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Review
A comprehensive and critical reviewof dental implant prognosis inperiodontally compromised partiallyedentulous patients
Ioannis K. KaroussisSotirios KotsovilisIoannis Fourmousis
Authors’ affiliations:Ioannis K. Karoussis, Sotirios Kotsovilis, IoannisFourmousis, Department of Periodontology, Schoolof Dental Medicine, University of Athens, Athens,Greece
Correspondence to:Dr Ioannis K. KaroussisDepartment of PeriodontologySchool of Dental MedicineUniversity of AthensThivon Street 2GR 11527 AthensGreeceTel.: þ30 210 7461203Fax: þ30 210 7461202e-mail: [email protected]
Key words: aggressive periodontitis, chronic periodontitis, dental implants, periodontally
compromised patients, survival
Abstract
Objectives: The outcome of implant treatment in periodontally compromised partially
edentulous patients has not been completely clarified. Therefore, the aim of the present study
was to perform, applying a systematic methodology, a comprehensive and critical review of
the prospective studies published in English up to and including August 2006, regarding the
short-term (o5 years) and long-term ( � 5 years) prognosis of osseointegrated implants
placed in periodontally compromised partially edentulous patients.
Material and methods: Using The National Library Of Medicine and Cochrane Oral Health
Group databases, a literature search for articles published up to and including August 2006 was
performed. At the first phase of selection the titles and abstracts and at the second phase full
papers were screened independently and in duplicate by the three reviewers (I. K. K., S. K., I. F.).
Results: The search provided 2987 potentially relevant titles and abstracts. At the first phase of
evaluation, 2956 publications were rejected based on title and abstract. At the second phase,
the full text of the remaining 31 publications was retrieved for more detailed evaluation. Finally,
15 prospective studies were selected, including seven short-term and eight long-term studies.
Because of considerable discrepancies among these studies, meta-analysis was not performed.
Conclusions: No statistically significant differences in both short-term and long-term implant
survival exist between patients with a history of chronic periodontitis and periodontally healthy
individuals. Patients with a history of chronic periodontitis may exhibit significantly greater
long-term probing pocket depth, peri-implant marginal bone loss and incidence of peri-
implantitis compared with periodontally healthy subjects. Even though the short-term implant
prognosis for patients treated for aggressive periodontitis is acceptable, on a long-term basis the
matter is open to question. Alterations in clinical parameters around implants and teeth in
aggressive periodontitis patients may not follow the same pattern, in contrast to what has been
reported for chronic periodontitis patients. However, as only three studies comprising patients
treated for aggressive periodontitis were selected, more studies, specially designed, are required
to evaluate implant prognosis in this subtype of periodontitis. As the selected publications
exhibited considerable discrepancies, more studies, uniformly designed, preferably longitudinal,
prospective and controlled, would be important.
Dental implant placement is an effective
and predictable treatment modality for re-
placing missing teeth in both fully (Brane-
mark et al. 1977; Mericske-Stern et al.
1994) and partially (Jemt 1986; Buser
et al. 1997) edentulous patients. Recent
systematic reviews (Berglundh et al.
2002; Lang et al. 2004; Pjetursson et al.
Date:Accepted 9 November 2006
To cite this article:Karoussis IK, Kotsovilis S, Fourmousis I. Acomprehensive and critical review of dental implantprognosis in periodontally compromised partiallyedentulous patients.Clin. Oral Impl. Res. 18, 2007; 669–679doi: 10.1111/j.1600-0501.2007.01406.x
c� 2007 The Authors. Journal compilation c� 2007 Blackwell Munksgaard 669
2004) have provided the highest level of
evidence supporting the favourable long-
term prognosis of implant therapy in the
general population. However, fewer data
seem to be available concerning the prog-
nosis of implants placed in periodontally
compromised patients.
A plethora of studies have proved that in
partially edentulous patients, periodontal
pathogens may be transmitted from teeth
to implants, implying that periodontal
pockets may serve as reservoirs for bacterial
colonization around implants (Apse et al.
1989; Quirynen & Listgarten 1990; Leon-
hardt et al. 1992, 1993; Mombelli et al.
1995; Papaioannou et al. 1995, 1996; Gou-
voussis et al. 1997; Sbordone et al. 1999;
De Boever & De Boever 2006; Quirynen
et al. 2006). A comprehensive review (Hey-
denrijk et al. 2002) of the studies published
up to and including December 2000, con-
cerning the microflora around implants,
has drawn the following conclusions: The
microbiota of the oral cavity before implant
placement determines the composition of
the peri-implant microflora; the microflora
of peri-implantitis lesions resembles that of
chronic periodontitis.
The similarity in microbial flora respon-
sible for periodontitis and peri-implantitis
supports the concept that periodontal
pathogens may be associated with peri-
implant infections and failing implants
(Mombelli et al. 1987; Mombelli & Lang
1992). An association between periodontal
and peri-implant conditions has been de-
monstrated (Bragger et al. 1997; Karoussis
et al. 2004), leading to the conclusion that
‘the rate of progression of attachment loss
adjacent to teeth and implants is similar in
a given patient’ (Karoussis et al. 2004).
This supports the hypothesis that an in-
creased susceptibility for periodontitis
might also imply an increased susceptibil-
ity for peri-implantitis.
The importance of periodontal therapy
before implant placement in partially eden-
tulous patients has been emphasized (Brag-
ger et al. 1997). According to this concept,
the potential colonization of the newly
formed peri-implant ecological niches by
presumptive periodontal pathogens would
be avoided. However, it has been reported
that potential periodontal pathogens pre-
sent in the oral cavity may not necessarily
act as peri-implant pathogens (Rams et al.
