Sren Schou Outcome of implant therapy in patients

Palle Holmstrup
Helen V. Worthington
with previous tooth loss due to
Marco Esposito periodontitis

Authors’ affiliations: Key words: complications, dental implants, oral implants, osseointegration, pathology,
Sren Schou, Department of Oral and Maxillofacial peri-implantitis, periodontal diseases, systematic review
Surgery, Aalborg Hospital, Aarhus University
Hospital, Aalborg, Denmark
Palle Holmstrup, Department of Periodontology, Abstract
School of Dentistry, University of Copenhagen,
Copenhagen, Denmark Background: It is frequently debated whether implant treatment in individuals with
Helen V. Worthington, Marco Esposito, School of previous tooth loss due to periodontitis is characterized by an increased incidence of
Dentistry, University of Manchester, Manchester,
implant loss and peri-implantitis.
UK
Objective: The objective of the present systematic review was to assess whether individuals
Correspondence to: with previous tooth loss due to periodontitis have an increased risk of loss of
Sren Schou
Department of Oral and Maxillofacial Surgery suprastructures, loss of implants, peri-implantitis, and peri-implant marginal bone loss as
Aalborg Hospital compared with individuals with previous tooth loss due to reasons other than periodontitis.
Aarhus University Hospital
Search strategy: Studies considered for inclusion were searched in MEDLINE (PubMed) and
18-22 Hobrovej
DK-9000 Aalborg relevant journals were hand searched. Moreover, reference lists of articles selected for full-
Denmark text screening as well as previously published reviews relevant for the present systematic
Tel.: þ 45 99 32 35 51
Fax: þ 45 99 32 28 04 review were searched. The search was performed by one reviewer and was restricted to
e-mail: ss@aas.nja.dk human studies published from January 1, 1980 to January 1, 2006. No language restrictions
were applied.
Selection criteria: Prospective and retrospective cohort studies with at least a 5-year follow-
up comparing the outcome of implant treatment in individuals with periodontitis-
associated and non-periodontitis-associated tooth loss, respectively, were included. The
outcome measures were survival of suprastructures, survival of implants, occurrence of peri-
implantitis, and peri-implant marginal bone loss. The 5- and 10-year time points were
evaluated.
Data collection and analysis: Screening of eligible studies, methodological quality
assessment, and data extraction were conducted in duplicate and independently by two of
the authors. The authors were contacted for missing information. Results were expressed as
random effect models using weighted mean differences for continuous outcomes and
relative risk for dichotomous outcomes with 95% confidence intervals (CIs).
Main results: Two studies with a 5- and 10-year follow-up, respectively, were identified
including a total of 33 patients with tooth loss due to periodontitis and 70 patients with
non-periodontitis-associated tooth loss. There was no significant difference in the survival
of the suprastructures after 5 years. Furthermore, there were no significant differences in
the survival of the implants after 5 and 10 years. However, there were significantly more
patients affected by peri-implantitis in the group with periodontitis-associated tooth loss
during the 10-year follow-up period, risk ratio (RR) 9 (95% CI 3.94–20.57). Moreover,
significantly increased peri-implant marginal bone loss was observed in patients with
periodontitis-associated tooth loss after 5 years, mean difference 0.5 mm (95% CI 0.06–
0.94).
Conclusions: The survival of the suprastructures and the implants was not significantly
different in individuals with periodontitis-associated and non-periodontitis-associated
tooth loss. However, significantly increased incidence of peri-implantitis and significantly
To cite this article: increased peri-implant marginal bone loss were revealed in individuals with periodontitis-
Schou S, Holmstrup P, Worthington HV, Esposito M.
Outcome of implant therapy in patients with previous associated tooth loss. The small sample size and the methodological quality assessment of
tooth loss due to periodontitis. the two studies suggest that the results should be interpreted with caution. Consequently,
Clin. Oral Imp. Res. 17 (Suppl. 2), 2006; 104–123
further long-term studies focusing particularly on the outcome of implant treatment in
r 2006 The Authors
young adults with aggressive periodontitis are needed before final conclusions can be
Journal compilation r Blackwell Munksgaard 2006 drawn about the outcome of implant treatment in patients with a history of periodontitis.

104

The first long-term study on implant treat-
ment involving fixed complete dentures
was published in 1981 (Adell et al. 1981).
During the following decades, implant
treatment has been assessed in numerous
reports involving both totally and partially
edentulous patients (Esposito et al. 1998;
Berglundh et al. 2002). A systematic review
on clinical studies with at least a 5-year
follow-up showed that 5% of the implants
with fixed dentures were lost before loading
or during function (Berglundh et al. 2002).
It was concluded that biological and me-
chanical complications occurred, but im-
plant treatment in general was to be
considered a treatment modality with pre-
dictable outcome and high survival rates.
In most long-term studies, the causality
behind tooth loss before implant placement
has not been specified, and presumably
some of the included patients have lost
some or all teeth due to periodontitis.
The susceptibility to periodontitis-asso-
ciated attachment and tooth loss shows
major individual variation, and accordingly
periodontitis has been classified into ag-
gressive and chronic subtypes (Armitage
1999). It is frequently debated whether
implant therapy in individuals with pre-
Medline (PubMed) search (1980-2005, human trials):
(exp Periodontal diseases) AND
(exp Dental implants OR exp Dental implantation OR “Oral implants”)
Abstracts reviewed:
Articles reviewed:
Articles included:
Fig. 1. Search strategy for identification of studies.
viously periodontitis-associated tooth loss
is associated with an increased incidence of
implant loss and peri-implantitis.
Objective
The objective of the present systematic
review was to assess whether individuals
with previous tooth loss due to perio-
dontitis have an increased risk of loss of
suprastructures, loss of implants, peri-im-
plantitis, and peri-implant marginal bone
loss as compared with individuals with
previous tooth loss due to reasons other
than periodontitis.
Criteria for considering studies
for this review
Types of studies, participants, and
intervention
Prospective and retrospective cohort stu-
dies with at least a 5-year follow-up com-
paring the outcome of implant treatment in
partially edentulous individuals with,
respectively, periodontitis-associated and
non-periodontitis-associated tooth loss
were assessed. More than 10 patients
Number Hand-searched journals (1980-2005):
2116
547
49
2
105 |
Schou et al . Periodontitis and implants
should be included in the study, and the
treatment should involve osseointegrated
oral implants.
Types of outcome measures
The outcome measures included the
following:

Loss of suprastructures.

Loss of implants defined as implant
mobility of previously clinically os-
seointegrated implants and removal of
non-mobile implants due to progressive
peri-implant marginal bone loss and
infection.

Occurrence of peri-implantitis defined
as progressive peri-implant marginal
bone loss associated with infection
signs.

Radiographic peri-implant marginal
bone loss on intraoral radiographs taken
with a paralleling technique.
Search strategy for
identification of studies
The search strategy used for identification
of studies is summarized in Fig. 1. Studies
Br J Oral Maxillofac Surg (1984-2005)
Br J Oral Surg (1980-1983)
Clin Implant Dent Relat Res (1999-2005)
Clin Oral Implants Res (1990-2005)
Implant Dent (1992-2005)
Int J Oral Maxillofac Implants (1986-2005)
Int J Oral Maxillofac Surg (1986-2005)
Int J Oral Surg (1980-1985)
Int J Periodontics Restorative Dent (1985-2005)
Int J Prosthodont (1988-2005)
J Clin Periodontol
J Craniomaxillofac Surg (1987-2005)
J Maxillofac Surg (1980-1986)
J Periodontal Res
J Periodontol
J Oral Implantol
J Oral Surg (1980-1981)
J Oral Maxillofac Surg (1982-2005)
J Prosthet Dent
J Prosthodont (1992-2005)
(0)
Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 104–123
Schou et al . Periodontitis and implants
considered for inclusion were searched in
MEDLINE (PubMed) with a broad search
strategy involving controlled vocabulary
(MeSH) and free text terms:
#1 exp Periodontal diseases
#2 exp Dental implantation
#3 exp Dental implants
#4 ‘Oral implants’
#5 2 OR 3 OR 4
#6 1 AND 5.
In addition, relevant journals were hand
searched page by page for relevant studies
(Fig. 1). Manual search also included the
bibliographies of all articles selected for
full-text screening as well as previously
published reviews relevant for the present
systematic review. Finally, the ‘related
article’ feature of PubMed was used for
all articles selected for full-text screening.
The search was performed by one reviewer
(S. S.) and was restricted to human studies
published from January 1, 1980 to January
1, 2006. No language restrictions were
applied.
Methods of the review
The titles of the identified reports were
initially screened (Fig. 1). The abstract was
assessed when the title indicated that the
study fulfilled the inclusion criteria. Full-
text analysis was carried out when an ab-
stract was unavailable or when the abstract
indicated that the above-described inclusion
criteria were fulfilled. The study selection
was performed by one reviewer (S. S.).
Quality assessment
The quality assessment of the included
studies was undertaken independently
and in duplicate by two authors (S. S., M.
E.) as part of the data-extraction process.
When disagreement between the two re-
viewers was revealed, consensus was
achieved by discussion. Additional infor-
mation provided by the authors of the
studies was taken into account, as de-
scribed in the following paragraph on data
extraction. The quality assessment was
performed according to the following para-
meters:

