96 96 96
Braz J Oral Sci. 12(2):95-99
of the periodontal sulcus against the penetration of chemical
pathogens and bacterial substances
2
. Rupture of this sealing
or lysis of connective tissue fibers attached to the apical
cementum to the junctional epithelium, lead to rapid
migration of the sulcular epithelium and consequent
pathological pocket formation. Since cementum or fiber
attachment is not seen around the titanium surface, mucosal
seal provides the main barrier against the dissemination of
pathological aggressions in the deep periimplant tissues. The
sealing around endosseous implants, which has weak
adherence to the titanium structure, is provided by the
presence of junctional epithelium, sulcular epithelium and
connective tissue by hemidesmosomes. The destruction of
the mucosal integrity around the titanium leads to the direct
extension of the pathological pocket to the bone tissue, which
may result in loss of the endosseous implant
1-3
.
Several reports emphasize the importance of the presence
of healthy gingival tissues around dental implants as being
the key factor not only for aesthetics, but also for long-term
success
2,4-5
. However, correct and early clinical diagnosis of
periimplant disease status is frequently critical, which makes
maintenance of the periimplant tissue difficult
6
. According
to the Seventh European Workshop on Periodontology, the
clinical parameters that indicate periimplant disease are
bleeding on probing (BOP) and increased probing depth
7
.
Clinical studies have shown that the key parameter for the
diagnosis of periimplant mucositis is bleeding on gentle
probing. Periimplantitis is characterized by changes in the
level of the crestal bone in conjunction with BOP with or
without concomitant deepening of periimplant pockets.
Presence of pus, gingival recession, fistula, edema and
hyperplasia are other common conditions found in
periimplantitis sites
6,8
. However, the radiographic detection
of periimplant bone loss shows only the involvement of the
proximal areas to the implant, and thus periimplant probing
as a diagnostic procedure is advisable to detect bone loss on
all faces
9
. In addition, probing in periimplant sulci allows
evaluating the clinical probing depth, the distance between
the marginal soft tissue and a reference point on the implant
(for identification of hyperplasia or gingival recession), BOP
and suppuration from the periimplant pocket
10
.
Regarding the clinical probing depth, it is important to
consider that in inflamed tissues around the implants the
probe penetrates close to the bone level, while in healthy
tissues the probe tip tends to stop at the histological level of
connective tissue attached to the implant. The inflamed tissue
with loss of connective tissue does not seem to inhibit the
penetration of the probe beyond the apical extension of the
junctional epithelium
11-12
. Quirynem et al.
13
(1991) found a
relation between the bone level identified by the radiographic
exam and the penetration of the probe into the periimplant
tissue. In screw-retained implants, the probe tip stops 1.4
mm coronally to the bone level.
This way, despite the fact that BOP is a diagnosis for
periimplant disease, it is important to mention that, according
to Ericsson and Lindhe
14
(1993), bleeding, though unusual
in healthy periodontium, is frequently found in most healthy
periimplant tissues. Ferreira et al.
15
(2006) stated that it is
still not clearly defined if BOP of periimplant tissues would
be a parameter for identifying the presence of periimplant
disease. Some studies suggest that periimplant mucosa may
be more sensitive to probing forces, causing more BOP when
compared with teeth
16-17
.
The correct diagnosis of periimplant disease is a critical
procedure, which makes it difficult the periimplant tissue
maintenance
6
. Actually, a clinical standard to diagnose
periimplant disease is based on the presence of BOP with
probing pocket depth e4 mm for mucositis diagnosis and
additional radiographic bone loss for correct periimplantitis
diagnosis
8
.

During the first year after abutment connection,
1 mm of marginal bone loss is allowed, followed by 0.2 mm
loss per year
18
. Currently, these criteria are still frequently
referred to as the gold standard for implant success
19
.
In the present study, we considered previously
established clinical characteristics of periimplant tissues that
justify the exclusion criterion of BOP to diagnose the presence
of periimplant disease. Based on periimplant anatomy, the
tested hypothesis is that healthy periimplant tissues can also
present BOP. Thus, the aim of this study was to assess if BOP
is directly related to the presence of periimplant disease.
