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Is bleeding on probing a differential diagnosis between periimplant health and disease?

Authors:
  • Fluminense Federal University, Niterói, RJ, Brazil

Abstract and Figures

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 51.7±12.4 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.
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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 Casado1, Ricardo Villas-Bôas2, Luana Cristine Leão da Silva3,
Cristiana Farias de Carvalho Andrade3, Letícia Ladeira Bonato4, José Mauro Granjeiro5
1Area of Morphology, Cell Therapy Center - Clinical Research Unit and Biology Institute, Fluminense Federal University – Niterói, RJ, Brazil and
Orthopedics and Traumatology National Institute, Rio de Janeiro, RJ, Brazil
2Area of Dentistry, Veiga de Almeida University, Rio de Janeiro, RJ, Brazil
3Dentist, Veiga de Almeida University, Rio de Janeiro, RJ, Brazil
4Dentist, Juiz de Fora Federal University, Juiz de Fora, MG, Brazil
5Area of Chemistry, Cell Therapy Center - Clinical Research Unit and Biology Institute - Fluminense Federal University - Niterói, RJ, Brazil and
National Institute of Metrology - Rio de Janeiro, RJ, Brazil
Correspondence to:
Priscila Ladeira Casado
Núcleo de Terapia Celular
Unidade de Pesquisa Clinica
Rua Marques de Paraná 303, 40° andar,
CEP: 24033-900 - Centro, Niterói, RJ, Brasil
Phone / Fax: +55 21 26299255
E-mail: pcasado@into.saude.gov.br
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 51.7±12.4 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 prognosis1.
In natural dentition, the junctional epithelium provides sealing on the base
Received for publication: February 21, 2013
Accepted: June 11, 2013
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Braz J Oral Sci. 12(2):95-99
of the periodontal sulcus against the penetration of chemical
pathogens and bacterial substances2. 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 implant1-3.
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
success2,4-5. However, correct and early clinical diagnosis of
periimplant disease status is frequently critical, which makes
maintenance of the periimplant tissue difficult6. According
to the Seventh European Workshop on Periodontology, the
clinical parameters that indicate periimplant disease are
bleeding on probing (BOP) and increased probing depth7.
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 sites6,8. 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 faces9. 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 pocket10.
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 epithelium11-12. 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 Lindhe14 (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 teeth16-17.
The correct diagnosis of periimplant disease is a critical
procedure, which makes it difficult the periimplant tissue
maintenance6. Actually, a clinical standard to diagnose
periimplant disease is based on the presence of BOP with
probing pocket depth e”4 mm for mucositis diagnosis and
additional radiographic bone loss for correct periimplantitis
diagnosis8. During the first year after abutment connection,
1 mm of marginal bone loss is allowed, followed by 0.2 mm
loss per year18. Currently, these criteria are still frequently
referred to as the “gold standard” for implant success19.
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 Board’s
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
51.7±12.4 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 Soskolne20 (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 (Student’s
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
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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
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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 Periodontology7
(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 tissues14 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 teeth16-17. 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
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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 interface10. Therefore, according to Heitz-Mayfield6
(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 stage10.
In addition, according to Leitão 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).
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Is bleeding on probing a differential diagnosis between periimplant health and disease?
... Recentemente, Casado et al. 144 desenvolveram um estudo clínico, com 144 pacientes e 486 implantes, onde pretenderam avaliar se a HS estava diretamente relacionada com a presença de doenças peri-implantares. Verificaram a presença de HS em 20,1% dos locais examinados em pacientes saudáveis, em 100% dos locais de pacientes com mucosite e em 19,9% dos locais examinados em pacientes com peri-implantite. ...
... Este estudo demonstrou que, após o dignóstico inicial de doenças peri-implantares, considerando outros parâmetros clínicos bem como radiográficos, a HS tornou-se secundária para a identificação da doença tendo em conta que uma mucosa saudável apresenta HS em 20% dos casos. Concluíram, assim que, per se, a HS não é um parâmetro fiável para diagnóstico de lesão peri-implantar 144 . ...
