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CLINICAL ARTICLE

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Claudio Gatti, Fulvio Gatti, Matteo Chiapasco, Marco Esposito

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Outcome of dental implants in partially edentulous


patients with and without a history of periodontitis:
a 5-year interim analysis of a cohort study
Claudio Gatti,
MD, DDS
Private practice,
Parabiago and Milan, Italy

Fulvio Gatti, DDS

Key words

bone level, dental implant, peri-implantitis, periodontitis, prognosis

Purpose: To evaluate the outcome of dental implants placed in partially edentulous patients with a
history of severe periodontitis (SP), moderate periodontitis (MP) and no periodontitis (NP).
Materials and methods: Sixty-two partially edentulous patients were consecutively enrolled in this
study. Patients were divided into three groups according to their initial periodontal conditions,
assessed with a modified Periodontal Screening and Recording (PSR) index: 26 patients were in the
SP group, 7 in the MP group, and 29 in the NP group. Patients requiring periodontal treatment were
treated prior to implantation. Various dental implants and procedures were used. In the SP group 129
implants were placed, 26 were placed in the MP group, and 72 in the NP group. Outcome measures
were prosthetic success, implant survival, prevalence of peri-implantitis and mean peri-implant bone
level changes on periapical radiographs.
Results: Six patients dropped out, two from each group, at 5 years. Two implants and their prosthesis failed with peri-implantitis in one patient and two implants were successfully treated for periimplantitis in another patient in the SP group. After 5 years, patients affected by SP and MP lost on
average twice the amount of peri-implant bone compared with healthy patients (2.6 mm versus
1.2 mm). This difference was highly statistically significant.
Conclusions: Patients with a history of SP and MP lose more peri-implant bone than periodontally
healthy patients and might be at higher risk for peri-implantitis and implant failures.

 Introduction
Results from a recent systematic review suggested
that patients with a previous history of periodontitis
are at higher risk for peri-implantitis and peri-implant
marginal bone loss 5 years after loading when com-

pared with patients who had their teeth replaced by


implants for other reasons1. These results were based
only on two studies with small sample sizes, both considered at high risk for bias2,3. Therefore, the results of
the systematic review should be interpreted with caution. It was recommended to conduct further long-

Eur J Oral Implantol 2008;1(1):4551

Trainee, Specialty of
Oral Surgery,
Unit of Oral Surgery,
Department of Medicine,
Surgery and Dentistry,
San Paolo Hospital,
University of Milan,
Milan, Italy

Matteo Chiapasco,
MD
Head Unit of Oral Surgery,
Department of Medicine,
Surgery and Dentistry,
San Paolo Hospital,
University of Milan,
Milan, Italy

Marco Esposito,
DDS, PhD
Senior Lecturer, Oral and
Maxillofacial Surgery,
School of Dentistry,
University of Manchester,
UK
and Associate Professor,
Department of Biomaterials,
Sahlgrenska Academy at
Gteborg University,
Sweden
Correspondence to:
Dr Marco Esposito,
School of Dentistry,
Oral and Maxillofacial
Surgery,
University of Manchester,
Higher Cambridge Street,
Manchester M15 6FH, UK
Email:
espositomarco@hotmail.com

Implants in patients with a history of periodontitis

The following outcome measures were considered:


Success of the prosthesis: a failed prosthesis or a
prosthesis that could not be placed due to
implant failure was considered a failure.

Eur J Oral Implantol 2008;1(1):4551

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This study was designed as a prospective cohort


study with three arms, including consecutively
treated partially edentulous patients. Follow-up was
5 years after implant loading for all included patients.
Treatments were carried out in two Italian private
dental practices between 1990 and 2002.
No ethical or institutional review board approval
was sought. All procedures were performed by one
experienced operator, except in one of the centres
where another surgeon performed some implant
placement.
To be included, patients had to be 18 years or
older. Exclusion criteria were:
edentulism in both jaws
irradiation in the head and neck region, or
chemotherapy
patients showing dubious cooperation
unrealistic aesthetic expectations
emotional instability and psychiatric problems
substance abusers
patients affected by HIV
autoimmune diseases
bone metabolic diseases
uncontrolled diabetes
serious coagulation problems
pregnant or lactating women.