1991; Leonhardt et al. 1993; Pontoriero
et al. 1994; Nevins & Langer 1995; Hey-
denrijk et al. 2002). Moreover, the presence
of putative periodontopathogens at peri-im-
plant and periodontal sites might not be
associated with future attachment loss, as
reported for both teeth and implants (Of-
fenbacher 1996; Sbordone et al. 1999; Ne-
vins 2001). Periodontopathogens may be
randomly detected at both stable and dete-
riorating periodontal and peri-implant sites
(Iacono et al. 1991; Socransky et al. 1991).
On the other hand, genetic factors have
been highly implicated in the pathogenesis
of periodontitis (Kornman et al. 1997; Wil-
son & Nunn 1999; Michalowicz et al.
2000; Feloutzis et al. 2003; Gruica et al.
2004) and susceptible subjects are consid-
ered to elicit a more intense response to
infectious agents, thereby inducing a more
pronounced tissue breakdown (Page et al.
1997). These data support the hypothesis
that implant prognosis in periodontally
compromised patients may be less favour-
able than in periodontally healthy subjects,
even in the case of a successful periodontal
therapy before implant installation.
Therefore, the aim of the present study
was to perform, applying a systematic
methodology, a comprehensive and critical
review of the prospective studies published
in the international peer-reviewed litera-
ture in the English language up to and
including August 2006, regarding the
short-term (o5 years) and the long-term
( � 5 years) prognosis of implants placed
in periodontally compromised partially
edentulous patients.
Material and methods
Search strategy
Using the National Library of Medicine
(http://www.ncbi.nlm.nih.gov/PubMed) and
Cochrane Oral Health Group databases, a
literature search was performed with a
personal computer (PC) on articles pub-
lished up to and including August 2006
in the English language.
The terms and key words used in the
search were:
(‘Dental’ OR ‘Oral’)
AND
(‘Implantn’ OR ‘Periimplantn’ OR ‘Peri-
implantn’)
AND
(‘Periodontn’)
Data sources also included the reference
lists of identified publications and several
hand-searched journals (British Journal of
Oral and Maxillofacial Surgery, British
Journal of Oral Surgery, Clinical Oral
Implants Research, Implant Dentistry, In-
ternational Journal of Oral & Maxillofa-
cial Implants, International Journal of
Oral and Maxillofacial Surgery, Interna-
tional Journal of Periodontics Restorative
Dentistry, International Journal of
Prosthodontics, Journal of Clinical Perio-
dontology, Journal of Maxillofacial Sur-
gery, Journal of Periodontal Research,
Journal of Periodontology, Journal of Oral
Surgery, Journal of Oral and Maxillofacial
Surgery, Journal of Prosthetic Dentistry).
Screening and selection
At the first phase of selection, the titles and
abstracts were screened independently and
in duplicate by the three reviewers (I. K. K.,
S. K., I. F.) for possible inclusion in the
review, based on defined inclusion criteria.
The inclusion criteria were as follows:
(1) Publications written only in the Eng-
lish language
(2) Clinical studies only
(3) Prospective design
(4) Placement of osseointegrated dental
implants in periodontally compro-
mised partially edentulous patients.
If both periodontally compromised pa-
tients and periodontally healthy indivi-
duals were enrolled in a study, separate
data should have been reported for each of
these two distinct categories of partici-
pants; similarly, if both totally and partially
edentulous patients participated in a study,
separate results for each of these two groups
should have been provided, otherwise the
study could not be included in the present
review.
(5) Completion of periodontal therapy be-
fore implant placement and absence of
active inflammation at the recipient
site at the time of implantation clearly
defined
(6) Follow-up period of more than 1 year
(7) Report of data revealing implant sur-
vival (or success) rate in periodontally
compromised partially edentulous pa-
tients
At the second phase of selection, the full
text of all selected studies was obtained.
Karoussis et al . Dental implant prognosis in periodontally compromised partially edentulous patients
670 | Clin. Oral Impl. Res. 18, 2007 / 669–679 c� 2007 The Authors. Journal compilation c� 2007 Blackwell Munksgaard
Subsequently, these studies were examined
independently and in duplicate by the three
reviewers (I. K. K., S. K., I. F.), based on the
aforementioned inclusion criteria. In case
of any potential disagreement among the
reviewers, consensus had to be achieved by
discussion.
Results
The search provided 2987 potentially rele-
vant titles and abstracts. Following the first
phase of evaluation, 2956 publications
were rejected based on title and abstract.
At the second phase, the full text of the
remaining 31 publications was retrieved for
more detailed evaluation.
Finally, 15 prospective studies were se-
lected. These included seven short-term
(Ericsson et al. 1986; Ellegaard et al.
1997a, 1997b; Buchmann et al. 1999;
Sbordone et al. 1999; Mengel & Flores-
de-Jacoby 2005a, 2005b) and eight long-
term studies (Brocard et al. 2000; Mengel
et al. 2001; Leonhardt et al. 2002; Karous-
sis et al. 2003; Baelum & Ellegaard 2004;
Rosenberg et al. 2004; Wennstrom et al.
2004; Ellegaard et al. 2006).
Of these publications, seven studies
(Ericsson et al. 1986; Ellegaard et al.
1997a, 1997b; Buchmann et al. 1999;
Sbordone et al. 1999; Mengel et al. 2001;
Mengel & Flores-de-Jacoby 2005a) re-
ported short-term data for chronic perio-
dontitis patients (Table 1), six studies
(Brocard et al. 2000; Karoussis et al. 2003;
Baelum & Ellegaard 2004; Rosenberg et al.
2004; Wennstrom et al. 2004; Ellegaard
et al. 2006) reported long-term data for
chronic periodontitis patients (Table 2),
two studies (Mengel & Flores-de-Jacoby
2005a, 2005b) reported short-term data
for generalized aggressive periodontitis pa-
tients (Table 3) and one study (Mengel et al.
