Review

Ioannis K. Karoussis Sotirios Kotsovilis Ioannis Fourmousis

A comprehensive and critical review of dental implant prognosis in periodontally compromised partially edentulous patients

Authors afliations: 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.: 30 210 7461203 Fax: 30 210 7461202 e-mail: ikaroussis@dent.uoa.gr

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 claried. 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 rst 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 rst 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 signicant 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 signicantly greater long-term probing pocket depth, peri-implant marginal bone loss and incidence of periimplantitis 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.

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; 669679 doi: 10.1111/j.1600-0501.2007.01406.x

Dental implant placement is an effective and predictable treatment modality for reneplacing missing teeth in both fully (Bra 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.

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2004) have provided the highest level of evidence supporting the favourable longterm prognosis of implant therapy in the general population. However, fewer data seem to be available concerning the prognosis 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; Leonhardt et al. 1992, 1993; Mombelli et al. 1995; Papaioannou et al. 1995, 1996; Gouvoussis et al. 1997; Sbordone et al. 1999; De Boever & De Boever 2006; Quirynen et al. 2006). A comprehensive review (Heydenrijk et al. 2002) of the studies published up to and including December 2000, concerning the microora around implants, has drawn the following conclusions: The microbiota of the oral cavity before implant placement determines the composition of the peri-implant microora; the microora of peri-implantitis lesions resembles that of chronic periodontitis. The similarity in microbial ora responsible for periodontitis and peri-implantitis supports the concept that periodontal pathogens may be associated with periimplant infections and failing implants (Mombelli et al. 1987; Mombelli & Lang 1992). An association between periodontal and peri-implant conditions has been demonstrated (Bra gger 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 increased susceptibility for periodontitis might also imply an increased susceptibility for peri-implantitis. The importance of periodontal therapy before implant placement in partially edentulous patients has been emphasized (Bra gger 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 present 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; Heydenrijk et al. 2002). Moreover, the presence of putative periodontopathogens at peri-implant and periodontal sites might not be associated with future attachment loss, as reported for both teeth and implants (Offenbacher 1996; Sbordone et al. 1999; Nevins 2001). Periodontopathogens may be randomly detected at both stable and deteriorating 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; Wilson & Nunn 1999; Michalowicz et al. 2000; Feloutzis et al. 2003; Gruica et al. 2004) and susceptible subjects are considered 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 favourable 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 literature 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.

Data sources also included the reference lists of identied publications and several hand-searched journals (British Journal of Oral and Maxillofacial Surgery, British Journal of Oral Surgery, Clinical Oral Implants Research, Implant Dentistry, International Journal of Oral & Maxillofacial Implants, International Journal of Oral and Maxillofacial Surgery, International Journal of Periodontics Restorative Dentistry, International Journal of Prosthodontics, Journal of Clinical Periodontology, Journal of Maxillofacial Surgery, 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 rst 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 dened inclusion criteria. The inclusion criteria were as follows: (1) (2) (3) (4) Publications written only in the English language Clinical studies only Prospective design Placement of osseointegrated dental implants 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 published 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 Periimplantn) AND (Periodontn)

If both periodontally compromised patients and periodontally healthy individuals were enrolled in a study, separate data should have been reported for each of these two distinct categories of participants; 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 before implant placement and absence of active inammation at the recipient site at the time of implantation clearly dened Follow-up period of more than 1 year Report of data revealing implant survival (or success) rate in periodontally compromised partially edentulous patients

(6) (7)

At the second phase of selection, the full text of all selected studies was obtained.

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Table 1. The selected short-term (o5 years) studies in partially edentulous patients with a history of chronic periodontitis
Authors (publication date) Ericsson et al. (1986) Groups/ implants (N ) 10 PC, 41 s nemark Bra impls Follow-up ISR MPBL Comments

Mean: 18 months, 100% range: 630 months

Most cases: o1 mm 3 impls: 41 mm (up to 3 mm)

