11
Review A comprehensive and critical review of dental implant prognosis in periodontally compromised partially edentulous patients Ioannis K. Karoussis Sotirios Kotsovilis Ioannis Fourmousis Authors’ affiliations: Ioannis K. Karoussis, Sotirios Kotsovilis, Ioannis Fourmousis, Department of Periodontology, School of Dental Medicine, University of Athens, Athens, Greece Correspondence to: Dr Ioannis K. Karoussis Department of Periodontology School of Dental Medicine University of Athens Thivon Street 2 GR 11527 Athens Greece Tel.: þ 30 210 7461203 Fax: þ 30 210 7461202 e-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 (Bra ˚ne- 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. A comprehensive and critical review of dental implant prognosis in periodontally compromised partially edentulous patients. Clin. Oral Impl. Res. 18, 2007; 669–679 doi: 10.1111/j.1600-0501.2007.01406.x c 2007 The Authors. Journal compilation c 2007 Blackwell Munksgaard 669

A Comprehensive and Critical Review of Dental Implant Prognosis in Periodontally Compromised Partially Edentulous Patients

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Page 1: A Comprehensive and Critical Review of Dental Implant Prognosis in Periodontally Compromised Partially Edentulous Patients

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

Page 2: A Comprehensive and Critical Review of Dental Implant Prognosis in Periodontally Compromised Partially Edentulous Patients

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

Page 3: A Comprehensive and Critical Review of Dental Implant Prognosis in Periodontally Compromised Partially Edentulous Patients

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

Page 4: A Comprehensive and Critical Review of Dental Implant Prognosis in Periodontally Compromised Partially Edentulous Patients

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

Page 5: A Comprehensive and Critical Review of Dental Implant Prognosis in Periodontally Compromised Partially Edentulous Patients

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

Page 6: A Comprehensive and Critical Review of Dental Implant Prognosis in Periodontally Compromised Partially Edentulous Patients

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

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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

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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

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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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