2001) reported long-term data for aggres-
sive periodontitis patients (Table 3). A
long-term study (Mengel et al. 2001) re-
Table 1. The selected short-term (o5 years) studies in partially edentulous patients with a history of chronic periodontitis
Authors(publicationdate)
Groups/implants(N)
Follow-up ISR MPBL Comments
Ericssonet al.(1986)
10 PC, 41Branemark
s
impls
Mean: 18 months,range: 6–30 months
100% Most cases: o1 mm3 impls: 41 mm(up to 3 mm)
No control group (no PH)Limited number of patientsRelatively short follow-up periodCombination of implants andteeth as abutments for fixedbridges
Ellegaardet al. (1997a)
19 PC, 31 Astras
impls, 56 PC, 93ITI
s
impls
Astras
impls: mean30 � 7.4 months,ITI
s
impls: mean33.3 � 21.8 months
Maxilla: 97.3%,mandible: 92.3%
At 36 months: 76.3% ofAstra
s
impls and 88.5%of osseointegrated ITI
s
impls had MPBLo1.5 mmAt 60 months: 57% ofosseointegrated ITI
s
implshad MPBLo1.5 mm
No control group (no PH)64% of the patients weresmokers
Ellegaardet al. (1997b)
24 PC, 25 Astras
,26 Astra
s
sinus,17 ITI
s
, 12 ITIs
sinus
Astras
impls: mean30.8 months, Astra
s
sinus impls: mean29.9 months, ITI
s
impls: mean 29.4months, ITI
s
sinusimpls: mean 25.3months
Astras
: 100%,Astra
s
sinus: 95%,ITI
s
:90.9%, ITI
s
sinus:85.7%
At 36 months: 76.2%,82.3%, 70.7% and 29.2%of Astra
s
, Astras
sinus,ITI
s
, ITIs
sinus impls, resp., hadMPBLo1.5 mm
No control group (no PH)15 patients were smokersSinus membrane elevationwas included
Sbordoneet al. (1999)
25 PC, 42Branemark
s
impls3 years 100% Not reported No control group (no PH)
No implant losses were reportedBuchmannet al. (1999)
50 PC, 36 Branemarks
,88 Frialit-2
s
, 43 IMZs
impls
3 years 100% (167/167) Not reported No control group (no PH)Sinus membrane elevationwas performed
Mengelet al. (2001)
5 PC, 12 Branemarks
impls3 years 100% 0.19 mm No control group (no PH)
Limited number of patientsOnly patients with generalizedchronic periodontitis areincludedin this table; data forgeneralized aggressiveperiodontitis are presentedin Table 3
Mengel &Flores-de-Jacoby(2005a)
12 PC, 43 impls, 12 PH, 30impls (MK II & Osseotite)
3 years PC: 100%,PH: 100%
PC: 0.86 mm,PH: 0.7 mm
Only patients with generalizedchronic periodontitis areincluded in this table; patientswith generalized aggressiveperiodontitis are included inTable 3Smokers were excluded.
N, number; ISR, implant survival rate; MPBL, mean peri-implant marginal bone loss; PC, periodontally compromised patients (with a history of chronic
periodontitis); PH, periodontally healthy subjects; impl(s), implant(s); resp., respectively.
Karoussis et al . Dental implant prognosis in periodontally compromised partially edentulous patients
c� 2007 The Authors. Journal compilation c� 2007 Blackwell Munksgaard 671 | Clin. Oral Impl. Res. 18, 2007 / 669–679
ported short-term (3 years) data for general-
ized chronic periodontitis patients (Table 1)
and long-term (5 years) data for generalized
aggressive periodontitis patients (Table 3).
It should be noted that in a long-term study
(Leonhardt et al. 2002), the patients, aged
21–71 years at implant surgery, had been
affected with advanced periodontitis. How-
ever, the subtype of periodontitis (chronic
or aggressive) was not clearly defined and
therefore the possibility of the inclusion of
aggressive periodontitis patients in this
study, along with patients treated for chronic
periodontitis, cannot be ruled out. This
study has been incorporated in Table 2.
Discussion
The present study evaluated, applying a
systematic methodology, any currently
available information about the effective-
ness and predictability of dental implant
therapy in partially edentulous perio-
dontally compromised patients. Therefore,
studies up to and including August 2006,
regarding the prognosis of implants placed
in this subgroup of patients, were critically
analysed. A previous review (van der Weij-
den et al. 2005) evaluated studies up to and
including October 2003, concerning the
long-term (�5 years) prognosis of implants
placed in partially edentulous periodontally
compromised patients, selected four stu-
dies and concluded that there were limited
data available by that time. A recent pub-
lication (Schou et al. 2006) assessed studies
up to and including December 2005 and
finally selected two studies (Hardt et al.
2002; Karoussis et al. 2003), already in-
cluded in the previous review (van der
Weijden et al. 2005).