Ellegaard 19 PC, 31 Astra et al. (1997a) impls, 56 PC, 93 s ITI impls

At 36 months: 76.3% of s Astra impls and 88.5% s of osseointegrated ITI impls had MPBLo1.5 mm At 60 months: 57% of s osseointegrated ITI impls had MPBLo1.5 mm s s s Ellegaard 24 PC, 25 Astra , Astra impls: mean Astra : 100%, At 36 months: 76.2%, No control group (no PH) s s s et al. (1997b) 26 Astra sinus, 30.8 months, Astra Astra sinus: 95%, 82.3%, 70.7% and 29.2% 15 patients were smokers s s s s s of Astra , Astra sinus, Sinus membrane elevation 17 ITI , 12 ITI sinus impls: mean ITI : s s s s was included 29.9 months, ITI 90.9%, ITI sinus: ITI , ITI sinus 85.7% impls: mean 29.4 sinus impls, resp., had s months, ITI sinus MPBLo1.5 mm impls: mean 25.3 months Sbordone 25 PC, 42 3 years 100% Not reported No control group (no PH) s nemark impls et al. (1999) Bra No implant losses were reported s nemark , Buchmann 50 PC, 36 Bra 3 years 100% (167/167) Not reported No control group (no PH) s s et al. (1999) 88 Frialit-2 , 43 IMZ Sinus membrane elevation impls was performed s nemark Mengel 5 PC, 12 Bra 3 years 100% 0.19 mm No control group (no PH) et al. (2001) impls Limited number of patients Only patients with generalized chronic periodontitis are included in this table; data for generalized aggressive periodontitis are presented in Table 3 12 PC, 43 impls, 12 PH, 30 3 years PC: 100%, PC: 0.86 mm, Only patients with generalized Mengel & impls (MK II & Osseotite) PH: 100% PH: 0.7 mm chronic periodontitis are Flores-deincluded in this table; patients Jacoby with generalized aggressive (2005a) periodontitis are included in Table 3 Smokers 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.

Astra impls: mean Maxilla: 97.3%, 30 7.4 months, mandible: 92.3% s ITI impls: mean 33.3 21.8 months

No control group (no PH) Limited number of patients Relatively short follow-up period Combination of implants and teeth as abutments for xed bridges No control group (no PH) 64% of the patients were smokers

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 relevant titles and abstracts. Following the rst 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. These included seven short-term (Ericsson et al. 1986; Ellegaard et al. 1997a, 1997b; Buchmann et al. 1999; Sbordone et al. 1999; Mengel & Floresde-Jacoby 2005a, 2005b) and eight longterm studies (Brocard et al. 2000; Mengel et al. 2001; Leonhardt et al. 2002; Karoussis et al. 2003; Baelum & Ellegaard 2004; Rosenberg et al. 2004; Wennstro m 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) reported short-term data for chronic periodontitis patients (Table 1), six studies (Brocard et al. 2000; Karoussis et al. 2003; Baelum & Ellegaard 2004; Rosenberg et al. 2004; Wennstro m 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 patients (Table 3) and one study (Mengel et al. 2001) reported long-term data for aggressive periodontitis patients (Table 3). A long-term study (Mengel et al. 2001) re-

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Table 2. The selected long-term ( 5 years) studies in partially edentulous patients with a history of chronic periodontitis
Authors (publication date) Brocard et al. (2000) Groups/implants (N) Follow-up ISR MPBL Comments

147 PC, 375 ITI impls

7 years

Leonhardt et al. (2002)

nemark 15 PC, 57 Bra impls

10 years

74.7% (success, according to Buser et al. 1997) Global success: 83.4% 94.74%

Not mentioned

Smokers were included Global success rate refers to the entire study population

Karoussis et al. (2003)

8 PC, 21 impls, 45 PH, 91 impls

10 years

m Wennstro et al. (2004) Rosenberg et al. (2004) Baelum & Ellegaard (2004)

51 PC, 149 Astra s Tech impls 151 PC, 923 impls, 183 PH, 588 impls (8 impl systems) 140 PC, 258 impls s (201 one-stage ITI impls in 108 PC and s 57 two-stage Astra impls in 32 PC)

5 years

PC total: 90.5%, PH total: 96.5%, PC smokers: 80%, PH smokers: 100%, PC non-smokers: 100%, PH non-smokers: 95.7% 97.32%