... Porém nem todos os autores estão de acordo com este papel secundário do exame radiográfico. Recentemente, Casado et al. 144 , num estudo clínico, detectaram que 56% dos locais afectados por perda óssea (peri-implantite) apresentavam uma mucosa saudável, o que em muitos casos não levaria o clínico a realizar exame radiográfico e assim não diagnosticando a peri-implantite 144 . ...
Thesis
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In order to study peri-implantitis some experimental models were developed, mainly using the dog as animal model. At the beginning of this study, a bibliographic review was performed regarding the experimental dog model for peri-implantitis studies. Fifty-six studies were included for analysis. All used ligatures in order to establish a peri-implant lesion, with great methodological heterogeneity. Considering that the present experimental model fails to recreate the anatomic, physiologic or pathological environment of the clinical conditions found in human peri-implantitis, there is a need to research new experimental models. The main objective of this study is to evaluate whether the absence of plaque control alters the clinical, radiological, microbiological and histological peri-implant tissue parameters. Six 2 ½ year-old male Beagle dogs had their bilateral mandible premolars and first molar extracted (week -24). Eight weeks later plaque control measures were suspended (week -16) until implant placement (week 0). Two SLA® surface implants (Standard Plus® Ø3,3x8mm, narrow neck, Institut Straumann® AG, Basel, Switzerland) were placed at each hemimandible and were randomly assigned to one of each group: a group with plaque control (control implants – CI); a group without plaque control (test implants – TI). On the day of implant placement a radiographic evaluation was performed. Implants were then evaluated clinically, radiographically and microbiologically at weeks 3, 6, 9, 12, 15 and 17, and histologically after euthanasia. Presence of plaque (PP), mucositis (Muc), probing depth (PD), bleeding on probing (BOP), gingival marginal level (GML), clinical attachment level (CAL) and suppuration were clinically evaluated. The distance between implant shoulder (IS) and first bone to implant contact (fBIC) was evaluated radiographically. Microbiological samples were collected during the 17 week experimental procedure. Using real-time polymerase chain reaction, the DNA of total bacteria (TB) load, Streptococcus species, Fusobacterium species, Porphyromonas gingivalis (Pg), Aggregatibacter actinomycetemcomitans (Aa) and Prevotella intermedia (Pi) was quantified. After euthanasia, implant and peri-implant tissues were histologically analyzed using a undecalcified technique, and histomorphometry performed to measure the following distances: gingival margin-apical junctional epithelium (GM-aJE); gingival margin-apical sulcular epithelium (GM-aSE); bone crest-apical sulcular epithelium (BC-aSE); bone crest-apical junctional epithelium (BC-aJE); gingival margin-bone crest (GM-BC); implant shoulder- bone crest (IS-BC); gingival margin-apical inflammatory infiltrate (GM-aINF) and inflammatory infiltrate percentage (%INF). A possible correlation between PD and GM-aJE or GM-aSE, and also between IS-fBIC and IS-BC, was analyzed. Regarding the results of the clinical parameters at the end of the protocol PP, Muc, PD, BOP and CAL had statistically significant differences between groups, with higher values of TI. The radiographic parameter evaluated, at the end of the procedure, revealed no statistically significant difference between groups. At the end of the experimental protocol microbiological analysis identified intergroup differences for TB, Fusobacterium spp., Pg and Aa, with TI having the highest value. Histomorphometry showed a single statistically significant difference between both groups, with TI having the higher values of %INF. Finally, a positive correlation was found between PD and the GM-aJE for TI. On the other hand, the radiographic distance IS-fBIC and histologic IS-HI correlate positively to both groups. The absence of measures to control plaque was the variable tested in this experimental study, and resulted in statistically significant differences between both groups in clinical, microbiological and histological parameters. However, despite all these changes, the lesions seen in this model did not overlap features due to the characteristics present in the human peri-implantitis. Key-words: experimental model, dog, peri-implantitis.