In an effort to acquire the broadest possible
spectrum of information on the subject, the
present comprehensive and critical review
included both short-term (o5 years) and
long-term ( � 5 years) studies. Moreover,
Table 2. The selected long-term (�5 years) studies in partially edentulous patients with a history of chronic periodontitis
Authors(publicationdate)
Groups/implants (N) Follow-up ISR MPBL Comments
Brocard et al.(2000)
147 PC, 375 ITIs
impls7 years 74.7% (success,
according to Buseret al. 1997)Global success:83.4%
Not mentioned Smokers were includedGlobal success rate refers tothe entire study population
Leonhardt etal. (2002)
15 PC, 57 Branemarkimpls
10 years 94.74% 1.7 � 1.2 mm (or1.7 � 1.1 mm)Inconsistency ofdata between thetext and Table 1 ofthe study
Subtype of periodontitis(chronic or aggressive) was notclearly definedNo control group (no PH)
Karoussis etal. (2003)
8 PC, 21 impls, 45 PH,91 impls
10 years PC total: 90.5%, PHtotal: 96.5%, PCsmokers: 80%, PHsmokers: 100%, PCnon-smokers: 100%,PH non-smokers:95.7%
PC: mesial1 � 1.38 mm, distal0.94 � 0.73 mm, PH:mesial0.48 � 1.1 mm,distal0.5 � 1.08 mm
Limited number of PCSmokers were included in thestudy, but separate resultswere provided for smokers andnon-smokers
Wennstromet al. (2004)
51 PC, 149 AstraTech
s
impls5 years 97.32% 0.41 � 1.01 mm
(mean on impl level)No control group (no PH)17 of the patients (one-third)were current smokers
Rosenberg etal. (2004)
151 PC, 923 impls,183 PH, 588 impls(8 impl systems)
13 years PC: 90.6%, PH:93.7%
Not reported ‘Survival’ was definedaccording to Albrektsson et al.(1986)
Baelum &Ellegaard(2004)
140 PC, 258 impls(201 one-stage ITI
s
impls in 108 PC and57 two-stage Astra
s
impls in 32 PC)
Duration: 14 yearsfollow-up (mean/range): one-stageimpls: 73.6 months/0–168 months, two-stage impls: 68.2months/0–128months
At 5 years: one-stage94.3%, two-stage97.4%At 10 years: one-stage 77.7%, two-stage 97.4%
MPBL: not reportedAt 10 years bone loss� 1.5 mm: one-
stage impls 40%,two-stage 31%Bone loss� 3.5 mm: one-
stage 14%, two-stage 5%
No control group (no PH)About 65% of the patientswere smokers
Ellegaard etal. (2006)
68 PC, 50 Astras
conventional impls,59 Astra
s
sinusimpls, 81 ITI
s
conventional impls,72 ITI
s
sinus impls
Follow-up (mean/range): Astra
s
impls:67.7 months/0–128months, Astra
s
sinusimpls: 64.2 months/0–128 months, ITI
s
impls: 61 months/0–147 months, ITI
s
sinus impls: 57.5months/0–143months
10-year estimates:Astra
s
impls: 97%,Astra
s
sinus impls:85.4%, ITI
s
impls:59%, ITI
s
sinusimpls: 79.9%
MPBL: not reportedAt 10 years bone loss� 3.5 mm: Astra
s
impls 5.9%, Astras
sinus impls 4.8%,ITI
s
impls 12.2%, ITIs
sinus impls 1.8%
No control group (no PH)Sinus membrane elevationwithout grafting was included57% (for Astra
s
) and 68% (forITI
s
) of the patients weresmokers
N, number; ISR, implant survival or success rate; MPBL, mean peri-implant marginal bone loss; PC, periodontally compromised patients (with a history of
chronic periodontitis); PH, periodontally healthy subjects; impl(s), implant(s).
Karoussis et al . Dental implant prognosis in periodontally compromised partially edentulous patients
672 | Clin. Oral Impl. Res. 18, 2007 / 669–679 c� 2007 The Authors. Journal compilation c� 2007 Blackwell Munksgaard
a distinct evaluation between data on im-
plant prognosis in patients with a history of
chronic periodontitis and those treated for
aggressive periodontitis was performed. In
order to increase the validity of the obtained
results, only studies of a prospective design
were included and furthermore studies re-
porting mixed data, on both totally and
partially edentulous patients, were excluded.
Definition of ‘periodontally compromised’patients
The necessity for a definition of ‘perio-
dontally compromised’ patients has been
particularly emphasized (van der Weijden
et al. 2005). A consensus definition has
not been universally accepted as yet. Some
of the studies selected in the present review
have provided a concept of ‘periodontally
compromised’ patients (Ericsson et al.
1986; Ellegaard et al. 1997a, 1997b, 2006;
Mengel et al. 2001; Karoussis et al. 2003;
Baelum & Ellegaard 2004; Mengel & Flores-
de-Jacoby 2005a, 2005b). According to these
studies, the ‘periodontally compromised’
patients have a history of periodontitis
(chronic or aggressive), but no active disease
at the time of implant placement. The
patients have been subjected to ‘successful’
periodontal therapy (non-surgical and/or sur-
gical) before implant placement. It has been
stressed that neglected or poorly treated
periodontitis might increase the risk for
peri-implantitis (Leonhardt et al. 2002).
However, there is no unanimously accepted
definition for ‘successful’ periodontal ther-
apy; the selected studies have not clearly
defined the periodontal status of the patients
at the time of implant placement.
Implant survival rates
Short-term studies/patients with a history ofchronic periodontitis (Table 1)
The selected short-term studies have re-
ported implant survival rates in patients
with a history of chronic periodontitis
well above 90%, reaching 100% in certain
cases. These survival rates are comparable
to the mean implant survival rates reported
for the general population (Lang et al. 2004;
Pjetursson et al. 2004).
Long-term studies/patients with a history ofchronic periodontitis (Table 2)
The majority of the selected long-term
studies have reported implant survival rates
in patients with a history of chronic perio-
dontitis well above 90% (Leonhardt et al.
2002; Karoussis et al. 2003; Rosenberg
et al. 2004; Wennstrom et al. 2004), reach-
ing up to 97.32% (Wennstrom et al. 2004).
Only two studies (Baelum & Ellegaard
2004; Ellegaard et al. 2006) have reported
implant survival rates o90%. However,
both studies included hollow-screw im-
plants, many of which had a short length
(defined by the authors as length
�10 mm). These lower survival rates
were attributed by the authors to the deci-
sion to remove surgically hollow implants,
when peri-implantitis had occurred, as
treatment of peri-implantitis in this type
of implants was considered virtually im-
possible. Furthermore, it has been reported
that hollow implants tend to perform
slightly worse than solid implants (Buser
et al. 1997).
In conclusion, the long-term survival
rates of implants placed in partially eden-
tulous patients with a history of chronic
periodontitis are comparable to the mean
implant survival rates reported for the gen-
eral population (Berglundh et al. 2002;
Lang et al. 2004; Pjetursson et al. 2004).