1.7 1.2 mm (or 1.7 1.1 mm) Inconsistency of data between the text and Table 1 of the study PC: mesial 1 1.38 mm, distal 0.94 0.73 mm, PH: mesial 0.48 1.1 mm, distal 0.5 1.08 mm 0.41 1.01 mm (mean on impl level) Not reported

Subtype of periodontitis (chronic or aggressive) was not clearly dened No control group (no PH)

Limited number of PC Smokers were included in the study, but separate results were provided for smokers and non-smokers

13 years

PC: 90.6%, PH: 93.7% At 5 years: one-stage 94.3%, two-stage 97.4% At 10 years: onestage 77.7%, twostage 97.4%

Duration: 14 years follow-up (mean/ range): one-stage impls: 73.6 months/ 0168 months, twostage impls: 68.2 months/0128 months Follow-up (mean/ s range): Astra impls: 67.7 months/0128 s months, Astra sinus impls: 64.2 months/ s 0128 months, ITI impls: 61 months/0 s 147 months, ITI sinus impls: 57.5 months/0143 months

Ellegaard et al. (2006)

68 PC, 50 Astra conventional impls, s 59 Astra sinus s impls, 81 ITI conventional impls, s 72 ITI sinus impls

10-year estimates: s Astra impls: 97%, s Astra sinus impls: s 85.4%, ITI impls: s 59%, ITI sinus impls: 79.9%

MPBL: not reported At 10 years bone loss  1.5 mm: onestage impls 40%, two-stage 31% Bone loss  3.5 mm: onestage 14%, twostage 5% MPBL: not reported At 10 years bone loss s  3.5 mm: Astra s impls 5.9%, Astra sinus impls 4.8%, s s ITI impls 12.2%, ITI sinus impls 1.8%

No control group (no PH) 17 of the patients (one-third) were current smokers Survival was dened according to Albrektsson et al. (1986) No control group (no PH) About 65% of the patients were smokers

No control group (no PH) Sinus membrane elevation without grafting was included s 57% (for Astra ) and 68% (for s ITI ) of the patients were smokers

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).

ported short-term (3 years) data for generalized 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 2171 years at implant surgery, had been affected with advanced periodontitis. However, the subtype of periodontitis (chronic or aggressive) was not clearly dened 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 effectiveness and predictability of dental implant therapy in partially edentulous periodontally 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 Weijden 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 studies and concluded that there were limited data available by that time. A recent publication (Schou et al. 2006) assessed studies up to and including December 2005 and nally selected two studies (Hardt et al. 2002; Karoussis et al. 2003), already included 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,

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Table 3. The selected short-term (o5 years) and long-term ( 5 years) studies in partially edentulous patients treated for generalized aggressive periodontitis
Authors (publication date) Mengel et al. (2001) Groups/implants (N) Follow-up ISR MPBL Comments

5 PC, 36 s nemark impls Bra

5 years (long term)

88.8% (reported 0.88 mm as success in the study)

Mengel & Flores-deJacoby (2005a) Mengel & Flores-deJacoby (2005b)

15 PC, 77 impls, 12 PH, 30 impls (MK II & Osseotite) 10 PC, 15 impls, 10 PH, 11 impls (MK II & Nobel Biocare)

3 years (short term)

3 years (short term)

PC: 95.7% in the maxilla, 100% in the mandible, PH: 100% PC: 100%, PH: 100%

PC (mean, total): 1.14 mm, PH: 0.7 mm PC: 1.78 mm, PH: 1.31 or 1.4 mm

No control group (no PH) Limited number of patients Only patients with generalized aggressive periodontitis are reported in this table; data for generalized chronic periodontitis are included in Table 1 Patients with generalized aggressive periodontitis are included in this table; patients with generalized chronic periodontitis are included in Table 1 Smokers were excluded GBR was performed in all PC Inconsistency of data reporting on MPBL between the 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.

a distinct evaluation between data on implant 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 reporting mixed data, on both totally and partially edentulous patients, were excluded.

dened the periodontal status of the patients at the time of implant placement.
Implant survival rates Short-term studies/patients with a history of chronic periodontitis (Table 1)

Denition of periodontally compromised patients

The necessity for a denition of periodontally compromised patients has been particularly emphasized (van der Weijden et al. 2005). A consensus denition 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 & Floresde-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 surgical) 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 denition for successful periodontal therapy; the selected studies have not clearly