Material and methods
Clinical study procedures were conducted according to
the Veiga de Almeida University Ethical Boards
recommendations (Process# 238/10).
Patient Selection
One hundred and thirty-four nonsmoking patients without
any systemic disease (77 women and 57 men; mean age of
51.712.4 years), presenting a total of 486 osseointegrated
endosseous implants, 295 in the maxilla and 191 in the
mandible, were randomly selected for this study (Table 1).
Patients signed an informed consent form after receiving full
information about the study nature and purposes.
Patients were admitted to the study if they had no
medical complications, were not taking medications affecting
periodontal status as described by Soskolne
20
(1997) and
had immediate postoperative radiographs showing the vertical
bone level around the implant in order to compare bone
levels after osseointegration period. Patients who had
undergone any periodontal or periimplant therapy within
the last six months were excluded from the study.
All periimplant regions were clinically and radiogra-
phically evaluated. Clinical examination of the periimplant
sites consisted of visual inspection and palpation, analysis
of mucosa color, plaque accumulation, edema and implant
mobility. Conventional periapical radiographs using the
paralleling technique measured the presence of vertical bone
loss adjacent to the implants. The height of periimplant bone
around the implant was recorded according to the exposure
of the screw. According to the clinical and radiographic
characteristics of the periimplant sites, patients were divided
into 3 groups. Patients in Group A (healthy sites) showed no
Is bleeding on probing a differential diagnosis between periimplant health and disease?
Braz J Oral Sci. 12(2):95-99
visual clinical signs of inflammation in the periimplant mucosa
and no signs of bone loss. In Group B, periimplant sites
characterized as mucositis, presence of mucosae presenting
red color and swelling, but no signs of pathologic bone loss.
Patients in Group C (periimplantitis sites) showed implant
mobility and suppuration in some cases, and radiographic signs
of pathologic bone loss (more than 2 screws exposed).
After initial classification, the periimplant sulci from
Groups A, B and C were gently probed at 4 sites around each
implant and the presence of BOP was recorded by a previously
trained clinician. Periimplant measurements were recorded
using a millimeter conventional U.N.C. periodontal probe, (Hu-
Friedy, Chicago, IL, USA). Then, if bleeding was detected
at any of the sites, a classification of BOP was established.
Statistical Analysis
The data of each, including clinical and radiographic
characteristics, were submitted to descriptive statistical
analyses considering age, gender, region and presence of
BOP using the statistical software SPSS version 12.0 (SPSS
Inc., Chicago, IL, USA). Numerical variables were expressed
as frequencies and percentages. The chi-square test was
performed to assess the significance of nominal variables
between groups. Continuous variables as age were expressed
as mean and standard deviation. Then, after Shapiro-Wilk
test, ANOVA was applied and parametric analysis (Students
t-test) was used to compare means between groups considering
that the variable had a normal distribution. The significance
level was set at 5%.
Results
Taking into consideration baseline characteristics,
Groups A and C showed statistically significant difference
in age and implant region distribution (p=0.009 and
p=0.008, respectively). In Group A (healthy periimplant
tissue), 131 (19.1%) periimplant regions were characterized
by the absence of BOP while 33 (20.1%) regions showed
BOP with no clinical or radiographic signs of inflammation.
All periimplant regions (100%) in Group B (periimplant
mucositis) characterized by clinical signs of inflammation
(red color of mucosa and swelling) and no radiographic bone
loss, presented BOP. In Group C (periimplantitis), 165 (80.1%)
regions around the implants showed BOP together with
pathologic bone loss and 41 (19.9%) regions presented no
signs of BOP even with bone loss. Periimplant mobility was
present in 6 implants in Group C (2.9%). Group A showed no
inflammation in mucosa while group B showed inflammation
in all periimplant mucosal tissues, helping differential clinical
diagnosis. However, group C showed 118 (57.3%) regions
without any sign of mucosal inflammation even when
pathological bone loss was present. These results distinguished
one group from another by this criterion (p<0.0001). All
groups had significant differences considering BOP
(p<0.0001). Periimplant disease groups (B and C) showed
higher incidence of BOP compared to group A, which showed
lower incidence of BOP, despite the presence of bleeding. In
addition, when comparing disease groups, higher incidence
of BOP was observed in group B (p<0.0001 in all analyses
comparing BOP among the 3 groups). Table 2 shows the clinical
and radiographic findings in each group.