Description of tooth loss, attachment
loss, and health status of periodontal
tissues at the time of implant place-
ment for each treatment group (yes, no).
106 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 104–123

Blinding of outcome assessment (yes,
no).

Completeness of follow-up. A clear
explanation for withdrawals and drop-
outs in each treatment group (yes, no).
The studies were grouped according to:

Low risk of bias (plausible bias unlikely
to alter the results seriously) if all
quality criteria were met.

High risk of bias (plausible bias that
seriously weakens confidence in the
results) if one or more quality criteria
were not met.
Data extraction
Data were extracted independently by two
reviewers (S. S., M. E.) according to a
specially designed data-collection form,
which ensured systematic recording of
data. When disagreement between the
two reviewers was revealed, consensus
was achieved by discussion. Characteris-
tics of patients, their treatment, follow-up
period, and treatment outcome, i.e., survi-
val of suprastructures, survival of implants,
occurrence of peri-implantitis, and peri-
implant marginal bone loss were obtained.
Finally, recording of study quality assess-
ment was included. The authors were con-
tacted for clarification or missing
information.
Data synthesis
For binary outcomes (loss of suprastruc-
tures, loss of implants, occurrence of peri-
implantitis), the estimate of effect of inter-
vention was expressed as risk ratios (RR),
together with 95% confidence intervals
(CIs). For continuous outcomes (peri-im-
plant marginal bone loss), weighted mean
differences (MD) and standard deviations
were used to summarize the data for each
group using MD and 95% CIs. The statis-
tical unit was the patient and not the
implant. Meta-analysis was only at-
tempted if there were studies of similar
comparisons reporting the same outcome
measures. RRs combined for binary data
were for implant loss only.
Description of studies and
methodological quality
The search result is outlined in Fig. 1. A
total of 2116 titles were identified, and 547
abstracts were reviewed. Full-text analysis
included 49 articles, and two studies were
finally included in the review (Hardt et al.
2002; Karoussis et al. 2003). The main
reason for exclusion was: no control group
included with non-periodontitis-associated
tooth loss, less than 10 patients included,
focus on aspects other than implant treat-
ment in patients with periodontitis-asso-
ciated tooth loss, relevant results reported
in other publications, and inclusion of
patients both with and without perio-
dontitis-associated tooth loss. No articles
were added as the result of hand-searching.
The two studies are described below and
summarized in Table 1.
The patients included in the retrospec-
tive study by Hardt et al. (2002) were
selected among patients treated at the Brå-
nemark Clinic, Göteborg, Sweden. A total
of 97 partially edentulous patients with
346 Brånemark implants inserted in the
posterior part of the maxilla without bone
regeneration were included. The marginal
bone loss of the remaining teeth at the time
of the implant treatment planning was
assessed on panoramic radiographs and an
age-related periodontal marginal bone loss
score was estimated to describe the perio-
dontal destruction. Two-end quartiles were
used to define a periodontitis group of
individuals with susceptibility to perio-
dontitis (n ¼ 25) and a non-periodontitis
group of individuals with minimal perio-
dontal breakdown (n ¼ 25). All patients
were recalled according to the standard
protocol at the Brånemark Clinic after 1,
3, and 5 years. In addition, all patients
visited their regular dentist once a year. It
could not be assessed whether adequate
treatment of plaque-induced inflammatory
reactions was performed during the 5-year
period. The peri-implant marginal bone
level was assessed blindly on intraoral
radiographs mesially and distally. The pri-
mary outcome measures were implant loss
and peri-implant marginal bone loss during
a 5-year follow-up period.
A total of 100 and 92 implants, respec-
tively, were inserted in the periodontitis
and non-periodontitis group. Penicillin was
prescribed for 10 days after implant place-
ment, and fixed partial dentures were in-
serted after a 6-month healing period. At
the time of implant installation, the mean
age of the periodontitis and non-perio-
dontitis group was, respectively, 54 and
 Table 1. Summary of included studies
Patients Implants and Supra- Follow-up Results References
antibiotics structure period
Peri-implant tissues Perio- Suprastructure Other results
(years)
dontal and implant and comments
tissues survival rate
25 PE susceptible to periodontitis 100 Brånemark FD in 5 Bone loss: 2.2 mm NR Suprastructure: 92% Significant correlation Hardt et al. (2002)
Teeth witho50% bone support: Penicillin for posterior part Implants: 92% between peri-implant bone
26% 10 days of maxilla loss and periodontal bone loss
No. of teeth: 16 before implant therapy
Age: 54 years
Women: 52%, men: 48%
Smoking: NR

25 PE with minimal periodontal 92 Brånemark Bone loss: 1.7 mm Suprastructure:

breakdown Penicillin for 100%
Teeth witho50% bone support: 10 days Implants: 97%
1%
No. of teeth: 17
Age: 57 years
Women: 64%, men: 36%
Smoking: NR

8 PE with tooth loss due to 21 ITI (hollow screw) FD, STR 10 BOP: 29% NR Suprastructure: NR Significantly higher incidence Karoussis et al. (2003)
chronic periodontitis Antibiotics: NR PD: 3 mm Implants: 91% of biological complications in
Age: NR Bone loss, mesial: 1 mm Implants with patients with tooth loss due to
Gender: NR Bone loss, distal: 0.9 mm PD45 mm, BOP, chronic periodontitis
Proportion of implants in Implants with peri- annual bone loss
smokers: 48% implantitis (BOP, PD 0.2 mm: 48%
5 mm, and bone loss):

107 |
38%

45 PE with tooth loss due to 91 ITI (hollow screw) BOP: 40% Suprastructure: NR
other reasons than periodontitis Antibiotics: NR PD: 2.5 mm Implants: 97%
Age: NR Bone loss, mesial: 0.5 mm Implants with
Gender: NR Bone loss, distal: 0.5 mm PD45 mm, BOP,
Proportion of implants in Implants with peri- annual bone loss
smokers: 20% implantitis (BOP, PD 0.2 mm: 21%
5 mm, and bone loss):
5%

All group values referred to are expressed as mean values. Clinical parameters recorded at four sites per implant.
BOP, bleeding on probing; FD, fixed denture; NR, not reported; PD, probing depth; PE, partial edentulous; STR, single tooth replacement.

Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 104–123

Schou et al . Periodontitis and implants
Schou et al . Periodontitis and implants
57 years. The gender distribution was
comparable in the periodontitis group (wo-
men: 52%, men: 48%), while women
prevailed in the non-periodontitis group
(women: 64%, men: 36%). The proportion
of smokers was not reported. The number
of remaining teeth was comparable in the
two groups (periodontitis group: 16, non-
periodontitis group: 17). The proportion of
teeth with less than 50% bone support
was, respectively, 26% in the periodontitis
group and 1% in the non-periodontitis
group. Data on the periodontal health sta-
tus could not be obtained either at implant
placement or at 5-year follow-up. No pa-
tients were excluded from the study due to
loss of all implants.
The patients included in the retrospec-
tive study by Karoussis et al. (2003) were
treated at the Department of Perio-
dontology and Fixed Prosthodontics,
School of Dental Medicine, University of
Berne, Switzerland. A total of 53 partially
edentulous patients with 112 ITI hollow
screw implants were included. Two patient
groups were identified, namely individuals
with tooth loss due to chronic periodontitis
(n ¼ 8) and individuals with tooth loss due
to other seasons (caries, fracture, tooth
agenesia, and trauma) (n ¼ 45). The pa-
tients were incorporated in an individually
designed maintenance care program at the
Table 2. Quality assessment of included studies
Quality assessment parameters
Description of tooth loss, attachment loss and health status of
periodontal tissues at the time of implant placement for each
treatment group (yes, no)
Blinding of outcome assessment (yes, no)
Completeness of follow-up. A clear explanation for withdrawals and
drop-outs in each treatment group (yes, no)
Review: testing data
Comparison: 01 periodontitis versus non-periodontitis patients
Outcome: 01 prosthesis failure
Study periodontitis
or sub-category n/N
01 5 years
Hardt 2002 2/ 25
Subtotal (95% CI) 25
Total events: 2 (periodontitis), 0 (non-periodontitis)
Test for heterogeneity: not applicable
Test for overall effect: Z = 1.06 (P = 0.29)
Fig. 2. Comparison between patients with and without periodontitis-associated tooth loss: loss of suprastructures.
108 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 104–123
Department of Periodontology and Fixed
Prosthodontics, School of Dental Medi-
cine, University of Berne, or at the referring
dentist. Patients with periodontitis-asso-
ciated tooth loss were recalled usually at
3–5-month intervals, while patients with
non-periodontitis-associated tooth loss
were not recalled more frequently than at
4–8-month intervals. At every recall exam-
ination during the 10-year period, peri-im-
plantitis was recorded and treated according
to the so-called cumulative interceptive
supportive therapy (CIST) (Lang et al.
2000). Moreover, clinical and radiographic
examination was performed after 1 and 10
years of function. The peri-implant mar-
ginal bone level was assessed on intraoral
radiographs mesially and distally. The as-
sessment was performed blindly. The pri-
mary outcome measures were implant
loss, implant success, and incidence of
peri-implantitis during the 10-year follow-
up period. Peri-implantitis was defined by
probing depths of 5 mm or more, bleeding
on probing, and radiographic signs of mar-
ginal bone loss.
A total of 21 and 91 implants, respec-
tively, were inserted in the periodontitis
and non-periodontitis group without the
use of antibiotics. Single-tooth restorations
or fixed partial dentures were inserted after
a 4–6-month healing period. The age at the
Hardt Karoussis
et al. et al.
(2002) (2003)
No No
Yes Yes
Yes Yes
non-periodontitis RR (random)
n/N 95% CI
2/ 25
25
0.01 0.1 1 10
Favours treatment Favours control
time of implant installation was unre-
ported. When the two groups were consid-
ered together, 67 of the implants (60%)
were inserted in women and 45 (40%) in
men. In the periodontitis group, 48% of the
implants were inserted in smokers, while
the same figure for the non-periodontitis
group was 20%. The number of remaining
teeth at the time of implant placement was
unreported. Finally, the periodontal health
status was not reported either at implant
placement or at 10-year follow-up. No
patients were excluded from the study
due to loss of all implants.
Based on the above-described criteria for
quality assessment, the risk of bias was
judged to be high for both studies (Table 2).
Results
Survival of suprastructures
After the 5-year follow-up period, two of
the 25 suprastructures were removed in the
periodontitis group (8%), while none were
lost in the non-periodontitis group in the
study by Hardt et al. (2002). These data can
be seen in Fig. 2, along with the RR of 5
and its 95% CI from 0.25 to 99.16.
Although the risk of loss of the suprastruc-
tures in the periodontitis group was five
times that of the non-periodontitis group,
the P-value of 0.29 indicates that no sig-
nificant difference in survival of the supra-
structures was observed between the two
groups after 5-year follow-up.
The survival rate of the suprastructures
was unreported by Karoussis et al. (2003).
Survival of implants
After a 5-year follow-up, six patients lost
one implant each and one patient lost two
implants in the periodontitis group in the
study by Hardt et al. (2002). Consequently,
Weight RR (random)
% 95% CI Order
100.00 5.00 [0.25, 99.16] 0
100.00 5.00 [0.25, 99.16]
100
 Schou et al . Periodontitis and implants

eight of the 100 implants (8%) were lost in
seven patients in the periodontitis group,
while three of the 92 implants (3%) were
lost in three patients in the non-perio-
dontitis group. After a 5-year follow-up,
none of the 21 implants were lost in the
periodontitis group, while one of the 92
implants (2%) was lost in the non-perio-
dontitis group within the study by Karous-
sis et al. (2003). A meta-analysis was
conducted for the two studies at 5 years,
and no significant difference in survival of
the implants was observed. The black dia-
mond in Fig. 3 shows the combined RR of
2.24 (95% CI 0.71–7.04), which was not
significant (P ¼ 0.17).
After the 10-year follow-up period, two
implants (9.5%) were lost in two indivi-
duals in the periodontitis group and three
implants (3.5%) in three individuals in the
non-periodontitis group within the study
by Karoussis et al. (2003). These data are
shown in Fig. 3, which also shows an RR of
3.75 (95% CI 0.74–19.02), which was not
significant (P ¼ 0.11).
Incidence of peri-implantitis
The incidence of peri-implantitis was un-
reported by Hardt et al. (2002).
Peri-implantitis was revealed around
eight of the 21 implants (38%) in eight
patients in the periodontitis group and
around five of the 91 implants (5%) in
five patients in the non-periodontitis group
in the study by Karoussis et al. (2003).
Based on these data, significantly more
patients were affected by peri-implantitis
in the group with periodontitis-associated
than in the group with non-periodontitis-
associated tooth loss during the 10-year
follow-up period, RR of 9 (95% CI 3.94–
20.57) (Karoussis et al. 2003). These data
are shown in Fig. 4, along with the P-value
for this comparison (Po0.00001).
Peri-implant marginal bone loss
At the patient level, the peri-implant mar-
ginal bone loss from the time of abutment
placement to the 5-year follow-up was
2.2 mm (SD ¼ 0.8 mm) in the periodontitis
group and 1.7 mm (SD ¼ 0.8 mm) in the
non-periodontitis group in the study by
Hardt et al. (2002). Based on these data,
significantly increased peri-implant mar-
ginal bone loss was observed around im-
plants placed in patients with periodontitis-
associated tooth loss at 5-year follow-up,
MD 0.5 mm (95% CI 0.06–0.94) (P ¼ 0.03)
(Fig. 5).
The peri-implant marginal bone loss was
unreported at the patient level by Karoussis
et al. (2003).
Discussion
The current scientific knowledge about
implant treatment in individuals with pre-
vious tooth loss due to periodontitis was
assessed in the present systematic review.
Prospective and retrospective cohort stu-
dies with at least a 5-year follow-up com-
paring the outcome of implant treatment
in partially edentulous individuals with,
respectively, periodontitis-associated and
non-periodontitis-associated tooth loss

Review: testing data

Comparison: 01 periodontitis versus non-periodontitis patients
Outcome: 02 implant failure

Study periodontitis non-periodontitis RR (random) Weight RR (random)

or sub-category n/N n/N 95% CI % 95% CI Order

01 5 years
Hardt 2002 7/ 25 3 / 25 86.48 2.33 [0.68, 8.01] 0
Karoussis 2003 0/8 1 / 45 13.52 1.70 [0.08, 38.58] 0
Subtotal (95% CI) 33 70 100.00 2.24 [0.71, 7.04]
Total events: 7 (periodontitis), 4 (non-periodontitis)
Test for heterogeneity: Chi = 0.03, df = 1 (P = 0.85), l = 0%
Test for overall effect: Z = 1.37 (P = 0.17)

02 10 years
Karoussis 2003 2/ 8 3/ 45 100.00 3.75 [0.74, 19.02] 0
Subtotal (95% CI) 8 45 100.00 3.75 [0.74, 19.02]
Total events: 2 (periodontitis), 3 (non-periodontitis)
Test for heterogeneity: not applicable
Test for overall effect: Z = 1.60 (P = 0.11)

0.01 0.1 1 10 100

Favours treatment Favours control

Fig. 3. Comparison between patients with and without periodontitis-associated tooth loss: loss of implants.