The selected short-term studies have reported 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 of chronic periodontitis (Table 2)

slightly worse than solid implants (Buser et al. 1997). In conclusion, the long-term survival rates of implants placed in partially edentulous patients with a history of chronic periodontitis are comparable to the mean implant survival rates reported for the general population (Berglundh et al. 2002; Lang et al. 2004; Pjetursson et al. 2004).
Aggressive periodontitis (Table 3)

The majority of the selected long-term studies have reported implant survival rates in patients with a history of chronic periodontitis well above 90% (Leonhardt et al. 2002; Karoussis et al. 2003; Rosenberg et al. 2004; Wennstro m et al. 2004), reaching up to 97.32% (Wennstro m 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 implants, many of which had a short length (dened by the authors as length  10 mm). These lower survival rates were attributed by the authors to the decision to remove surgically hollow implants, when peri-implantitis had occurred, as treatment of peri-implantitis in this type of implants was considered virtually impossible. Furthermore, it has been reported that hollow implants tend to perform

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 longterm study (Mengel et al. 2001) reported a 5-year implant survival rate of 88.8%. Therefore, the long-term survival of implants in patients treated for aggressive periodontitis still remains open to question and more studies are required.
Probing pocket depth (PPD) and clinical attachment level (CAL) Short-term studies/patients with a history of chronic periodontitis (Table 1)

Sbordone et al. (1999) reported no statistically signicant 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 signicant differences in clinical parameters were found between implants and the selected control teeth. However, 10% of the implant sites had a mean clinical attachment

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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 rst 3 years, a continuous clinical attachment loss was recorded only around implants. This intriguing nding was attributed to peri-implant soft tissue recession. Furthermore, in the rst study (Mengel et al. 2001) no differences in PPD and CAL between implants and teeth were found. However, in the second study (Mengel & Flores-deJacoby 2005a) clinical attachment loss was statistically signicantly higher at the implants than at the teeth. Nevertheless, it is clear that, on a long-term observation 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 signicant differences in clinical parameters among periodontally compromised patients with chronic periodontitis and periodontally healthy controls. Ellegaard et al. (1997a) reported a continuous increase of the percentages of implants exhibiting PPD  4 mm and  6 mm throughout the study. Five-year s estimates were provided only for ITI implants. These data imply an increase in the number of deep peri-implant pockets in the course of time. Interestingly, approximately 64% of the patients were smokers.
Long-term studies/patients with a history of chronic periodontitis (Table 2)

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)

At the completion of a 5-year observation period (Wennstro m et al. 2004), the mean peri-implant PPD was 3.1 mm. Eighty percent 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 signicantly greater proportion of PPD45 mm without bleeding on probing, as well as of PPD 5 mm with bleeding on probing, compared with patients without a history of periodontitis. Baelum & Ellegaard (2004) found a continuous increase of the percentages of implants exhibiting PPD  4 mm and  6 mm from one to 5 years and

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 signicantly lower at the implants than at the teeth, mean clinical attachment loss was statistically signicantly higher around the implants (3.62 mm) than around the teeth (1.61 mm). Similar results were reported by Mengel & Flores-de-Jacoby (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 (Karoussis et al. 2004) for non-aggressive periodontitis subjects. This hypothesis has to be tested by further investigations with longer observation periods. Mengel & Flores-de-Jacoby (2005b) found no statistically signicant 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 regeneration). However, clinical attachment loss in generalized aggressive periodontitis patients was greater, to a very high statistically signicant degree, than that in periodontally healthy controls. The comparison between teeth and implants revealed statistically signicantly higher PPD and attachment loss at the implants in generalized aggressive periodontitis patients.
Peri-implant marginal bone loss Short-term studies/patients with a history of chronic periodontitis (Table 1)