Aggressive periodontitis (Table 3)
The reported short-term implant survival
rates for patients treated for aggressive
periodontitis were above 95% (Mengel &
Flores-de-Jacoby 2005a), reaching up to
100% (Mengel & Flores-de-Jacoby
2005b). However, the only available long-
term study (Mengel et al. 2001) reported a
5-year implant survival rate of 88.8%.
Therefore, the long-term survival of im-
plants in patients treated for aggressive
periodontitis still remains open to question
and more studies are required.
Probing pocket depth (PPD) and clinicalattachment level (CAL)
Short-term studies/patients with a history ofchronic periodontitis (Table 1)
Sbordone et al. (1999) reported no statisti-
cally significant alterations in PPD and
CAL around implants placed in patients
with a history of chronic periodontitis
throughout a 3-year observation period.
Furthermore, no statistically significant
differences in clinical parameters were
found between implants and the selected
control teeth. However, 10% of the im-
plant sites had a mean clinical attachment
Table 3. The selected short-term (o5 years) and long-term (�5 years) studies in partially edentulous patients treated for generalizedaggressive periodontitis
Authors(publicationdate)
Groups/implants (N) Follow-up ISR MPBL Comments
Mengelet al. (2001)
5 PC, 36Branemark
s
impls5 years (longterm)
88.8% (reportedas ‘success’ in thestudy)
0.88 mm No control group (no PH)Limited number of patientsOnly patients with generalized aggressive periodontitisare reported in this table; data for generalized chronicperiodontitis are included in Table 1
Mengel &Flores-de-Jacoby(2005a)
15 PC, 77 impls, 12PH, 30 impls(MK II & Osseotite)
3 years(short term)
PC: 95.7% in themaxilla, 100% inthe mandible,PH: 100%
PC (mean,total):1.14 mm, PH:0.7 mm
Patients with generalized aggressive periodontitisare included in this table; patients with generalizedchronic periodontitis are included in Table 1Smokers were excluded
Mengel &Flores-de-Jacoby(2005b)
10 PC, 15 impls,10 PH, 11 impls(MK II & NobelBiocare)
3 years(short term)
PC: 100%, PH:100%
PC: 1.78 mm,PH: 1.31 or1.4 mm
GBR was performed in all PCInconsistency of data reporting on MPBL betweenthe text (1.31 mm) and Table 4 (1.4 mm) of the study
N, number; ISR, implant survival rate; MPBL, mean peri-implant marginal bone loss; PC, periodontally compromised patients (treated for generalized
aggressive periodontitis); PH, periodontally healthy subjects; impl(s), implant(s); GBR, guided bone regeneration.
Karoussis et al . Dental implant prognosis in periodontally compromised partially edentulous patients
c� 2007 The Authors. Journal compilation c� 2007 Blackwell Munksgaard 673 | Clin. Oral Impl. Res. 18, 2007 / 669–679
loss of 2.5 mm over the 3 years. A similar
stability of PPD at teeth and implants of
chronic periodontitis patients was reported
in other short-term studies (Mengel et al.
2001; Mengel & Flores-de-Jacoby 2005a).
In these two studies, unlike PPD, which
remained unchanged in the first 3 years, a
continuous clinical attachment loss was
recorded only around implants. This intri-
guing finding was attributed to peri-im-
plant soft tissue recession. Furthermore,
in the first study (Mengel et al. 2001) no
differences in PPD and CAL between im-
plants and teeth were found. However, in
the second study (Mengel & Flores-de-
Jacoby 2005a) clinical attachment loss
was statistically significantly higher at
the implants than at the teeth. Neverthe-
less, it is clear that, on a long-term obser-
vation basis, changes in PPD and CAL
follow the same pattern around both teeth
and implants (Karoussis et al. 2004).
Mengel & Flores-de-Jacoby (2005a)
found no statistically significant differ-
ences in clinical parameters among perio-
dontally compromised patients with
chronic periodontitis and periodontally
healthy controls.
Ellegaard et al. (1997a) reported a con-
tinuous increase of the percentages of im-
plants exhibiting PPD � 4 mm and
� 6 mm throughout the study. Five-year
estimates were provided only for ITIs
im-
plants. These data imply an increase in the
number of deep peri-implant pockets in the
course of time. Interestingly, approxi-
mately 64% of the patients were smokers.
Long-term studies/patients with a history ofchronic periodontitis (Table 2)
At the completion of a 5-year observation
period (Wennstrom et al. 2004), the mean
peri-implant PPD was 3.1 mm. Eighty per-
cent of peri-implant sites presented
PPD�3 mm, while only 5.3% had a value
of � 6 mm. In a 10-year study, Karoussis
et al. (2003) demonstrated that implants
placed in patients with a history of chronic
periodontitis had statistically significantly
greater proportion of PPD45 mm without
bleeding on probing, as well as of
PPD¼ 5 mm with bleeding on probing,
compared with patients without a history
of periodontitis. Baelum & Ellegaard (2004)
found a continuous increase of the percen-
tages of implants exhibiting PPD � 4 mm
and � 6 mm from one to 5 years and
subsequently from 5 to 10 years. Similar
results were reported by Ellegaard et al.
(2006) for implants placed in patients with
a history of chronic periodontitis, following
a sinus membrane elevation procedure. In
conclusion, these data suggest that PPD
around implants placed in patients with a
history of chronic periodontitis tends to
increase throughout a long-term period.
Moreover, the proportion of deep pockets
seems to be higher in patients with a
history of chronic periodontitis than in
periodontally healthy subjects.