Review: testing data

Comparison: 01 periodontitis versus non-periodontitis patients
Outcome: 03 periimplantitis

Study periodontitis non-periodontitis RR (random) Weight RR (random)

or sub-category n/N n/N 95% CI % 95% CI Order

02 10 years
Karoussis 2003 8 /8 5 /45 100.00 9.00 [3.94, 20.57] 0
Subtotal (95% CI) 8 45 100.00 9.00 [3.94, 20.57]
Total events: 8 (periodontitis), 5 (non-periodontitis)
Test for heterogeneity: not applicable
Test for overall effect: Z = 5.21 (P < 0.00001)

0.01 0.1 1 10 100

Favours treatment Favours control

Fig. 4. Comparison between patients with and without periodontitis-associated tooth loss: incidence of peri-implantitis.

109 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 104–123

Schou et al . Periodontitis and implants
Review: testing data
Comparison: 01 periodontitis versus non-periodontitis patients
Outcome: 04 bone level
Study periodontitis
or sub-category N Mean (SD)
01 5 years
Hardt 2002 25 2.20 (0.80)
Subtotal (95% CI) 25
Test for heterogeneity: not applicable
Test for overall effect: Z = 2.21 (P = 0.03)
Fig. 5. Comparison between patients with and without periodontitis-associated tooth loss: peri-implant marginal bone loss.
were assessed and two studies with 5- and
10-year follow-up, respectively, were iden-
tified (Hardt et al. 2002; Karoussis et al.
2003). A total of 121 implants were in-
stalled in 33 patients with previous tooth
loss due to periodontitis and 183 implants
were inserted in 70 patients with non-
periodontitis-associated tooth loss in the
two studies.
The survival of the suprastructures was
not significantly different in individuals
with periodontitis-associated and non-
periodontitis-associated tooth loss after 5
years. Also, the survival of the implants
was not significantly different after 5 and
10 years. When peri-implantitis was de-
fined by probing depths of 5 mm or more,
bleeding on probing, and radiographic signs
of marginal bone loss, significantly more
individuals with periodontitis-associated
tooth loss were affected by peri-implantitis
than individuals with non-periodontitis-as-
sociated tooth loss during the 10-year fol-
low-up period. Finally, significantly
increased peri-implant marginal bone loss
was observed in patients with previous
tooth loss due to periodontitis after 5 years.
Consequently, there is no appropriate
scientific evidence to conclude that indivi-
duals with periodontitis-associated tooth
loss demonstrate increased failure rates of
the suprastructures and the implants.
However, the sample size of the two stu-
dies is probably too small to detect a
difference in loss of suprastructures as
well as implants. Moreover, the quality
assessment of both studies indicated that
the risk of bias was high.
Therefore, the results should be inter-
preted with caution, and further long-term
studies involving a sufficient number of
patients are needed before final conclusions
can be drawn about the outcome of implant
treatment in patients with a history of
periodontitis. Particularly, the outcome of
110 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 104–123
non-periodontitis WMD (fixed)
N Mean (SD) 95% CI
25 1.70 (0.80)
25
−4 −2 0 2
Favours treatment Favours control
implant treatment in young adults with
aggressive periodontitis should be assessed.
However, it must be assumed that the
significantly higher incidence of peri-im-
plantitis and the significantly increased
peri-implant marginal bone loss in patients
with a history of periodontitis may jeopar-
dize the longevity of implant treatment. In
general, these conclusions are in accor-
dance with a recently published systematic
review including four studies with more
than a 5-year follow-up (van der Weijden
et al. 2005).
A total of 47 studies were excluded from
the present review because the inclusion
criteria were not fulfilled. When studies of
titanium implants, more than five patients
with periodontitis-associated tooth loss,
and a follow-up period of more than 1
year are considered, 19 studies were iden-
tified (Ericsson et al. 1986; Nevins &
Langer 1995; Mengel et al. 1996; Daele-
mans et al. 1997; Ellegaard et al. 1997a,
1997b; Schwartz-Arad & Chaushu 1998;
Buchmann et al. 1999; Sbordone et al.
1999; Mengel et al. 2001; Yi et al. 2001;
Leonhardt et al. 2002; Feloutzis et al. 2003;
Baelum & Ellegaard 2004; Karoussis et al.
2004; Wennström et al. 2004; Cordaro
et al. 2005; Jansson et al. 2005; Mengel
& Flores-de-Jacoby 2005a, 2005b).
These studies are frequently included in
the discussion of implant therapy in indi-
viduals with tooth loss due to periodontitis.
The main findings are summarized in Ta-
ble 3. Most studies focused on partially
edentulous patients. Although the number
of individuals within each patient group
varied between five and 766, most groups
involved less than 25 individuals. The
variation was huge, but most patients
were above the age of 55 years. The attach-
ment loss of the remaining teeth at the
time of implant placement was rarely spe-
cified. In addition, the subtype of perio-
Weight WMD (fixed)
% 95% CI Order
100.00 0.50 [0.06, 0.94] 0
100.00 0.50 [0.06, 0.94]
4
dontitis in the patients differed and was
mainly described by the terms ‘advanced
periodontitis’, ‘progressive periodontitis’,
‘aggressive periodontitis’, ‘chronic perio-
dontitis’, ‘severe periodontitis’, ‘moderate
to advanced periodontitis’, ‘tooth loss due
to periodontitis’, ‘periodontally compro-
mised’, and ‘treated for periodontal dis-
ease’. Therefore, elderly patients with
chronic periodontitis presumably prevailed.
Finally, the length of the follow-up period
varied, but most patients were followed less
than 3 years after placement of the supra-
structures. Therefore, firm conclusions
based on these studies cannot be provided.
Please note that publications from the
same research group may include at least
some patients in more than one study.
Similarly, additional reports are fre-
quently included in the discussion of im-
plant treatment in periodontitis-
susceptible individuals (Rosenquist &
Grenthe 1996; Grunder et al. 1999; Bro-
card et al. 2000; Polizzi et al. 2000; Quir-
ynen et al. 2001; van Steenberghe et al.
2002). Data for patients with periodontitis-
associated and non-periodontitis-associated
tooth loss were mixed and therefore not
usable for the present review. These studies
are summarized in Table 4.
The incidence of biological complica-
tions may depend on subtype of perio-
dontitis, i.e., aggressive and chronic
periodontitis (Mengel et al. 1996, 2001;
Mengel & Flores-de-Jacoby 2005a). How-
ever, the comparison of the treatment out-
come is compromised by a limited number
of included patients in each group (5–15)
and a short follow-up period (3–5 years).
Therefore, a detailed description of the
periodontal tissues and subtype of perio-
dontitis before implant treatment should be
included in future studies.
Infection control including extraction of
non-retainable teeth, oral hygiene instruc-
 Table 3. Summary of studies on implant treatment in individuals with periodontitis-associated tooth loss involving more than a 1-year follow-up period and more than five individuals
Patients Implants and Suprastructure Follow-up period Results References
antibiotics
Peri-implant tissues Periodontal Suprastructure Other results
tissues and implant and comments
survival rate
10 PE with advanced 41 Brånemark FD on implants 18 (6–30) months Plaque: 15% Plaque: 13% Suprastructure: 100% Significant Ericsson et al.
periodontitis Antibiotics: NR and teeth BOP: 8% BOP: 4% Implants: 100% difference in PD (1986)
Age: 31–60 years PD: 3.3 mm PD: 2.3 mm around implants
Women: 70%, men: 30% PD3 mm: 60% PD3 mm: 90% and teeth
Smoking: NR PD 4–5 mm: 38% PD 4–5 mm: 10%
PD6 mm: 2% PD6 mm: 0%
Bone loss: Most cases No bone loss
o1 mm, 3 implants:
1–3 mm