Article
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To explore peri-implant health (and relation with periodontal status) 4-5 years after implant insertion. A practice-based dental research network multicentre study was performed in 11 Spanish centres. The first patient/month with implant insertion in 2004 was considered. Per patient four teeth (one per quadrant) showing the highest bone loss in the 2004 panoramic X-ray were selected for periodontal status assessment. Bone losses in implants were calculated as the differences between 2004 and 2009 bone levels in radiographs. A total of 117 patients were included. Of the 408 teeth considered, 73 (17.9%) were lost in 2009 (losing risk: >50% for bone losses ≥7 mm). A total of 295 implants were reviewed. Eight of 117 (6.8%) patients had lost implants (13 of 295 implants installed; 4.4%). Implant loss rate (quadrant status) was 1.4% (edentulous), 3.6% (preserved teeth), and 11.1% (lost teeth) (p=0.037). The percentage of implant loss significantly (p<0.001) increased when the medial/distal bone loss was ≥3 mm. The highest (p≤0.001) pocket depths were found in teeth with ≥5 mm and implants with ≥3 mm bone losses, with similar mean values (≥4 mm), associated with higher rates of plaque index and bleeding by probing. The significant bi-directional relation between plaque and bone loss, and between each of these two parameters/signs and pocket depths or bleeding (both in teeth and implants, and between them) together with the higher percentage of implants lost when the bone loss of the associated teeth was ≥3 mm suggest that the patient's periodontal status is a critical issue in predicting implant health/lesion.
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An implant-supported restoration offers a predictable treatment for tooth replacement. Reported success rates for dental implants are high. Nevertheless, failures that mandate immediate implant removal do occur. The consequences of implant removal jeopardize the clinician's efforts to accomplish satisfactory function and esthetics. For the patient, this usually involves further cost and additional procedures. The aim of this paper is to describe different methods and treatment modalities to deal with dental implant failure. The main topics for discussion include identifying the failing implant, implants replacing failed implants at the exact site, and the use of other restorative options. When an implant fails, a tailor made treatment plan should be provided to each patient according to all relevant variables. Patients should be informed regarding all possible treatment modalities following implant failure and give their consent to the most appropriate treatment option for them.
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Osseointegrated dental implants have been considered the most es-thetical and functional alternative to missing teeth. However, the treat-ment is not always successful resulting in the implant loss. The im-plant failure can be classified as early failure (the osseointegration is not established) and late failure (involving a breakdown of the estab-lished osseointegration). The implant loss can be attributed to factors such as biological, microbiological and biomechanical, but the cause and mechanism of the early implant failure are still obscure. The cluster phenomenon, multiple implant failures in the same subject, supports the evidence that individual characteristics play an impor-tant role in the early failure process. However, little is known about the influence of genetic susceptibility on osseointegration. The aim of this article was to present an evaluation of the literature regarding mechanism, epidemiology, histopathologic observations, role of in-flammatory mediators and factors associated with early implant fail-ures.
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Osseointegrated dental implants are used routinely in dentistry in the confidence of predictable success. However, if the implant surfaces become colonised by pathogenic bacteria, the plaque-induced inflammation around the implants may cause peri-implant tissue destruction. Peri-implant mucositis is a reversible, plaque-induced inflammatory lesion confined to the peri-implant soft tissue unit and clinically is characterised by redness, swelling and bleeding on gentle probing. Peri-implantitis is an extension of peri-implant mucositis to involve the bone supporting the implant: it is characterised by loss of osseointegration of the coronal part of the implant, by increased probing depth and by bleeding and/or suppuration on probing. Established peri-implantitis does not respond predictably to treatment. The best management of plaque-induced peri-implant inflammatory diseases is prevention. Regular personal and professional cleaning of the implant is mandatory to minimise bacterial load. Despite our best efforts, plaque-induced peri-implant inflammatory diseases will occur frequently, and as these diseases respond best to early treatment, early detection of peri-implant mucositis by regular assessment will permit timely treatment. Peri-implant mucositis is readily treated non-surgically. Peri-implantitis is more difficult to treat largely because of the problem of decontamination of the roughened, threaded surfaces of exposed implants. As a rule, surgical treatment will be necessary, and even then success is not assured.