Aggressive periodontitis (Table 3)
Mengel et al. (2001) reported that after the
third year of follow-up in the generalized
aggressive periodontitis group, mean PPD
and clinical attachment loss underwent a
distinct rise around both implants and
teeth. Even though PPD was statistically
significantly lower at the implants than at
the teeth, mean clinical attachment loss
was statistically significantly higher
around the implants (3.62 mm) than
around the teeth (1.61 mm). Similar results
were reported by Mengel & Flores-de-Ja-
coby (2005a). These observations give rise
to the hypothesis that changes in clinical
parameters around teeth and implants in
aggressive periodontitis patients may not
follow the same pattern, in contrast to
what has been previously analyzed (Kar-
oussis et al. 2004) for non-aggressive perio-
dontitis subjects. This hypothesis has to be
tested by further investigations with longer
observation periods.
Mengel & Flores-de-Jacoby (2005b) found
no statistically significant differences in
PPD around implants between generalized
aggressive periodontitis patients (who had
undergone guided bone regeneration before
implantation) and periodontally healthy
controls (without need of guided bone re-
generation). However, clinical attachment
loss in generalized aggressive periodontitis
patients was greater, to a very high statisti-
cally significant degree, than that in perio-
dontally healthy controls. The comparison
between teeth and implants revealed statis-
tically significantly higher PPD and attach-
ment loss at the implants in generalized
aggressive periodontitis patients.
Peri-implant marginal bone loss
Short-term studies/patients with a history ofchronic periodontitis (Table 1)
Ellegaard et al. (1997a) reported that 76.3%
of Astras
implants and 88.5% of ITIs
implants exhibited radiographic bone loss
o1.5 mm after 36 months. All (100%)
Astras
implants and 95.7% of ITIs
im-
plants presented radiographic bone loss
o3.5 mm after 36 months. These short-
term results may be considered acceptable.
However, a decrease of the proportions of
ITIs
implants – which were followed up to
60 months – presenting radiographic bone
loss o1.5 and o3.5 mm was demonstrated
(57% and 81.5%, respectively). In another
study of the same group (Ellegaard et al.
1997b), similar short-term results were
reported for radiographic bone loss
o1.5 mm and o3.5 mm after 36 months
at implants placed conventionally or con-
comitantly with sinus membrane eleva-
tion. Even though a lower percentage of
one-stage implants presenting radiographic
bone loss o1.5 mm was found, no statis-
tically significant difference was reported
either between one-stage and two-stage im-
plants or implants placed with or without
sinus membrane elevation. Nevertheless, no
control group (periodontally healthy sub-
jects) was included in both these studies
(Ellegaard et al. 1997a, 1997b).
Mengel & Flores-de-Jacoby (2005a), fol-
lowing a 3-year observation period, re-
ported that bone loss around implants was
0.86 mm in the generalized chronic perio-
dontitis group and 0.7 mm in periodontally
healthy subjects. This difference was not
statistically significant.
Long-term studies/patients with a history ofchronic periodontitis (Table 2)
Leonhardt et al. (2002) found a mean bone
loss of 1.7 mm around implants; however,
the subtype of periodontitis of enrolled
patients (chronic or aggressive) is not clar-
ified from the presented data. Karoussis
et al. (2003) reported a higher 10-year
mean bone loss around implants placed in
patients with a history of chronic perio-
dontitis than in periodontally healthy in-
dividuals. Wennstrom et al. (2004)
determined that the mean total bone-level
change around implants placed in moder-
ate-to-advanced chronic periodontitis pa-
tients over a 5-year follow-up period was
0.41 mm on all three levels of analysis
(subject level, restoration level, implant
level). 29% of the implants presented
bone loss � 1 mm in 23% of the patients.
Karoussis et al . Dental implant prognosis in periodontally compromised partially edentulous patients
674 | Clin. Oral Impl. Res. 18, 2007 / 669–679 c� 2007 The Authors. Journal compilation c� 2007 Blackwell Munksgaard
15 out of 137 implants, evaluated at 5
years, exhibited bone loss 42 mm. How-
ever, these implants were placed in only
two patients. Baelum & Ellegaard (2004)
found a continuous increase of the percen-
tages of implants exhibiting bone loss
� 1.5 mm and � 3.5 mm throughout
the study. Finally, after 10 years, 31% of
the two-stage and 40% of the one-stage
implants exhibited bone loss � 1.5 mm,
while the corresponding proportions for
bone loss � 3.5 mm were 5% and 14%,
respectively. Similar results were presented
by another study of the same group (Elle-
gaard et al. 2006). Interestingly, a lower
percentage of implants placed in conjunc-
tion with sinus membrane elevation pre-
sented bone loss � 1.5 mm, as well as
� 3.5 mm, compared with conventionally
placed implants, irrespective of the staging
of implantation (one-stage, two-stage).
In conclusion, a number of studies with-
out a control group (Leonhardt et al. 2002;
Baelum & Ellegaard 2004; Wennstrom
et al. 2004; Ellegaard et al. 2006) have
indicated that the long-term mean peri-
implant marginal bone loss for patients
with a history of chronic periodontitis
may be considered comparable to what
has been presented for the general popula-
tion (Naert et al. 1992; Jemt & Lekholm
1993; Lekholm et al. 1994; Buser et al.
1997). On the other hand, the only avail-
able controlled study (Karoussis et al. 2003)
has found a statistically significant differ-
ence in mean peri-implant marginal bone
loss between patients with a history of
chronic periodontitis and periodontally
healthy subjects. Therefore, the effect of
the history of periodontitis on the long-
term mean peri-implant bone loss has not
been clarified as yet and more controlled
long-term studies are required.
Aggressive periodontitis (Table 3)
Mengel et al. (2001) found a statistically
significantly higher bone loss around im-
plants placed in patients treated for aggres-
sive periodontitis than in patients with a
history of chronic periodontitis 3 years
after final abutment insertion. Mengel &
Flores-de-Jacoby (2005a), following a 3-
year observation period, reported that
bone loss around implants was 1.14 mm
in the generalized aggressive periodontitis
group and 0.7 mm in periodontally healthy
subjects. However, this difference did not
reach statistical significance. In another
study of the same group (Mengel &
Flores-de-Jacoby 2005b), the 3-year bone
loss around the implants placed in regener-
ated bone in patients treated for generalized
aggressive periodontitis was 1.78 mm,
while in periodontally healthy subjects it
was 1.4 mm. However, this difference did
not reach statistical significance.