59 with PE and E jaws 309 Brånemark FD, RD 1 year: 23 implants Several patients with 1 NR Suprastructure: 100% NR Nevins &
Tooth loss due to Maxilla: 177 2 years: 42 implants or more implants with Implants, maxilla: Langer (1995)
recalcitrant periodontitis Mandible: 132 3–5 years: 185 implants bone loss to the 1st or 98%
(failed to respond to Antibiotics: NR 6–7 years: 38 implants 2nd thread Implants, mandible:
appropriate periodontal 8 years: 21 implants Seven implants with bone 97%
treatment) loss to the 4th thread
Age: 42–86 years
Gender: NR
Smoking: NR

19 PE with tooth loss 31 Astra (TiO2 Predominantly STR and 30 (12–40) months 1, 3 year NR 1, 3 year No significant Ellegaard
due to progressive blasted) FD Implants with plaque: Suprastructure: NR difference in et al. (1997a)
periodontitis Antibiotics: NR Two patients treated 0%, 17% Implants: 100%, implant survival
No. of maxillary teeth: 7 with partial RD Implants with BOP: 0%, 100% rate
No. of mandibular teeth: 32%
11 Implants with PDo4 mm:
Age: 60 years 88%, 44%
Women: 79%, men: 21% Implants with PD46 mm:
Smokers: 63% 0%, 0%
Implants with bone

111 |
losso1.5 mm: 100%, 76%
Implants with bone
loss43.5 mm: 0%, 0%

56 PE with tooth loss 93 ITI (hollow 33 (3–84) months 1, 3, 5 year 1, 3, 5 year

due to progressive screw) Implants with plaque: Suprastructure: NR
periodontitis Antibiotics: NR 17%, 31%, 45% Implants: 97%, 95%,
No. of maxillary teeth: 8 Implants with BOP: 11%, 95%
No. of mandibular teeth: 30%, 45%
10 Implants with PDo4 mm:
Age: 60 years 90%, 63%, 18%
Women: 75%, men: 25% Implants with PD46 mm:
Smokers: 64% 4%, 8%, 31%
Implants with bone
losso1.5 mm: 96%, 86%,
55%
Implants with bone
loss43.5 mm: 3%, 7%,
21%

Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 104–123

Schou et al . Periodontitis and implants
 Table 3. Continued
Patients Implants and Suprastructure Follow-up period Results References
antibiotics
Peri-implant tissues Periodontal Suprastructure Other results
tissues and implant and comments

112 |
survival rate
24 PE with tooth loss 25 Astra Predominantly STR and 31 months 1, 3 year NR 1, 3 year No significant Ellegaard
due to progressive (TiO2 blasted) FD Implants with plaque: Suprastructure: NR difference in et al. (1997b)
periodontitis No sinus lift Four patients treated 0%, 20% Implants: 100%, implant survival rate
Age: 57 (42–73) years Antibiotics: NR with partial RD Implants with BOP: 0%, 100% and frequency of
Women: 88%, men: 12% 35% implants without
Smokers: 63% Implants with PDo4 mm: plaque, BOP,
Mainly implants in 86%, 44% increased PD, and
maxilla with or without Implants with PD46 mm: bone loss around
sinus lift procedure 0%, 0% implants with or
Schou et al . Periodontitis and implants

No bone graft Implants with bone without sinus lift

losso1.5 mm: 100%, 76%
Implants with bone
loss43.5 mm: 0%, 0%

26 Astra 30 months 1, 3 year 1, 3 year

(TiO2 blasted) Implants with plaque: Suprastructure: NR

Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 104–123

Sinus lift 0%, 11% Implants: 95%, 95%
Antibiotics: NR Implants with BOP: 0%,
27%
Implants with PDo4 mm:
100%, 59%
Implants with PD46 mm:
0%, 0%
Implants with bone
losso1.5 mm: 95%, 82%
Implants with bone
loss43.5 mm: 5%, 5%

17 ITI 29 months 1, 3 year 1, 3 year

(hollow or solid Implants with plaque: Suprastructure: NR
screw) 8%, 18% Implants: 91%, 91%
No sinus lift Implants with BOP: 8%,
Antibiotics: NR 28%
Implants with PDo4 mm:
100%, 80%
Implants with PD46 mm:
0%, 0%
Implants with bone
losso1.5 mm: 91%, 71%
Implants with bone
loss43.5 mm: 9%, 9%

12 ITI 25 months 1, 3 year 1, 3 year

(solid screw) Implants with plaque: Suprastructure: NR
Sinus lift 0%, 14% Implants: 86%, 86%
Antibiotics: NR Implants with BOP: 0%,
14%
Implants with PDo4 mm:
100%, 64%
Implants with PD46 mm:
0%, 0%
Implants with bone
losso1.5 mm: 73%, 29%
Implants with bone
loss43.5 mm: 14%, 14%
 33 E and PE with tooth 121 Brånemark FD 40 (3–80) months NR NR Suprastructure: 98% NR Daelemans
loss due to periodontal Amoxicillin Implants: 93% et al. (1997)
disease 500 mg  4 or
Age: 52 (27–75) years clindamycine
Women: 48%, men: 52% 300 mg  3
Smoking: NR
Implants inserted in the
posterior part of maxilla
concomitant with the
sinus lift procedure and
AB from iliac crest

25 PE with moderate to 42 Brånemark NR 3 years 1, 2, 3 year 1, 2, 3 year 1, 2, 3 year Comparable Sbordone

advanced adult (MK III) PI: 0.9, 1, 1 PI: 1, 0.9, 0.7w Suprastructure: NR microflora around et al. (1999)
periodontitis Antibiotics: NR GI: 1.6, 1.7 GI: 1.6, 1.7w Implants: 100%, implants and teeth
Age: 37–68 years PD: 3.2, 3.3, 3.4 mm PD: 3.2, 3, 3 mmw 100%, 100% throughout study
Women: 52%, men: 48% Periodontal
Smoking: NR pathogens seldom
detected and when
detected at low levels

22 with severe 214 screw-type Full-arch FD 1 year: 211 implants NR NR 1, 5 year NR Schwartz-Arad
periodontitis titanium implants 5 years: 28 implants Suprastructure: NR & Chaushu
Age: 54 (36–66) years inserted Implants: 99%, 99% (1998)
Women: 73%, men: 27% immediately after
Smoking: NR extraction of all
AB chips into peri- teeth
implant defect when Maxilla: 128
necessary Mandible: 86
Amoxicillin or

113 |
erythromycin for
5–7 days

50 patients with chronic 167 Brånemark, FD, RD 5 years PI: 0.4 NR Suprastructure: 100% NR Buchmann
adult periodontitis IMZ, Frialit-2 GI: 0.4 Implants: 100% et al. (1999)
treated with the sinus Antibiotics: NR PD: 2.9 mm
lift procedure, AB, and
simultaneous implant
placement
Age: 52 years
Women: 58%, men: 42%
Smoking: NR

Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 104–123

Schou et al . Periodontitis and implants
 Table 3. Continued
Patients Implants and Suprastructure Follow-up period Results References

114 |
antibiotics
Peri-implant tissues Periodontal Suprastructure Other results
tissues and implant and comments
survival rate
37 periodontally healthy 60 IMZ, ITI, PI: 0.5
patients treated with Ledermann GI: 0.6
maxillary implants Antibiotics: NR PD: 3 mm
without the sinus lift
procedure and AB
Age: 44 years
Gender: NR
Smoking: NR
Schou et al . Periodontitis and implants

5 PE with generalized 36 Brånemark Predominantly FD 5 years 1, 2, 3, 4, 5 year Baseline and 1, 2, 3, Suprastructure: 100% Significantly more Mengel et al.
aggressive periodontitis Maxilla: 21 One patient treated PI: 0.8, 0.5, 0.3, 0.6, 0.7 4, 5 year Implants, maxilla: attachment loss at (1996, 2001)
Healthy periodontal Mandible: 15 with RD GI: 0.2, 0, 0.2, 0.5, 0.5 PI: 0.3, 0.9, 0.6, 0.7, 86% implants than teeth
tissues (PDo3 mm, no Antibiotics: NR PD: 2, 2, 2.2, 3.8, 3.3 mm 0.6, 0.8 Implants, mandible: Two teeth extracted
BOP) AL: 2, 2.3, 2.4, 4.7, GI: 0, 0.2, 0, 0.1, 0.3, 93% in one patient

Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 104–123

No. of teeth: 10 5.6 mm 0.5
Age: 31–44 years 1, 3, 5 year PD: 3, 3, 2.8, 3, 4.1,
Women: 100% Bone loss: 0.6, 0.8, 3.5 mm
Smokers: 20% 0.9 mm AL: 4.1, 4.5, 4.7, 4.9,
6.1, 6.3 mm
1, 3, 5 year
Bone loss: 1.6%,
3.4%, 5.1%

5 PE with generalized 12 Brånemark FD, STR 3 years 1, 2, 3 year Baseline and 1, 2, 3 Suprastructure: 100% No significant
chronic periodontitis Antibiotics: NR PI: 0.4, 0.5, 0.5 years Implants, maxilla: difference in
Healthy periodontal GI: 0.2, 0, 0.2 PI: 0.5, 0.3, 0.3, 0.3 100% attachment loss at
tissues (PDo3 mm, no PD: 3.1, 3, 3 mm GI: 0.2, 0.1, 0.2, 0.2 Implants, mandible: implants and teeth
BOP) AL: 4, 4.4, 5.5 mm PD: 2.7, 3, 2.8, 100%
No. of teeth: 23 1, 3 year 2.6 mm
Age: 35–42 years Bone loss: 0.1, 0.2 mm AL: 3.2, 3.7, 3.9,
Women: 100% 3.6 mm
Smoking: NR 1, 3 year
Bone loss: 1.5%, 2.7%

43 PE and E treated for 125 Astra (TiO2 FD 3 years 3 year NR Suprastructure: 100% NR Yi et al. (2001)
advanced periodontitis blasted) Surfaces with Implants: 100%
Age: 50 (26–65) years Amoxicillin plaque:o10%
Women: 53%, men: 47% 500 mg  2 for Bone loss: 0.2 mm
Smoking: NR 10 days Implants with bone loss
AB and ePTFE membrane 0.5 mm: 81%
concomitant with Implants with 0.5–2 mm
implant placement (n ¼ 5) bone loss: 19%
15 PE with advanced 57 Brånemark FD 10 years Implants with BOP: 61% Teeth with BOP: 35% Suprastructure: NR No significant Leonhardt
periodontitis Maxilla: 31 Bone loss: 1.7 mm Teeth with PD Implants, maxilla: correlation between et al. (2002)
Total No. of maxillary Mandible: 26 Implants with bone loss 4 mm: 16% 94% bone loss around
teeth: 125 Antibiotics: NR 0.5 mm: 15% Teeth with PD Implants, mandible: implants and teeth
Total No. of mandibular Implants with bone loss 6 mm: 3% 96% Survival of teeth: 87%
teeth: 136 0.6–2 mm: 52% Bone loss: 0.8 mm 5 patients without
Age: 21–71 years Implants with bone loss tooth loss
Women: 47%, men: 53% 2.1 mm: 33%
Smoking: NR
 90 PE treated for 182 ITI (hollow FD, STR 5.6 (2–12) years BOP: 15%n BOP: 13%n Suprastructure: NR Significantly Feloutzis et al.
chronic periodontitis cylinder, screw Bone loss, IL-1 positive Implants: 96% increased bone loss (2003)
Age: 60 (33–88) years cylinder, solid genotype: 0.2 mmn in heavy smokers as
Gender: NR screws) Bone loss, IL-1 negative compared to non-
Non-smokers: 43%, Antibiotics: NR genotype: 0.5 mmn smokers
former smokers (smoking No significantly
cessation45 years): 26%, different bone loss
moderate smokers (5–19 between IL-1 positive
cigarettes/day): 16%, and negative
heavy smokers (20 genotype individuals
cigarettes/day): 16% IL-1 positive genotype
individuals:
Significantly
increased bone loss in
heavy smokers as
compared to non-
smokers
IL-1 negative
genotype individuals:
No significantly
different bone loss in
heavy smokers as
compared to non-
smokers

32 periodontally 57 Astra Predominantly STR 68 (0–128) months 1, 5, 10 year NR 1, 5, 10 year 39 implants in 20 Baelum &
compromised PE (TiO2 blasted) and FD Implants with BOP: 0%, Suprastructure: NR patients treated Ellegaard
No. of maxillary teeth: 8 Antibiotics: NR Four patients treated 51%, 91% Implants: 100%, surgically due to (2004)
No. of mandibular teeth: with partial RD Implants with PDo4 mm: 97%, 97% peri-implantitis
11 98%, 55%, 25% However, 18 removed
Age: 60 (44–78) years Implants with PD46 mm: due to unsuccessful
Women: 75%, men: 25% 0%, 6%, 23% treatment
Smokers: 66% Implants with bone Smoking significantly
losso1.5 mm: 100%, associated with
85%, 70% increased implant

115 |
Implants with bone failure rate
loss43.5 mm: 0%, 5%,
5%

108 periodontally 201 ITI (hollow 74 (0–168) months 1, 5, 10 year 1, 5, 10 year

compromised PE and solid screw) Implants with BOP: 2%, Suprastructure: NR
No. of maxillary teeth: 8 Antibiotics: NR 46%, 70% Implants: 100%, 94%,
No. of mandibular teeth: Implants with PDo4 mm: 78%
10 95%, 40%, 24%
Age: 58 (34–87) years Implants with PD46 mm:
Women: 66%, men: 34% 1%, 15%, 25%
Smokers: 64% Implants with bone
losso1.5 mm: 98%, 72%,
60%
Implants with bone
loss43.5 mm: 0%, 6%,
14%

Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 104–123

Schou et al . Periodontitis and implants
 Table 3. Continued
Patients Implants and Suprastructure Follow-up period Results References
antibiotics
Peri-implant tissues Periodontal Suprastructure Other results
tissues and implant and comments

116 |
survival rate
51 PE with moderate to 149 Astra FD 5 years Plaque: 5% NR Suprastructure: 95% No significantly Wennström
advanced chronic Maxilla: 83 BOP: 5% Implants: 97% different bone loss et al. (2004)
periodontitis Mandible: 66 PD: 3.1 mm around implants with
Periodontal bone level: Minimum one PD3 mm: 80% TiO2 blasted and
44% TiO2 blasted and PD 4–5 mm: 15% machined surface
No. of teeth: 19 one with turned PD6 mm: 5%
Age: 60 (36–80) years surface in each Bone loss, implants with
Women: 61%, men: 39% patient TiO2 blasted surface:
Smokers: 33% Penicillin 1 g  2 0.5 mm
for 7 days Bone loss, implants with
Schou et al . Periodontitis and implants

turned surface: 0.3 mm

Bone loss, maxilla: 0.6 mm
Bone loss, mandible:
0.2 mm
Implants with42 mm
bone loss: 11%

Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 104–123

Bone loss, smokers:
0.8 mm
Bone loss, non-smokers:
0.2 mm

89 PE treated for 179 ITI (hollow FD, STR 10 (8–12) years PI: 0.4 Contralateral teeth: Suprastructure: NR PD around implants Karoussis et al.
periodontal disease screw, hollow BOP: 42% PI: 0.4 Implants: 92% significantly influenced (2004)
No. of teeth: 20 cylinder, PD: 2.8 mm BOP: 30% by full-mouth PD and
Age: 49 (19–78) years angulated hollow Bone loss: 0.7 mm PD: 2 mm full-mouth attachment
Women: 62%, men: 38% cylinder) Bone loss: 0.6 mm loss
Smoking: NR Maxilla: 104 Bone loss around
Mandible: 75 implants significantly
Antibiotics: NR influenced by smoking,
full-mouth attachment
level, and change in
full-mouth PD
Survival of teeth: 95%