Discussion
This study evaluated the presence of BOP in periimplant
regions clinically and radiographically characterized as
healthy, mucositis and periimplantitis, excluding BOP as the
initial diagnostic factor. Healthy patients presented no signs
of visual clinical inflammation (red color or swelling) or
radiographic bone loss. Regions affected by mucositis were
characterized by visible clinical mucosal inflammation
without signs of bone loss, and periimplantitis regions (Group
C) were characterized as all regions with bone loss and more
than two exposed screws, considering the radiography
obtained to determine alveolar bone levels after physiologic
remodeling. The main question was: The presence of BOP is
really reliable when used as the unique parameter for disease
diagnosis? This study showed that after the initial diagnosis
97 97 97 97 97
Is bleeding on probing a differential diagnosis between periimplant health and disease?
Table 1. Patients baseline findings.
*p-values <0.05 are considered significant; CI: confidential interval;

chi-square test;
**
Student T-test
98 98 98 98 98
Braz J Oral Sci. 12(2):95-99
considering other clinical and radiographic parameters of
periimplant disease, the presence of BOP was secondary for
disease identification, taking into consideration that healthy
periimplant mucosae (without inflammation or bone loss)
showed BOP in 20% of cases.
According to the Seventh Workshop of Periodontology
7
(2011) the presence of BOP characterizes periimplant disease.
However, despite BOP being a diagnosis of periimplant
disease, bleeding, unusual in healthy periodontium, is found
in most healthy periimplant tissues
14
as evident in this work.
Therefore, according to Ferreira et al.
15
(2006) it has not been
clearly defined whether periimplant BOP could represent a
reliable parameter for identifying the presence of periimplant
disease. Some studies suggest that periimplant mucosa may
be more sensitive to probing forces, causing more BOP when
compared with teeth
16-17
. Luterbacher et al.
21
affirm that
absence of BOP represents a stable periimplant condition.
However, lack of keratinized tissue, a common finding after
implant placement surgery, could also simulate an inflamed
tissue, due to gingival manipulation and its red aspect, which
can also be associated with non-keratinized mucosa.
Therefore, swelling, pus and radiographic findings were
considered for diagnosis of mucositis.
The present study showed that 20% of patients
considered clinically and radiographically healthy had BOP
and all the periimplant regions with a clinical aspect of
inflammation (Group B - mucositis) had BOP, which lead to
the conclusion that BOP is always present in inflamed mucosa,
but it will not always be absent in healthy mucosa, obviously
due to periimplant anatomical reasons that, even in healthy
conditions, do not limit penetration of the probe beyond the
barrier in the epithelial junction. However, future studies are
required, including in vivo analysis in order to show how
the probe penetration can stimulate bleeding in healthy and
diseased periimplant mucosa.
Quirynem et al.
13
(1991) found a relation between the
bone level identified by the radiographic exam and the
penetration of the probe into the periimplant tissue. In screw-
retained implants, the probe tip appears to stop 1.4 mm
coronally from the bone level. In addition, the type of probe
used to measure clinically the depth does not seem to
influence the result. Christensen et al.
22
used different types
of probe to characterize CPD around endosseous implants
and they concluded that the differences between the analyzed
probe types during the research were not larger than 0.1 mm.
In this study only one type of probe was used, which
standardized the obtained results.
Another important consideration is that previous studies
claim that when changes in the clinical parameters indicate
disease (BOP, increased probing depth); the clinician is
encouraged to take a radiograph to evaluate possible bone
loss. The results of the performed research showed that 56%
of the regions affected by pathological bone loss
(periimplantitis Group C) showed healthy mucosa, which
in many cases leads the clinician not to perform a radiographic
exam and to an erroneous healthy diagnosis. Therefore, the
radiographic exam must be always considered as a follow-
up measure and not only due to the presence of BOP, for if
BOP is not present and bone loss has been triggered, possible
subclinical periimplantitis may be developing. The clinical
aspect as well as the radiographic aspect must be used as a
diagnostic factor of periimplant disease, even if BOP is absent,
instead of BOP guiding the radiographic analysis. In
Implantology, the follow-up should be performed by clinical
and radiographic examination at least once a year, to identify
underlying bone loss in an apparently healthy periimplant
gingival tissue and restore bone health before the implant
failure. In case of rapid progression of periimplantitis, the
following question arises: would rapid progression of
periimplantitis be a consequence of a late diagnosis based
solely on the clinical aspect of the mucosa?