 Materials and methods

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term studies before final conclusions can be drawn


about the prognosis of implant treatment in patients
with a history of periodontitis1.
The aim of the present cohort study was to investigate whether partially edentulous patients with a history of severe periodontitis (SP) are at higher risk for
implant failures and peri-implantitis when compared
with patients affected by moderate forms of periodontitis (MP) or healthy ones (no periodontitis, NP). This is
a preliminary 5-year report of a larger ongoing study.
Future reports will be aimed at describing larger sample
sizes with longer follow-up periods (10, 15 and 20
years).

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ubany reaImplant survival: implants removedPfor
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was not assessed with the removed
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Peri-implantitis: defined as loss of > 2 mm of periimplant marginal bone from the last radiographic
assessment, in the presence of pus or another
sign of infection and probing pocket depth
> 5 mm.
Marginal bone level changes on periapical intraoral radiographs made with the paralleling technique: radiographs were taken at implant loading and after 5 years of loading. Measurements
were made by a single non-blinded calibrated
assessor (CG, who treated and followed all
patients) using a magnifying ocular grid. Measurements of the mesial and distal bone crest
level adjacent to each implant were made to the
nearest 0.1 mm. Reference points for the linear
measurements were the coronal margin of the
implant collar and the most coronal point of
bone-to-implant contact.

 Description of the procedures


Periodontal therapy
At the first visit, the periodontal conditions were
assessed using a modification of the Periodontal
Screening and Recording (PSR) index4, and subsequently periodontal therapy (non-surgical and surgical) was administered as required (Table 1). The PSR
index is a modification of the Community Periodontal
Index of Treatment Needs (CPITN), commissioned by
the World Health Organization to evaluate periodontal treatment needs in epidemiological studies5. The
PSR index added to the original CPITN coding system
an additional symbol code (*) denoting additional
periodontal abnormities such as furcation involvement, tooth mobility, mucogingival defects and recessions. The following recording system was used on
sextants and has five categories (wisdom teeth were
excluded). Only the highest score was recorded for
each sextant:
0 = healthy patient.
1 = bleeding on probing.
2 = presence of calculus and/or defective restorations.
3 = probing pocket depths between 3.5 to 5.5 mm
and/or furcation involvement degree 1

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Implants in patients with a history of periodontitis

Moderate
periodontitis

Number of patients

26

Number of patients with PSR = 02 at implant placement

20

Number of patients with PSR = 3 at implant placement

Mean age (range) at implant placement

56 (3585)

56 (4270)

40 (1861)

Number of females (%)

16 (62%)

3 (43%)

20 (69%)

Received surgical periodontal therapy (%)

18 (69%)

2 (29%)

0 (0%)

Smokers (%)

5 (19%)

3 (43%)

6 (20%)

Number of prostheses (failed)

48 (1)

9 (0)

38 (0)

Number of implants (failed)

129 (2)

26 (0)

72 (0)

Patients treated with machined surfaces (%)

15 (58%)

2 (29%)

20 (69%)

Implants affected by peri-implantitis (failed)

4 (2)

Implants in maxillae

48

38

Implants in anterior jaws*

59

33

Implants in augmented bone

17

15

Drop-outs at 5 years

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Patients were divided into three groups according the


following characteristics: patients with PSR 02 were
considered healthy (NP group); patients with a PSR =
3 were considered as affected by MP; and patients
with PSR = 4 were considered as affected by SP (Table
1). The periodontal conditions of the patients at
implant placement (after periodontal therapy) are presented in Table 1.

Implant placement
Implants were inserted according the guidelines of
the various manufacturers. When required, various
bone augmentation procedures were implemented
(Table 1). Implants from different manufacturers
(Nobel Biocare [Gothenburg, Sweden], Zimmer
Dental [Carlsbad, CA, USA], Mathys [Bettlach,
Switzerland], Straumann [Basel, Switzerland] and
Dentsply Friadent [Mannheim, Germany]), and with
different shapes and surface characteristics (Table 1)
were used. After surgical procedures, patients were

instructed to use 0.2% chlorhexidine mouthwashes,


starting 1 hour prior to the intervention, twice a day
for 2 weeks.