Implant success rates
The definition of success still remains a
matter of debate, as a consensus agreement
on criteria of success has not been achieved
as yet (van Steenberghe et al. 1999). It has
been clearly demonstrated that the use of
different criteria for the definition of success
diversifies the calculated success rates (Kar-
oussis et al. 2003). In this study, success
criteria at 10 years were set at:
PPD�5 mm, no bleeding on probing, bone
loss o0.2 mm annually. With the initial
success criteria set, 52.4% of the implants
placed in patients with a history of chronic
periodontitis (group A) and 79.1% of the
implants placed in periodontally healthy
subjects (group B) were successful. With a
threshold set at PPD�6 mm, no bleeding
on probing and bone loss o0.2 mm an-
nually, the success rates were elevated to
62% and 81.3% for groups A and B, respec-
tively. Relying purely on clinical parameters
of PPD�5 mm and on the absence of bleed-
ing of probing, success rates were 71.4% and
94.5% for groups A and B, respectively; with
a threshold set at PPD�6 mm and on the
absence of bleeding on probing, these propor-
tions were elevated to 81% and 96.7% for
groups A and B, respectively. In conclusion,
setting of thresholds for success criteria is
crucial for determining success rates.
With the strict success criteria set by this
study (Karoussis et al. 2003), implants
placed in patients with a history of chronic
periodontitis presented statistically signifi-
cantly lower success rate than implants
placed in patients without periodontitis,
indicating an influence of the history of
chronic periodontitis on the long-term suc-
cess of implants. A 7-year prospective
study (Brocard et al. 2000), employing
defined success criteria (Buser et al.
1997), reported a cumulative success rate
of 74.7% for ITIs
implants placed in perio-
dontally compromised patients. This result
is in agreement with the findings of Kar-
oussis et al. (2003), as Brocard et al. (2000)
did not include the radiographically mea-
sured bone loss into their definition of
success. Their result corresponds to the
clinical success of 71.4% reported by Kar-
oussis et al. for implants placed in patients
with a history of chronic periodontitis.
Furthermore, the aforementioned success
rate (74.7%) was statistically significantly
lower than the cumulative success rate for
all 1022 implants included in the study by
Brocard et al. (2000).
Occurrence/incidence of peri-implantitis
Brocard et al. (2000) reported an overall
failure due to peri-implant infection of
4.8% in the entire study population. The
authors considered this proportion to be
high, attributing it to the relatively high
percentage of periodontally maintained pa-
tients (33.4%). However, no data were
provided regarding the incidence of peri-
implantitis in periodontally compromised
patients, as well as the proportion of cases
of peri-implantitis not leading to implant
failure. Karoussis et al. (2003) found a
statistically significantly higher incidence
of peri-implantitis for implants placed
in patients with a history of chronic
periodontitis (28.6%) compared with perio-
dontally healthy subjects (5.8%).
In conclusion, it appears that the history
of chronic periodontitis may predispose to
the development of peri-implantitis. How-
ever, the body of evidence supporting this
conclusion is limited. Therefore, it seems
reasonable to suggest that future studies
should provide data for the incidence of
peri-implantitis developed both in perio-
dontally compromised patients and in
periodontally healthy individuals.
Implant surface
Rosenberg et al. (2004) reported that the
exclusion of hydroxyapatite-coated im-
plants from the overall number of implants
evaluated in their study increased the im-
plant survival rates, both for periodontally
compromised patients (from 81% to
90.6%) and for periodontally healthy sub-
jects (from 92.6% to 93.7%). Wennstrom et
al. (2004) found no statistically significant
differences in peri-implant bone loss be-
tween machined and rough surface designs.
Smoking
Karoussis et al. (2003) reported separate
results for smokers and non-smokers,
Karoussis et al . Dental implant prognosis in periodontally compromised partially edentulous patients
c� 2007 The Authors. Journal compilation c� 2007 Blackwell Munksgaard 675 | Clin. Oral Impl. Res. 18, 2007 / 669–679
both for patients with and without a his-
tory of chronic periodontitis. However,
owing to the limited number of subjects
followed over 10 years, the differences in
survival, incidence rates of peri-implantitis
or success rates between smokers and non-
smokers in both groups of patients, with
and without a history of chronic perio-
dontitis, did not reach statistical signifi-
cance. Nevertheless, there was a trend for a
lower survival rate of implants in smokers
vs. non-smokers (80% vs. 100%) in pa-
tients with a history of chronic perio-
dontitis. This finding indicates that
smokers susceptible to chronic perio-
dontitis yield a higher risk for implant
loss than non-smoking periodontal patients
or individuals without a history of perio-
dontitis at all.
Moreover, following a 5-year follow-up
period, Wennstrom et al. (2004) reported
that smokers exhibited statistically signifi-
cantly higher mean peri-implant marginal
bone loss than non-smokers (0.76 mm vs.
0.22 mm, respectively).
Baelum & Ellegaard (2004) reported that
implants were explanted in periodontally
compromised smokers at a 2.6 times
higher rate than in periodontally compro-
mised non-smokers. Periodontally com-
promised smokers were 1.9, 2.4 and 1.8
times more likely to exhibit a first occur-
rence of peri-implant PPD � 4 mm, peri-
implant PPD � 6 mm and bleeding on
probing, respectively, as compared with
periodontally compromised non-smokers.
Ellegaard et al. (2006) found that smoking,
although not statistically significantly, in-
creased the risk of explantation (hazard
ratio: 2.2) in periodontally compromised
patients (with or without sinus membrane
elevation).