766 PE treated for 1796 Brånemark NR Up to 10 years NR NR Suprastructure: NR Analysis involving 22 Jansson et al.
periodontal disease Maxilla: 1091 Implants, maxilla: patients with loss of (2005)
Age: NR Mandible: 705 97% 32 implants (at least
Women: 56%, men: 44% Antibiotics: NR Implants, mandible: one in each patient):
Smoking: NR 92% No significant
difference in implant
loss between IL-1
positive and negative
genotype individuals
Significantly
increased implant loss
in smokers than non-
smokers with IL-1
positive genotype
No significant
difference in implant
loss between smokers
and non-smokers
with IL-1 negative
genotype
 15 PE with generalized 52 Brånemark FD 3 years 1, 2, 3 year Baseline and 1, 2, 3 1, 2, 3 year Significantly greater Mengel &
aggressive periodontitis (MK II) and 25 PI: 0.5, 0.4, 0.3 year Suprastructure: attachment loss at Flores-de-
(generalized attachment Osseotite 3i GI: 0.1, 0.1, 0.2 PI: 0.4, 0.5, 0.5, 0.5 100%, 100%, 100% implants than teeth Jacoby (2005a)
loss 3 mm in 1 year at Maxilla: 47 PD: 2.5, 2.9, 3.2 mm GI: 0.1, 0.1, 0.1, 0.1 Implants, maxilla: in all groups
43 teeth excluded 1st Mandible: 30 AL: 2.9, 3.7, 4.3 mm PD: 3.2, 2.7, 2.9, 96%, 96%, 96% No significant
molars and incisors) Antibiotics: NR 1, 3 year 3.2 mm Implants, mandible: difference in clinical
Healthy periodontal Bone loss: 0.8, 1.1 mm AL: 4.4, 4.1, 4.4, 100%, 100%, 100% and radiographic
tissues (PD3 mm, 4.9 mm parameters between
no BOP) 1, 3 year groups
No. of teeth: 15 Bone loss: 1.7%, 3.5%
Age: 32 years
Women: 53%, men: 47%
Non-smokers

12 PE with generalized 17 Brånemark 1, 2, 3 year Baseline and 1, 2, 3 1, 2, 3 year

chronic periodontitis (MK II) and 26 PI: 0.4, 0.4, 0.6 year Suprastructure:
(generalized attachment Osseotite 3i GI: 0.1, 0.1, 0 PI: 0.3, 0.3, 0.3, 0.4 100%, 100%, 100%
losso3 mm in 1 year at Maxilla: 20 PD: 2.7, 2.7, 2.7 mm GI: 0.3, 0.1, 0.2, 0.1 Implants, maxilla:
43 teeth) Mandible: 23 AL: 3.9, 4.8, 4.6 mm PD: 2.8, 2.8, 2.6, 100%, 100%, 100%
Healthy periodontal Antibiotics: NR 1, 3 year 2.6 mm Implants, mandible:
tissues (PD3 mm, no Bone loss: 0.7, 0.9 mm AL: 3.9, 4.2, 4, 100%, 100%, 100%
BOP) 3.9 mm
No. of teeth: 19 1, 3 year
Age: 34 years Bone loss: 1.6%, 3%
Women: 50%, men: 50%
Non-smokers

12 PE periodontally 14 Brånemark 1, 2, 3 year Baseline and 1, 2, 3 1, 2, 3 year

healthy (PD3 mm, (MK II) and 16 PI: 0.3, 0.4, 0.5 year Suprastructure:
no BOP) Osseotite 3i GI: 0.1, 0.1, 0.1 PI: 0.6, 0.2, 0.4, 0.5 100%, 100%, 100%
No. of teeth: 25 Maxilla: 15 PD: 2.4, 3.2, 3.3 mm GI: 0.2, 0, 0.1, 0.1 Implants, maxilla:
Age: 31 years Mandible: 15 AL: 2.8, 4.3, 4 mm PD: 2.5, 2.5, 2.6, 100%, 100%, 100%
Women: 58%, men: Antibiotics: NR 1, 3 year 2.5 mm Implants, mandible:
42% Bone loss: 0.6, 0.7 mm AL: 2.8, 2.8, 3.1, 100%, 100%, 100%
Non-smokers 3 mm
1, 3 year

117 |
Bone loss: 1.3%, 2%

9 PE with reduced 71 ITI (solid Full-arch FD on implants 37 (24–94) months NR NR Suprastructure: Regardless of Cordaro et al.
periodontal support screw) and 19 3i and teeth with rigid or 100% connection type, no (2005)
(o2/3 bone support for (turned surface) non-rigid connection Implant survival: tooth intrusion when
all teeth) Antibiotics: NR 100% periodontal support
Age: NR Prosthetic reduced
Gender: NR complications: 0%
Smoking: NR

10 PE with normal Suprastructure: 100%

periodontal support (two new prosthesis)
(42/3 bone support Implant survival: 98%
for all teeth) Prosthetic
Age: NR complications: 40%
Gender: NR
Smoking: NR

Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 104–123

Schou et al . Periodontitis and implants
118 |
Table 3. Continued
Patients Implants and Suprastructure Follow-up period Results References
antibiotics
Peri-implant tissues Periodontal Suprastructure Other results
Schou et al . Periodontitis and implants

tissues and implant and comments

10 PE with generalized 15 Brånemark STR 3 years 1, 2, 3 year Baseline and 1, 2, 3 Suprastructure: 100% Significantly greater Mengel &
aggressive periodontitis (MK II) in maxilla PI: 0.3, 0.3, 0.3 year Implants: 100% attachment loss Flores-de-
(attachment loss 3 mm (incisor and GI: 0, 0, 0.3 PI: 0.2, 0.4, 0.5, 0.5 around implants in Jacoby (2005b)
in 1 year at 43 teeth) premolar regions) PD: 3.1, 3.4, 3.4 mm GI: 0, 0, 0.2, 0.1 regenerated bone
Healthy periodontal Amoxicillin AL: 5.1, 5.4, 5.7 mm PD: 2.8, 2.7, 2.9, than in non-

Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 104–123

tissues (PD3 mm, no BOP) 500 mg  3 for 3 1, 3 year 2.9 mm regenerated bone
Age: NR days Bone loss: 1.2, 1.8 mm AL: 3.7, 3.7, 4.1,
Women: 100% Significantly greater 4.1 mm
Non-smokers attachment loss at 1, 3 year
Vertical and horizontal implants than teeth Bone loss: 2.2%, 5.4%
guided bone regeneration
by titanium-reinforced
ePTFE membrane
supported by titanium
screws 6–8 months before
implant placement

10 periodontally healthy 11 Brånemark STR 1, 2, 3 year Baseline and 1, 2, 3 Suprastructure: 100%

PE (PDo3 mm, no BOP) (MK II) in maxilla PI: 0.3, 0.4, 0.5 year Implants: 100%
Age: NR (incisor and GI: 0.1, 0.1, 0.1 PI: 0.6, 0.2, 0.4, 0.5
Women: 80%, men: 20% premolar regions) PD: 3.4, 3.1, 3.3 mm GI: 0.2, 0, 0.1, 0.1
Non-smokers Antibiotics: NR AL: 3.9, 4.1, 4 mm PD: 2.5, 2.5, 2.6,
1, 3 year 2.5 mm
Bone loss: 1.1, 1.4 mm AL: 2.3, 2, 2.6, 2.5 mm
Significantly greater 1, 3 year
attachment loss at teeth Bone loss: 1.5%, 2.3%
than implants

All group values referred to are expressed as mean values, if not otherwise specified. Clinical parameters recorded at four sites per implant/tooth, if not otherwise specified.
n
Median.
wRecorded at 6 sites per tooth at one randomly selected tooth.
AB, autogenous bone; AL, attachment level; BOP, bleeding on probing; E, edentulous; ePTFE, expanded polytetrafluoroethylene; FD, fixed denture; GI, gingival index; NR, not reported; PD, probing depth; PE,
partial edentulous; PI, plaque index; RD, removable denture; STR, single-tooth replacement.
 Table 4. Summary of studies on various potential risk factors for implant loss and peri-implant marginal bone loss
Patients Implants and Supra- Follow-up Results References
antibiotics structure period
Peri-implant tissues Periodontal Suprastructure and Other results
tissues implant survival rate and comments
51 PE 109 Brånemark (turned FD, STR 31 (1–67) months NR NR Suprastructure: 100% Infection after 3–5 weeks Rosenquist &
Age: 33 (16–72) years surface) inserted Implants when tooth in five patients (four Grenthe
Women: 41%, men: 59% immediately after tooth extraction due to patients with tooth loss (1996)
Smoking: NR extraction periodontitis: 92% due to periodontitis)
ePTFE membrane in five Implants when tooth Exposure of cover screw in
patients extraction due to reasons 12 patients (10 patients
Penicillin for 10 days other than periodontitis: with tooth loss due to
96% periodontitis)