Prosthetic and maintenance procedures


After an unloaded healing period ranging from 0 days
to 11 months (immediate loading procedures were
also implemented), abutments were connected and
various types of prostheses (overdentures, fixed-cross
arch prostheses, partial fixed bridges and single
crowns) were placed. Patients of the SP group were
recalled for oral hygiene maintenance every 3 months,
those in the MP group every 4 months, and those in
the NP group every 6 months.

 Statistical analyses
All data analysis was carried out according to a preestablished analysis plan. The patient was the statistical unit of the analyses. A biostatistician with expertise in dentistry analysed the data, without knowing the
group allocation. Independent sample chi-square tests

Eur J Oral Implantol 2008;1(1):4551

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* Second to second premolar.

4 = probing pocket depths > 5.5 mm and/or furcation involvement degree 2 or more

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Severe
periodontitis

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Pu 1 Patients main
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No periodontitis
characteristics.
cat
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Implants in patients with a history of periodontitis

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Fig 1a Periapical radiograph showing peri-implant marginal


bone levels just prior to implant loading of three two-piece
transmucosal implants in the maxilla of a patient belonging
to the severe periodontitis group.

Fig 1b After 5 years of loading, bone loss up to the third to


fourth thread can be observed around all implants, in the
absence of clinical symptoms.

were to be used to compare the relative numbers of


patients who had at least one prosthesis failure,
implant failure or presence/absence of peri-implantitis. However, there were insufficient data for these
analyses. The average radiographic values for the
mesial and distal surfaces were calculated and averaged for each patient. An analysis of variance was
used to compare mean bone level at 5 years and the
change in bone level for the three groups, followed by
Bonferroni test to make specific pairwise comparisons.
Age was considered as a covariate in an analysis of
covariance model. The Bonferroni test modified the
critical P-values for each comparison to achieve an
overall error rate of 0.05.

six patients had a PRS index = 02, and one patient


had a PSR index = 3 (Table 1). They received 26
implants supporting nine prostheses. Two patients
dropped out 5 years after loading because of economic problems, but confirmed that all implants were
fine; one patient was ill.
The NP group (Table 1) consisted of 29 patients,
with a mean age of 40 years. At the time of implant
placement all patients had a PRS index = 02 (Table
1). They received 72 implants supporting 38 prostheses. Two patients dropped out 5 years after loading:
one was not willing to attend the follow-up, but confirmed that all implants were fine. The other patient
was no longer reachable.
One prosthesis was lost in the SP group: the two
anterior mandibular implants (Ha-Ti with an acidetched sand-blasted surface, Mathys) supporting this
prosthesis failed because of peri-implantitis. Those
implants failed after 3 and 5 years respectively (Figs 3a
and 3b). No therapy was delivered to save these
implants because the bone loss was too advanced, and
the implants were removed. Two additional implants
(MKIII with the TiUnite surface, Nobel Biocare) in the
posterior mandible of another patient of the SP group
were affected by peri-implantitis. They were treated
with an apically repositioned flap, removal of the
exposed threads, polishing of the implant surface, disinfection with betadine, and systemic antibiotics (a
cocktail of amoxicillin and metronidazole for 10 days6).
The implants were still in function at the 5-year followup. Both patients had a PSR index = 3 at the time of

 Results
Sixty-two partially edentulous patients were consecutively treated. After 5 years, six patients dropped out.
The SP group (Table 1; Figs 1a and 1b) consisted of
26 patients, with a mean age of 56 years. At the time
of implant placement, after periodontal therapy, 20
patients had a PRS index = 02, and six patients had a
PSR index = 3 (Table 1). They received 129 implants
supporting 48 prostheses. Two patients dropped out 5
years after loading: one moved but confirmed that all
implants were fine, and the other died.
The MP group (Table 1; Figs 2a and 2b) consisted
of seven patients, with a mean age of 56 years. At the
time of implant placement, after periodontal therapy,

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Implants in patients with a history of periodontitis

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Fig 2a Periapical radiograph showing peri-implant marginal


bone levels immediately before implant loading of three
mandibular one-piece transmucosal implants in a patient belonging to the moderate periodontitis group.