Methodological discrepancies and/orshortcomings of selected studies
(1) Certain studies included a control
group (Karoussis et al. 2003; Rosen-
berg et al. 2004; Mengel & Flores-de-
Jacoby 2005a, 2005b), comprising
periodontally healthy individuals,
whereas other studies included only
periodontally compromised patients
(Ericsson et al. 1986; Ellegaard et al.
1997a, 1997b, 2006; Buchmann et al.
1999; Sbordone et al. 1999; Mengel
et al. 2001; Leonhardt et al. 2002;
Baelum & Ellegaard 2004; Wenn-
strom et al. 2004). In a particular
case (Brocard et al. 2000), the entire
population of the study was used as
the control to be compared with the
subgroup of periodontally compro-
mised patients.
(2) Certain studies included a relatively
limited number of patients (Ericsson
et al. 1986; Mengel et al. 2001; Leon-
hardt et al. 2002; Karoussis et al.
2003; Mengel & Flores-de-Jacoby
2005b), while other studies evaluated
larger sample sizes (Brocard et al.
2000; Baelum & Ellegaard 2004; Ro-
senberg et al. 2004; Wennstrom et al.
2004; Ellegaard et al. 2006).
(3) A number of studies included smokers
(Ellegaard et al. 1997a, 1997b, 2006;
Brocard et al. 2000; Karoussis et al.
2003; Baelum & Ellegaard 2004; Wenn-
strom et al. 2004), while elsewhere
smokers were excluded (Mengel &
Flores-de-Jacoby 2005a). Of the studies
including smokers, only one (Karoussis
et al. 2003) presented all evaluated
parameters separately for smokers and
non-smokers, both in patients with a
history of chronic periodontitis and in
periodontally healthy subjects.
(4) Implant ‘success’ was defined in some
cases (Brocard et al. 2000; Karoussis et
al. 2003), and not defined in others
(Mengel et al. 2001).
(5) In certain cases, sinus membrane ele-
vation (Ellegaard et al. 1997b, 2006;
Buchmann et al. 1999) and guided
bone regeneration procedures (Mengel
& Flores-de-Jacoby 2005b) were em-
ployed.
Conclusions
From the present comprehensive and criti-
cal review the following conclusions may
be drawn:
General conclusions
� As considerable discrepancies existed
among the selected studies, more pro-
spective controlled studies, uniformly
designed, are required.
� A universally accepted definition of
‘periodontally compromised’ patients
is not currently available. There is a
definite need for this definition in order
to facilitate the comparison of the re-
sults of future studies.
� For the same reason, consensus criteria
of implant success certainly have to be
established in the future.
Conclusions from short-term studies onchronic periodontitis
� The majority of studies tend to indicate
that short-term implant survival rates
in partially edentulous patients with a
history of chronic periodontitis are
comparable to those reported for perio-
dontally healthy individuals. It should
be emphasized that in these studies an
uninterrupted strict individualized
maintenance care programme was ap-
plied following implant placement.
� A stability of PPD and CAL (clinical
parameters) and peri-implant marginal
bone loss (radiographic parameter)
around implants has been demonstrated
on a short-term basis.
Conclusions from long-term studies onchronic periodontitis
� Long-term survival rates of implants
placed in partially edentulous patients
with a history of chronic periodontitis
may exceed 90%, being comparable to
the mean implant survival rates re-
ported for the general population.
� PPD around implants placed in patients
with a history of chronic periodontitis
tends to increase throughout a long-
term period and the proportion of
deep pockets seems to be higher in
patients with a history of chronic perio-
dontitis than in periodontally healthy
subjects.
� A significant difference in mean peri-
implant marginal bone loss between
patients with a history of chronic perio-
dontitis and periodontally healthy sub-
jects may be expected. However, there
is only one controlled prospective study
available to support this conclusion.
Therefore, the impact of the history of
chronic periodontitis on the long-term
mean peri-implant bone loss still re-
mains unclarified and more controlled
long-term studies have to be conducted.
� Although surviving, implants placed in
patients with a history of chronic perio-
Karoussis et al . Dental implant prognosis in periodontally compromised partially edentulous patients
676 | Clin. Oral Impl. Res. 18, 2007 / 669–679 c� 2007 The Authors. Journal compilation c� 2007 Blackwell Munksgaard
dontitis may demonstrate a higher in-
cidence of peri-implantitis than im-
plants placed in patients without a
history of periodontitis.
� The evaluation of the potential impact
of various parameters on the prognosis
of implants placed in patients with a
history of chronic periodontitis may
lead to the following conclusions:
Smoking may exert a negative influence
on peri-implant PPD, marginal bone loss
and implant survival.
From the limited available data, it ap-
pears that patients with a history of chronic
periodontitis may be considered as candi-
dates for dental implant treatment includ-
ing sinus membrane elevation or guided
bone regeneration procedures.
� Implant surface (rough or smooth) does
not appear to have an impact on im-
plant prognosis.
Conclusions from studies on aggressiveperiodontitis
� The short-term implant survival rates
for patients treated for aggressive perio-
dontitis may exceed 95%, reaching up
to 100%. However, the long-term sur-
vival of implants in patients treated for
aggressive periodontitis still remains
questionable, due to the limited avail-
able data.
� No statistically significant differences
in peri-implant PPD between patients
treated for generalized aggressive perio-
dontitis and periodontally healthy con-
trols have been found. However,
clinical attachment loss appears to be
significantly greater in aggressive perio-
dontitis patients.
� On a short-term basis, no statistically
significant differences in peri-implant
marginal bone loss may be detected
between patients treated for aggressive
periodontitis and periodontally healthy
subjects. Nevertheless, on a long-term
basis this matter is open to question.
� Alterations in clinical parameters
around teeth and implants in aggressive
periodontitis patients may not follow
the same pattern, in contrast to what
has been reported for non-aggressive
periodontitis subjects. This hypothesis
has to be tested by further investiga-
tions on a long-term basis.
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