From all patients with more than two exposed threads
(pathological bone loss), 20% did not show BOP. How can
this be explained? The study hypothesis is that in some
patients, even with pathological bone loss, the mucosal
epithelium remains adhered limiting the penetration of the
probe into the tissue due to some of the following reasons:
(1) bacterial penetration into the connective tissue is faster
and triggers a more aggressive inflammatory response in
periimplant bone, which would justify progressive bone loss
without prior involvement of the mucosa; (2) at some point,
mucosal inflammation might occurr with subsequent
periimplant bone loss and spontaneous mucosal healing after
routine cleaning procedures performed by the patient, as
mucositis is characterized for being a reversible lesion, but
the underlying bone shows pathological loss resulting from
prior involvement due to the irreversibility of periimplantitis;
(3) the thickness of the mucosa may influence the
dissemination of the disease to the underlying bone limiting
the damage to the thick mucosa, but further studies are needed.
Is bleeding on probing a differential diagnosis between periimplant health and disease?
Table 2. Clinical aspects in each group
*Reference for calculation= number of implants; BOP= bleeding on probing, measure considering the presence of bleeding
in at least one from the 4 analyzed aspects (mesial, distal, buccal, lingual/palatal); p values <0.05 are considered
significant;

chi-square test; () non measurable value due to values=0.

Braz J Oral Sci. 12(2):95-99
99 99 99 99 99
Correct diagnosis of periimplant disease is still difficult
to establish. Mobility of implants indicates the final stage
of the disease, characterized by complete loss of the bone/
implant interface
10
. Therefore, according to Heitz-Mayfield
6
(2008), mobility cannot be a parameter for early diagnosis
of periimplant disease, but it may indicate complete lack of
osseointegration, which requires the implant to be
immediately removed. In order to be able to intervene in the
development of periimplantitis before advanced bone loss,
it is important to diagnose the disease in its initial stage
10
.
In addition, according to Leito et al.
23
(2005) even when
significant inflammatory signs are absent in periimplant
tissue, the qualitative detection of pathogens may indicate
risk of periimplantitis, requiring stricter postoperative control.
In summary, several cases of failure found in this research
were not directly related to the presence of BOP. BOP is
always present in inflamed mucosa, but it will not always be
absent in healthy mucosa. It is also important to consider
that not all tissues presenting pathologic bone loss show
clinical signs of inflammation. In the present study was
considered that BOP alone cannot distinguish between the
presence and absence of periimplant health and other factors
involving a thorough clinical and radiographic characteriza-
tion of the disease should be considered. The clinical aspect
as well as the radiographic aspect must be always used as a
diagnostic factor of periimplant disease, even if BOP is absent.
The authors expect that this research can contribute to a
better diagnosis of periimplant disease, thus reducing the
rate of failures in implantology.
Acknowledgements
The authors would like to CAPES/FAPERJ for granting
funds for this study (E-26/102.288/2010).
References
1. Jovanovic SA. Diagnosis and treatment of peri-implant diseases. Curr
Opin Periodontol. 1994; 194-204.
2. Sumi T, Braian M, Shimada A, Shibata N, Takeshita K, Vandeweghe S et
al. Characteristics of implant CAD/CAM abutment connections of two
different internal connection systems. J Oral Rehabil. 2012; 39: 391-8.
3. Santos MCLG, Campos MIG, Line SRP. Early dental implant failure: a
review of literature. Braz J Oral Sci. 2002; 1: 103-11.
4. Kan JY, Rungcharassaeng K, Lozada JL. Bilaminar subepithelial connective
tissue grafts for immediate implant placement and provisionalization in the
esthetic zone. J Can Dent Assoc. 2005; 33: 865-71.