Article
The aim of this study was to evaluate a clinical and a microbiological test for monitoring tissue condition during supportive periodontal therapy (SPT) and to compare their diagnostic characteristics at implant and tooth sites. Twelve female (age: 37–72 years) and 7 male patients (age: 26–83 years) were evaluated in this study on the basis of availability to follow a rigid SPT program. Patients had received a complete periodontal examination at 1 and 5 years after implant placement. This included standardized radiographs obtained at implants and matching control teeth. One implant site and one tooth site per patient were followed during the last 2 years of the SPT program. At each recall visit microbiological samples were analyzed according to DNA/RNA analysis identifying periodontal pathogens (IAI Pado Test 4.5®, Institute for Applied Immunology, Zuchwil, Switzerland). Presence or absence of bleeding on probing at these sites was also noted using a standardized probing force of 0.25 N (Audio Probe®, ESRO, Thalwil ZH, Switzerland). The percentage number of recall visits with positive bacteriological test results and positive BOP scores were calculated. Disease progression at the sites was defined if the annual increase in probing depth was ≥0.5 mm/year (2.5 mm in 5 years) or if the annual decrease in CADIA values (Computer Assisted Densitometric Image Analysis) was more than −0.7 per year (−3.5 in 5 years). Changes below these values were considered as negative test results indicating stability of the sites. The diagnostic characteristics (sensitivity, specificity, positive and negative predictive values) of BOP and microbiological tests alone or in combination were then calculated using two-by-two tables. By application of increasing thresholds of BOP frequencies set for definition of positive test outcome (BOP ≥10% ≥20% ≥25% ≥50% ≥75% ≥90% or the combined BOP ≥75%, but DNA positive ≥10%, ≥25% ≥34% ≥50% ≥67% ≥90%) receiver operator characteristics curves (ROC) were constructed for teeth and implants. The areas under the ROC curves were calculated and compared by means of chi-square tests. The results indicated statistically significant better diagnostic characteristics of both tests at implants compared to teeth. The inclusion of an additional microbiological test significantly enhanced the diagnostic characteristics of BOP alone at teeth as well as at implants.
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Three different probing devices (Audio-Probe, Florida-Probe, Peri-Probe) were tested in order to determine the clinical probing depth (CPD) around clinically stable oral implants and their homologous teeth and to evaluate their reproducibility. In all 37 patients, in the age range of 24-80 years, who had undergone periodontal therapy and placement of 1 or more oral implants (ITI), were selected for the study. The CPD was determined on 75 oral implants in total and at 4 sites of both the implants and the control teeth at 3 visits, each 1 week apart. At the 1st visit, the Florida-Probe and the Audio-Probe were used. At the 2nd visit, the Florida-Probe and the Peri-Probe and, at the 3rd visit, again, the Florida-Probe and the Audio-Probe were used. At each visit bleeding on probing (BOP) was registered. A statistically significant (P < 0.05) difference between the mean scores of implant and tooth sites was found showing slightly higher values for implant sites. A tendency for the deeper pockets to bleed more frequently than the shallow pockets was observed. The comparisons of differences of the readings of the Audio-Probe on 2 different occasions were smaller than for the Florida-Probe. However, comparisons between 2 different probes showed significantly greater measurement errors than when comparing the probes alone. There was a tendency for the Peri-Probe to yield the highest and the Audio-Probe the lowest values in inflamed sites. It was concluded that all 3 probing devices appeared to have adequate reproducibility both around teeth and oral implants. For clinical use in daily practice, the Audio-Probe was found to be the most simple device with the highest reproducibility.