Ellegaard et al. (1997a) reported that 76.3% s s of Astra implants and 88.5% of ITI implants exhibited radiographic bone loss o1.5 mm after 36 months. All (100%) s s Astra implants and 95.7% of ITI implants presented radiographic bone loss o3.5 mm after 36 months. These shortterm results may be considered acceptable. However, a decrease of the proportions of s ITI 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 concomitantly with sinus membrane elevation. Even though a lower percentage of one-stage implants presenting radiographic bone loss o1.5 mm was found, no statistically signicant difference was reported either between one-stage and two-stage implants or implants placed with or without sinus membrane elevation. Nevertheless, no control group (periodontally healthy subjects) was included in both these studies (Ellegaard et al. 1997a, 1997b). Mengel & Flores-de-Jacoby (2005a), following a 3-year observation period, reported that bone loss around implants was 0.86 mm in the generalized chronic periodontitis group and 0.7 mm in periodontally healthy subjects. This difference was not statistically signicant.
Long-term studies/patients with a history of chronic 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 claried 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 periodontitis than in periodontally healthy individuals. Wennstro m et al. (2004) determined that the mean total bone-level change around implants placed in moderate-to-advanced chronic periodontitis patients 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.

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15 out of 137 implants, evaluated at 5 years, exhibited bone loss 42 mm. However, these implants were placed in only two patients. Baelum & Ellegaard (2004) found a continuous increase of the percentages 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 (Ellegaard et al. 2006). Interestingly, a lower percentage of implants placed in conjunction with sinus membrane elevation presented 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 without a control group (Leonhardt et al. 2002; Baelum & Ellegaard 2004; Wennstro m et al. 2004; Ellegaard et al. 2006) have indicated that the long-term mean periimplant marginal bone loss for patients with a history of chronic periodontitis may be considered comparable to what has been presented for the general population (Naert et al. 1992; Jemt & Lekholm 1993; Lekholm et al. 1994; Buser et al. 1997). On the other hand, the only available controlled study (Karoussis et al. 2003) has found a statistically signicant difference 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 longterm mean peri-implant bone loss has not been claried as yet and more controlled long-term studies are required.
Aggressive periodontitis (Table 3)

reach statistical signicance. In another study of the same group (Mengel & Flores-de-Jacoby 2005b), the 3-year bone loss around the implants placed in regenerated 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 signicance.
Implant success rates

did not include the radiographically measured bone loss into their denition of success. Their result corresponds to the clinical success of 71.4% reported by Karoussis et al. for implants placed in patients with a history of chronic periodontitis. Furthermore, the aforementioned success rate (74.7%) was statistically signicantly lower than the cumulative success rate for all 1022 implants included in the study by Brocard et al. (2000).
Occurrence/incidence of peri-implantitis

Mengel et al. (2001) found a statistically signicantly higher bone loss around implants placed in patients treated for aggressive periodontitis than in patients with a history of chronic periodontitis 3 years after nal abutment insertion. Mengel & Flores-de-Jacoby (2005a), following a 3year 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

The denition 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 denition of success diversies the calculated success rates (Karoussis 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 annually, the success rates were elevated to 62% and 81.3% for groups A and B, respectively. Relying purely on clinical parameters of PPD  5 mm and on the absence of bleeding 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 proportions 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 signicantly lower success rate than implants placed in patients without periodontitis, indicating an inuence of the history of chronic periodontitis on the long-term success of implants. A 7-year prospective study (Brocard et al. 2000), employing dened success criteria (Buser et al. 1997), reported a cumulative success rate s of 74.7% for ITI implants placed in periodontally compromised patients. This result is in agreement with the ndings of Karoussis et al. (2003), as Brocard et al. (2000)

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 patients (33.4%). However, no data were provided regarding the incidence of periimplantitis 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 signicantly higher incidence of peri-implantitis for implants placed in patients with a history of chronic periodontitis (28.6%) compared with periodontally healthy subjects (5.8%). In conclusion, it appears that the history of chronic periodontitis may predispose to the development of peri-implantitis. However, 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 periodontally compromised patients and in periodontally healthy individuals.
Implant surface

Rosenberg et al. (2004) reported that the exclusion of hydroxyapatite-coated implants from the overall number of implants evaluated in their study increased the implant survival rates, both for periodontally compromised patients (from 81% to 90.6%) and for periodontally healthy subjects (from 92.6% to 93.7%). Wennstro m et al. (2004) found no statistically signicant differences in peri-implant bone loss between machined and rough surface designs.
Smoking