5. Pelegrini AA, Costa CES, Sendyk WR. Connective tissue graft: a clinical
alternative perimplant aesthetics. Case report. Implant News. 2006; 3:
249-54.
6. Heitz-Mayfield LJA. Peri-implant diseases: diagnosis and risk indicators.
J Clin Periodontol. 2008; 35: 292-304.
7. Lang NP, Berglundh T. On Behalf of Working Group 4 of the Seventh
European Workshop on Periodontology: Periimplant diseases: where are
we now? Consensus of the Seventh European Workshop on
Periodontology. J Clin Periodontol. 2011; 38(Suppl. 11): 178-81
8. Zitzmann NU, Berglundh T. Definition and prevalence of peri-implant
diseases. J Clin Periodontol. 2008; 35: 286-91.
9. Albrektsson TO, Isidor F. Consensus report of session IV, 1994 apud
Salvi GE, Persson GR, Heitz-Mayfield LS, Frei M, Lang NP. Adjunctive
local antibiotic therapy in the treatment of peri-implantitis II: clinical and
radiographic outcomes. Clin Oral Implants Res. 2007; 18: 281-5.
10. Mombelli A, Muhle T, Bragger U, Lang NP, Burgin WB. Comparison of
periodontal and peri-implant probing by depth-force pattern analysis. Clin
Oral Implants Res. 1997; 8: 448-54.
11. Lang NP, Wetzel AC, Stich H, Caffesse RJ. Histologic probe penetration
in healthy and inflamed periimplant tissues. Clin Oral Implants Res. 1994;
5: 191-201.
12. Khammissa RA, Feller L, Meyerov R, Lemmer J. Peri-implant mucositis
and peri-implantitis: clinical and histopathological characteristics and
treatment. SADJ. 2012; 67: 124-6.
13. Quirynen M, Van Steenberghe D, Jacobs R, Schotte A, Darius B. The
reliability of pocket probing around screw type implants. Clin Oral Implants
Res. 1991; 2: 186-92.
14. Ericsson L, Lindhe J. Probing depth at implants and teeth. An experimental
study in the dog. J Clin Periodontol. 1993; 9: 623-7.
15. Ferreira SD, Silva GL, Cortelli JR, Costa JE, Costa FO. Prevalence and
risk variables for peri-implant disease in Brazilian subjects. J Clin
Periodontol. 2006; 33: 929-35.
16. Casado PL, Otazu IB, Balduino A, Mello W, Barboza EP, Duarte MEL.
Identification of periodontal pathogens in healthy periimplant sites. Implant
Dent. 2011; 20: 226-35.
17. Lopez-Piriz R, Morales A, Gimnez MJ, Bowen A, Carroquino R, Aguilar
L et al. Correlation between clinical parameters characterising peri-implant
and periodontal health: A practice-based research in Spain in a series of
patients with implants installed 4-5 years ago. Med Oral Patol Oral Cir
Bucal. 2012; 17: e893-901.
18. Albrektsson T, Zarb G, Worthington P, Eriksson AR. The long term efficacy
of currently used dental implants: a review and proposed criteria of success.
Int J Oral Maxillofac Implants. 1986; 1: 11-25.
19. Levin L. Dealing with dental implant failures. J Appl Oral Sci. 2008; 16:
171-5.
20. Soskolne WA. Subgingival delivery of therapeutic agents in the treatment
of peridontal diseases. Critic Rev Oral Biol Med. 1997; 8: 164-74.
21. Luterbacher S, Mayfield I, Bragger U, Lang NP. Diagnostic characteristics
of clinical and microbiological tests for monitoring periodontal and peri-
implant mucosal tissue conditions. Clin Oral Implan Res. 2000; 11: 521-9.
22. Christensen MM, Joss A, Lang NP. Reproducibility of automated periodontal
probing around teeth and osseointegrated oral implants. Clin Oral Implant
Res. 1997; 8: 455-64.
23. Leito JA, De Lorenzo JL, Avila-Campos MJ, Sendyk WR. Analysis of
the presence of pathogens which predict the risk of disease at peri-implant
sites through polymerases chain reaction. Braz Oral Res. 2005; 19: 52-7.
Is bleeding on probing a differential diagnosis between periimplant health and disease?