440 PE and E 1022 ITI (hollow screw, solid NR 5 years: 371 NR NR Suprastructure: NR Significantly lower implant Brocard et al.
Age: 53 (16–90) years screw, hollow cylinder) implants All patients after 4–5, 6–7 success rate in patients (2000)
Women: 58%, men: 42% Maxilla: 415 7 years: 132 year treated for periodontal
Smokers: 30% (mainlyo5 Mandible: 607 implants Implant success rate: 94%, disease after 6–7 years
cigarettes/day) Antibiotics: NR 83% Implant success rate not
147 (33%) treated for Patients treated for significantly influenced by
periodontal disease (oral periodontal disease before smoking
hygiene instruction, scaling, implant treatment after
root planing followed in 4–5, 6–7 year
some cases by periodontal Implant success rate: 89%,
surgery) before implant 75%
placement
Bone regeneration
(bioabsorbable collagen
membrane with or without
hydroxyapatite spacer)
before or concomitant with
placement of 177 implants

143 PE and E 264 Brånemark FD, STR 5 years Baseline and 1, 3, 5 year NR 3, 5 year Slight tendency of Grunder et al.
Age: 40–47 years Maxilla: 165 BOP, maxilla: 24%, 19%, Suprastructure: NR correlation between reason (1999);
Women: 52%, men: 48% Mandible: 99 21%, 25% Maxilla: 92%, 92% for tooth loss and implant Polizzi
Smoking: NR Placed immediately after BOP, mandible: 28%, Mandible: 95%, 95% failure et al. (2000)

119 |
tooth extraction (82%) or 3– 13%, 16%, 30% In 14 of 17 patients with
5 weeks after tooth PDo4 mm, maxilla: 82, implant failure, reason for
extraction (18%) with or 79%, 80%, 73% tooth extraction was
without membrane, freeze- PDo4 mm, mandible: periodontitis alone or one of
dried bone, AB, or collagen 91%, 92%, 95%, 88% reasons
Antibiotics: NR PD4 mm, maxilla: 18%, However, 78% of implants
21%, 20%, 27% inserted after tooth
PD4 mm, mandible: 9%, extraction due to
8%, 5%, 12% periodontitis
1, 5 year
Bone loss, maxilla, mesial:
1.4, 1.2 mm
Bone loss, maxilla, distal:
1.6, 1.2 mm
Bone loss, mandible,
mesial: 0.8, 0.7 mm
Bone loss, mandible,
distal: 0.9, 0.6 mm

Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 104–123

Schou et al . Periodontitis and implants
Schou et al . Periodontitis and implants

tion, scaling, root planing, and periodontal

AB, autogenous bone; BOP, bleeding on probing; E, edentulous; ePTFE, expanded polytetrafluoroethylene; FD, fixed denture; NR, not reported; PD, probing depth; PE, partial edentulous; RD, removable
Steenberghe
et al. (2001)

et al. (2002)
surgery, if indicated, was performed before
References

Quirynen
implant treatment. The importance of pre-
implant infection control is supported by

van
experimental studies in humans and ani-

failures when tooth loss due

not influenced by smoking
Bone loss around implants

Bone loss around implants

mals demonstrating that bacterial coloniza-

bone loss around teeth as

attachment nor bone loss

failures in heavy smokers

Significantly more early

Significantly more early

correlated with neither
tion of the implant surface may cause peri-

Significantly increased

compared to implants

(410 cigarettes/day)
implant mucositis (Berglundh et al. 1992;
and comments

Ericsson et al. 1992; Pontoriero et al. 1994;

Other results

around teeth
Abrahamsson et al. 1998; Zitzmann et al.

to trauma
2001). This has been further substantiated
by experimental studies in animals with
peri-implantitis due to ligature-enhanced
plaque accumulation (Lindhe et al. 1992;
Lang et al. 1993; Schou et al. 1993a,
implant survival rate
Suprastructure and

1993b). Moreover, the microflora around

Suprastructure: NR

implants and teeth appear to be similar in

Implants: 96%

Implants: 98%
partially edentulous patients with a history
of periodontitis, why periodontitis-asso-
ciated microorganisms may be transmitted
to implants from residual pockets of teeth
in partially edentulous patients (Leonhardt
Periodontal

loss: 0.7 mm
Attachment
Bone loss:

et al. 1993; Mombelli et al. 1995; Pa-

0.5 mm
tissues

paioannou et al. 1996; Quirynen et al.

NR

All group values referred to are expressed as mean values. Clinical parameters recorded at 4 sites per implant/tooth.
1996; Lee et al. 1999; Sbordone et al.
mandible, mesial: 8%, 8%
Bone loss42 mm, maxilla,

Bone loss42 mm, maxilla,

1999).
mandible, distal: 9%,
Peri-implant tissues

Attachment loss: NR

It is likely that the presence of perio-

mesial: 20%, 18%

Bone loss: 0.1 mm

Bone loss42 mm,

Bone loss42 mm,

distal: 24%, 18%

dontitis-associated microorganisms for an

extended period of time increases the risk
of peri-implantitis, especially in indivi-
Results

duals with tooth loss due to periodontitis.

12%

NR

Thus, it has been reported that the health

status of the peri-implant tissues is influ-
placement to 1
5 (3–11) years

From implant

enced by the health status of the perio-

month after
Follow-up

placement
abutment

dontal tissues (Brägger et al. 1997;

period

Karoussis et al. 2004). In other words, the

periodontal conditions may influence the
conditions of the peri-implant tissues.
FD, RD, STR
structure

Although such a relation was not found

Supra-

in one study (Quirynen et al. 2001), it is

FD

generally accepted that neglected or impro-

perly treated periodontitis may compro-
1263 Brånemark (turned
289 Brånemark (turned

mise the prognosis of implant treatment

by increasing the risk for biological com-
plications. This is why the importance of
Antibiotics: NR

Antibiotics: NR
Implants and

denture; STR, single-tooth replacement.

adequate infection control before implant

antibiotics

placement and an individualized supportive

Age at last visit: 63 (30–81) surface)

surface)

periodontal maintenance regimen was em-

phasized early and repeatedly underlined
Women: 67%, men: 33%

Women: 59%, men: 41%

for many years (Newman & Flemmig

Age: 50 (15–80) years

1988; Brägger et al. 1990).

Table 4. Continued

Various prophylactic antibiotic regimens

have been used to minimize the infection
399 PE and E
Smoking: NR

Smoking: NR

risk after implant installation, but this use

Patients

of antibiotics is controversial and no rando-

84 PE

years

mized clinical trial has been published so

far (Esposito et al. 2003). It was seldom

120 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 104–123


reported whether a prophylactic antibiotic
regimen was used at implant placement
(Tables 1 and 3). When reported, amoxicil-
lin was usually the treatment of choice.
Therefore, the scientific evidence to re-
commend use or non-use of antibiotics to
prevent infection after implant placement
is lacking and further studies are needed. It
is important to mention that infection
shortly after implant installation has been
reported more often in individuals with
tooth loss due to periodontitis than in
individuals with tooth loss due to reasons
other than periodontitis (Rosenquist &
Grenthe 1996). However, infection shortly
after implant installation and early implant
failure do not, even in patients with perio-
dontitis-associated tooth loss, seem to be a
major problem.
Implants inserted in regenerated bone
have demonstrated high survival rates, as
shown in three systematic reviews (Häm-
merle et al. 2002; del Fabbro et al. 2004;
Esposito et al. 2006). Three studies with a
3–5-year follow-up period were identified
in which bone regeneration in individuals
with periodontitis-associated tooth loss
was assessed (Ellegaard et al. 1997b; Buch-
mann et al. 1999; Mengel & Flores-
de-Jacoby 2005b). These studies showed a
similar survival of implants inserted in
either pristine bone or bone regenerated
with a barrier membrane or a sinus lift
procedure with or without autogenous
bone grafts.
It was beyond the scope of this review to
discuss the periodontal condition appropri-
ate for a tooth to be extracted and replaced
by an implant. However, it has been sug-
gested that periodontitis-affected teeth
should be extracted before the alveolar
bone is extensively resorbed (Nevins &
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