Fig 2b After 5 years of loading, no appreciable bone loss


can be detected.

Fig 3a Periapical radiograph showing peri-implant marginal


bone levels immediately before implant loading of one of
four mandibular two-piece transmucosal implants in a patient belonging to the severe periodontitis group.

Fig 3b After 5 years of loading, more than 50% of the supporting bone was lost because of peri-implantitis. The implant was removed.

implant placement and did not smoke. No other failure or peri-implantitis occurred.
All radiographs could be evaluated at both the
mesial and distal site of each implant. Baseline, 5year results and changes in bone level are shown for
the three study groups in Table 2. There were statistically significant differences in bone levels at 5 years
and in change in bone level, with the healthy subjects
having less bone loss than the other two groups (P <
0.001) (95% CI for 5 year bone levels: SP versus NP

0.551.96, MP versus NP 0.212.65; 95% CI for


bone level changes: SP versus NP 0.602.04, MP
versus NP 0.222.73). There was a statistically significant difference in the mean age of the subjects, with
the healthy subjects being younger than those in the
other two groups (P < 0.001). If age is treated as a
co-variable in an analysis of covariance, when comparing the change in bone levels, the differences
between groups are still significant, and age is not
significant (P = 0.62)

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Implants in patients with a history of periodontitis

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Healthy
l
(n = 27) ica
tio
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te (0.23)
0.13
ss e n c e

Severe periodontitis
(n = 24)

Moderate periodontitis
(n = 5)

Baseline

0.06 (0.17)

0.08 (0.18)

5 years

2.63 (1.06)

2.80 (0.45)

1.37 (1.04)

Change (5 years baseline)

2.57 (1.06)

2.72 (0.44)

1.24 (1.09)

Eur J Oral Implantol 2008;1(1):4551

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The present investigation was designed to evaluate


whether patients with a previous history of periodontitis are at higher risk of developing similar problems
around dental implants. The results clearly indicate
that patients with a previous history of SP or MP lost
about twice the amount of peri-implant bone (2.6 and
2.7 mm respectively) when compared with non-periodontitis-susceptible patients (1.2 mm) over a 5-year
period. All failures (one prosthesis and two implants in
the same patient) and peri-implantitis (four implants
in two patients, two of which ended in the failure of
the two affected implants [Figs 3a and 3b] and their
prosthesis) occurred in patients with a history of severe
periodontitis. In particular, both patients had a PSR
index = 3 at implant placement, after periodontal therapy, meaning that their periodontal conditions were
improved, but not completely healed. These results are
in agreement with similar studies published on this
topic2,3. However, results still have to be interpreted
with some caution because of the limitations of the
present study. Groups were not completely comparable at baseline. The potentially most relevant differences were in terms of age and number of implants/
prosthesis. Patients in the healthy group were on average 16 years younger than patients with a previous history of periodontitis, and received approximately half
as many implants. The ideal study should be conducted after matching patients of the various groups
for some factors (for instance age and number of
implants and prostheses) believed to be of importance.
There were too few patients in the present study to
allow appropriate matching. In addition, the differences in age and number of implants could have plausible explanations, such as different patterns of tooth
loss among groups. Patients with a previous history of
periodontitis are likely to have lost more teeth because
of periodontal disease, and therefore required more
implants, whereas the healthy group included several
patients who had lost teeth through trauma or were

 Discussion

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Table 2 Mean (SD)


bone levels at baseline,
5 years and the change
for the three study
groups.