Karoussis et al. (2003) reported separate results for smokers and non-smokers,

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Karoussis et al . Dental implant prognosis in periodontally compromised partially edentulous patients

both for patients with and without a history 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 nonsmokers in both groups of patients, with and without a history of chronic periodontitis, did not reach statistical signicance. Nevertheless, there was a trend for a lower survival rate of implants in smokers vs. non-smokers (80% vs. 100%) in patients with a history of chronic periodontitis. This nding indicates that smokers susceptible to chronic periodontitis yield a higher risk for implant loss than non-smoking periodontal patients or individuals without a history of periodontitis at all. Moreover, following a 5-year follow-up period, Wennstro m et al. (2004) reported that smokers exhibited statistically signicantly 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 compromised non-smokers. Periodontally compromised smokers were 1.9, 2.4 and 1.8 times more likely to exhibit a rst occurrence of peri-implant PPD  4 mm, periimplant 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 signicantly, increased the risk of explantation (hazard ratio: 2.2) in periodontally compromised patients (with or without sinus membrane elevation).

(2)

(3)

(4)

(5)

Baelum & Ellegaard 2004; Wennstro m 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 compromised patients. Certain studies included a relatively limited number of patients (Ericsson et al. 1986; Mengel et al. 2001; Leonhardt 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; Rosenberg et al. 2004; Wennstro m et al. 2004; Ellegaard et al. 2006). A number of studies included smokers (Ellegaard et al. 1997a, 1997b, 2006; Brocard et al. 2000; Karoussis et al. 2003; Baelum & Ellegaard 2004; Wennstro m 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. Implant success was dened in some cases (Brocard et al. 2000; Karoussis et al. 2003), and not dened in others (Mengel et al. 2001). In certain cases, sinus membrane elevation (Ellegaard et al. 1997b, 2006; Buchmann et al. 1999) and guided bone regeneration procedures (Mengel & Flores-de-Jacoby 2005b) were employed.

denite need for this denition in order to facilitate the comparison of the results 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 on chronic 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 periodontally healthy individuals. It should be emphasized that in these studies an uninterrupted strict individualized maintenance care programme was applied 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 on chronic periodontitis

Conclusions
Methodological discrepancies shortcomings of selected studies and/or

(1)

Certain studies included a control group (Karoussis et al. 2003; Rosenberg et al. 2004; Mengel & Flores-deJacoby 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;
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From the present comprehensive and critical review the following conclusions may be drawn:
General conclusions

 As considerable discrepancies existed among the selected studies, more prospective controlled studies, uniformly designed, are required.  A universally accepted denition of periodontally compromised patients is not currently available. There is a

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 reported for the general population. PPD around implants placed in patients with a history of chronic periodontitis tends to increase throughout a longterm period and the proportion of deep pockets seems to be higher in patients with a history of chronic periodontitis than in periodontally healthy subjects. A signicant difference in mean periimplant marginal bone loss between patients with a history of chronic periodontitis and periodontally healthy subjects 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 remains unclaried and more controlled long-term studies have to be conducted. Although surviving, implants placed in patients with a history of chronic perio-

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Karoussis et al . Dental implant prognosis in periodontally compromised partially edentulous patients

dontitis may demonstrate a higher incidence of peri-implantitis than implants 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:

 Implant surface (rough or smooth) does not appear to have an impact on implant prognosis. 
Conclusions from studies on aggressive periodontitis

Smoking may exert a negative inuence on peri-implant PPD, marginal bone loss and implant survival. From the limited available data, it appears that patients with a history of chronic periodontitis may be considered as candidates for dental implant treatment including sinus membrane elevation or guided bone regeneration procedures.

 The short-term implant survival rates for patients treated for aggressive periodontitis may exceed 95%, reaching up to 100%. However, the long-term survival of implants in patients treated for aggressive periodontitis still remains questionable, due to the limited available data.  No statistically signicant differences in peri-implant PPD between patients treated for generalized aggressive periodontitis and periodontally healthy con-

trols have been found. However, clinical attachment loss appears to be signicantly greater in aggressive periodontitis patients. On a short-term basis, no statistically signicant 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 investigations on a long-term basis.

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