Article
The purpose of this study was to compare the tissue resistance to probing and the accuracy of depth determination at different force levels around implants and teeth. In 11 subjects 1 implant and 1 tooth at a comparable location and with comparable probing depth were investigated. The sites were located on either the mesial or distal aspect of the tooth and the implant. A probing device was used which allowed simultaneous monitoring of probing force and probe penetration and which standardized the insertion pathway for repeated measurements. The probing instrument was fitted with an attachment for an aiming device to take a radiograph with the probe tip in the sulcus, using a standardized projection geometry. Probing depth values were determined at 0.25, 0.50, 0.75, 1.00 and 1.25 N probing force. The standard error of the individual measurement (Si), evaluated by comparison of repeated measurements in the same session, was 0.2 mm on implants and 0.1 mm on teeth. For implants there was a trend for slightly better reproducibility at higher force levels. Curve analysis of depth force patterns showed that a change in probing force had more impact on the depth reading in the peri-implant than in the periodontal situation. The mean distance between the probe tip and the peri-implant bone crest amounted to 0.75 +/- 0.60 mm at 0.25 N probing force. It is concluded that peri-implant probing depth measurements are more sensitive to force variation than periodontal pocket probing.
Article
: The aim of this study was to evaluate the presence of periodontopathogens in subgingival periimplant sites in partially edentulous patients using polymerase chain reaction procedures, with regard to areas with clinical and radiographic signs of health and areas presenting periimplant disease. : Thirty nonsmoking, partially edentulous patients, aged 30 to 76 years, were included in this study and divided in 3 groups according their clinical and radiographic characteristics. Group A (n = 10) presented periimplant health, group B (n = 10) presented periimplant mucositis, and group C (n = 10) were patients with periimplantitis. Periimplant tissues were clinically examined as regards the color of mucosae, presence of bacterial plaque, depth and bleeding on probing, and local suppuration. History of periodontal disease was also considered. Radiographic analysis evaluated the presence of bone loss around the implant. Samples of periimplant crevicular fluid were collected to analyze the presence of periodontal pathogens, Actinobacillus actinomycetemcomitans (Aa), Porphyromonas gingivalis (Pg), Prevotella intermedia (Pi), Tannerella forsythensis (Tf), and Treponema denticola (Td). : The results showed that the history of periodontal disease is associated with periimplant disease. The bacteria Aa, Pg, Pi, Td, and Tf were present in periimplant sites clinically and radiographically characterized, as healthy periimplant tissues, mucositis, and periimplantitis. : We concluded that Aa, Pg, Pi, Td, and Tf are present in healthy and diseased conditions. Therefore, these periodontal pathogens are not strictly related to periimplant disease sites.
Article
Peri-implant diseases present in two forms - peri-implant mucositis and peri-implantitis. The literature was systematically searched and critically reviewed. Four manuscripts were produced in specific topics identified as key areas to understand the microbial aetiology and the pathogenesis of peri-implant diseases and how the implant surface structure may affect pathogenesis. While peri-implant mucositis represents the host response of the peri-implant tissues to the bacterial challenge that is not fundamentally different from gingivitis representing the host response to the bacterial challenge in the gingiva, peri-implantitis may differ from periodontitis both in the extent and the composition of cells in the lesion as well as the progression rate. A self-limiting process with a "protective" connective tissue capsule developing appears to dominate the periodontitis lesion while such a process may occasionally be lacking in peri-implantitis lesions. Bacterial biofilm formation on implant surfaces does not differ from that on tooth surfaces, but may be influenced by surface roughness. Nevertheless there is no evidence that such differences may influence the development of peri-implantitis. It was agreed that clinical and radiographic data should routinely be obtained after prosthesis installation on implants in order to establish a baseline for the diagnosis of peri-implantitis during maintenance of implant patients.