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affected by tooth agenesia, and therefore they were


likely to be younger and require less implants. In addition, statistical calculations suggested that age did not
significantly affect results of bone level calculations.
Another limitation of this study was that implants
were not tested for stability at the 5-year interval since
many of prostheses could not be removed because they
were permanently cemented. This might have led to an
underestimation of actual failures, as was found in a previous study7. Finally, the outcome assessor was the same
clinician who placed the implants and therefore this
study was not blinded. On the other hand, it should be
recognised that the periodontal condition of the
patients was determined at entry and not retrospectively and that the number of drop-outs was relatively
small, with efforts made to determine their reasons.
In two groups not a single failure occurred, and
both implant losses were concentrated in one patient
in the SP group. Despite this, the 5-year results for the
periodontitis group are more than acceptable, with
only one patient out of 25 experiencing failure of the
implant treatment.
The present report represents an interim analysis of
a larger ongoing study. It is planned to follow the
included patients for up to 20 years, and new patients
are still being enrolled in the study. All patients subjected to implant treatment were consecutively
included. The completion of this interim report
required 12 years, and over such a long period many
changes in terms of implant design and techniques
occurred. Further material and technical changes are
expected. No statistical analyses were performed to
evaluate whether there were differences for prosthesis and implant failure rates, and for occurrence of periimplantitis between groups because there were too
few events for a statistically significant difference to be
found. In addition, when a significance level of 0.05 is
used in an interim analysis, in the subsequent analysis,
the significance level has to be halved to 0.025, which
makes small statistically significant differences even
harder to detect.

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University of Manchester, for her help with the statistical calculations.

 References
1. Schou S, Holmstrup P, Worthington HV, Esposito M.
Outcome of implant therapy in patients with previous tooth
loss due to periodontitis. Clin Oral Implants Res 2006;
17(Suppl 2):104-123.
2. Hardt CR, Grndahl K, Lekholm U, Wennstrm JL. Outcome
of implant therapy in relation to experienced loss of periodontal bone support. Clin Oral Implants Res 2002;13:
488-494.
3. Karoussis IK, Salvi GE, Heitz-Mayfield LJA, Brgger U,
Hmmerle CHF, Lang NP. Long-term implant prognosis in
patients with and without a history of chronic periodontitis:
a 10-year prospective cohort study of the ITI Dental Implant
System. Clin Oral Implants Res 2003;14:329-339.
4. American Dental Association and American Academy of
Periodontology. Periodontal screening and recording training program kit. Chicago: American Dental Association and
American Academy of Periodontology, 1992.
5. Ainamo J, Barmes D, Beagrie G, Cutress T, Martin J, SardoInfirri J. Development of the World Health Organization
(WHO) community periodontal index of treatment needs
(CPITN). Int Dent J 1982;32:281-291.
6. van Winkelhoff AJ, Rodenburg JP, Goen RJ, Abbas F,
Winkel EG, de Graaff J. Metronidazole plus amoxycillin in
the treatment of Actinobacillus actinomycetemcomitans
associated periodontitis. J Clin Periodontol 1989;16:
128-131.
7. Grndahl K, Lekholm U. The predictive value of radiographic diagnosis of implant instability. Int J Oral Maxillofac
Implants 1997;12:59-64.

Eur J Oral Implantol 2008;1(1):4551

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Patients with a history of severe and moderate periodontitis 5 years after implant placement lost on average over twice the amount of peri-implant marginal
bone (approx. 2.6 mm) compared with patients with
no history of periodontal disease (bone loss approx.
1.2 mm). There was also a tendency toward more
peri-implantitis and implant failures in subjects with a
history of severe periodontal disease. Patients with a
history of periodontitis might be at higher risk for periimplantitis and implant failures and should be enrolled
in more stringent maintenance protocols.

 Conclusions

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 Acknowledgements
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The authors wish to thank Prof Helen Worthington,tes
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The main clinical implication of the present study is


that patients with a previous history of periodontitis are
at higher risk for marginal bone loss, and potentially for
peri-implantitis, in the long term. Therefore, those
patients ought to be properly informed about their
increased risk for problems and should be enrolled in a
stricter maintenance regimen than healthy patients. It
is possible that the number of failures in patients with
a history of periodontitis can increase over time, as suggested by the increased peri-implant marginal bone
loss. To address this hypothesis, cohort studies of a minimum duration of 10 years or more including a sufficient number of patients are needed.

Implants in patients with a history of periodontitis

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