J Periodontol • February 2015
Review Long-Term Evaluation of Periodontal Parameters and Implant Outcomes in Periodontally Compromised Patients: A Systematic Review Mariana Schutzer Zangrando,* Carla Andreotti Damante,* Adriana Campos Sant’Ana,* Maria Lu´cia Rubo de Rezende,* Sebastia ˜o Luiz Greghi,* and Leandro Chambrone†
Background: The aim of this systematic review is to evaluate the long-term outcomes of patients with periodontitis submitted to periodontal therapy/maintenance and implant placement. Methods: Studies reporting clinical and/or long-term implant outcomes from partially edentulous patients with periodontitis who were treated and followed periodontal maintenance for ‡5 years were considered eligible for the review. Screening of the articles, data extraction, and quality assessment were conducted independently and in duplicate. Results: Search of MEDLINE, EMBASE, and CENTRAL databases resulted in 959 papers, and of them 931 were excluded after title/abstract assessment. The full texts of 28 potentially eligible publications were screened, but only 10 studies met inclusion criteria. Most of the included studies (77.8%) presented a medium/high methodologic quality. The results demonstrated that patients with a diagnosis of periodontitis had satisfactory implant outcomes. Implant survival was high (92.1%) within studies reporting 10 years of follow-up. Parameters related to probing depth, clinical attachment level, and bone loss around teeth increased the occurrence of peri-implantitis and implant loss. Non-attendance to periodontal maintenance and smoking habits were also associated with less favorable implant outcomes. Conclusions: This systematic review confirmed that implant therapy can be successfully used in patients with a diagnosis of periodontitis who underwent proper therapy and regular periodontal maintenance. Residual pockets, nonattendance to the periodontal maintenance program, and smoking were considered to be negative factors for the long-term implant outcomes. J Periodontol 2015;86:201-221. KEY WORDS Dental implants; osseointegration; peri-implantitis; periodontitis; systematic review. * Division of Periodontics, Department of Prosthodontics, School of Dentistry at Bauru (Faculty of Odontology of Bauru), University of Sa˜o Paulo, Bauru, Sa˜o Paulo, Brazil. † Unit of Basic Oral Investigation, Faculty of Dentistry, El Bosque University, Bogota´, Colombia.
B
ecause an increasing number of patients receive implants to replace missing teeth lost as a result of periodontitis, the question arises as to whether a history of periodontitis may increase the risk of peri-implant disease (e.g., mucositis and peri-implantitis) and implant loss. The term ‘‘implant survival’’ refers to the presence of an implant with or without complications, and ‘‘implant success’’ refers to the presence of an implant in the absence of complications of either a biologic or technical nature.1 Some review papers clearly indicated that partially and completely edentulous patients can be rehabilitated predictably by oral implants with high implant survival rate.2-6 When evaluating implant success criteria, several reviews concluded that patients with a history of treated chronic periodontitis (CP) exhibited significantly greater longterm probing depth (PD) and marginal bone loss and a higher incidence of periimplantitis compared with periodontally healthy patients (PHPs).2,3,7-9 Quirynen et al.10 reported a higher incidence of late implant loss and/or marginal bone loss in patients with a history of treated periodontitis. When periodontal maintenance was not provided, the number of implant losses was almost three times higher for patients with a history of treated periodontitis.11 However, in patients doi: 10.1902/jop.2014.140390
201
Implants in Patients With Periodontitis
with a history of treated periodontitis who received periodontal maintenance, the rates of implant failure seem to be low.12-15 However, one question remains: Are the diagnosis of periodontitis and the control of periodontal and peri-implant parameters during periodontal maintenance the key factors for implant longevity? Thus, the aim of this systematic review is to evaluate the long-term (‡5 years) clinical/radiographic outcomes of patients with periodontitis submitted to periodontal therapy and implant placement. The following focused questions were addressed: What are the longterm outcomes of periodontitis patients submitted to periodontal therapy/maintenance and implant placement? Can the original periodontal diagnosis influence the implant prognosis? MATERIALS AND METHODS This review is conducted in accordance with PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses),16 the Cochrane Handbook for Systematic Reviews of Interventions,17 and Check Review18 guidelines. Type of Studies and Inclusion Criteria Observational studies, randomized controlled trials, and/or controlled clinical trials were performed. Studies reported outcomes from titanium implants placed in partially edentulous patients with a history of treated periodontitis. To be included, there has to be evidence that patients with periodontitis had undergone active periodontal treatment and/or maintenance therapy for ‡5 years. Exclusion Criteria Studies not reporting that patients with periodontitis received periodontal therapy before implant placement and periodontal maintenance after implant placement were excluded from the review. Outcome Measures Primary and secondary outcome measures. Primary outcome measures included implant survival and clinical/radiographic peri-implant bone changes (e.g., PD, clinical attachment level [CAL], bleeding on probing [BOP], suppuration, plaque index [PI], and radiographic bone level [BL]). Clinical and/or radiographic periodontal parameters (e.g., PD, CAL, BOP, suppuration, PI, and BL) were secondary outcome measures. Search Strategy Comprehensive search strategies were established to identify studies for this systematic review. The MEDLINE, EMBASE, and CENTRAL databases were searched for papers published before December 15, 2013 based on the following search strategy prepared for MEDLINE: ((((implant OR dental implant 202
Volume 86 • Number 2
OR osseointegration)) OR (attachment loss OR bone remodeling OR bone resorption OR bone loss OR bone defect OR implant failure))) AND (((periodontitis OR chronic periodontitis OR alveolar bone loss OR periodontal treatment OR scaling and root planing OR periodontal therapy))) AND (maintenance OR periodontal maintenance OR supportive periodontal therapy OR maintenance and control). Databases were searched without language restrictions using MeSH terms, key words, and other free terms, and Boolean operators (OR, AND) were used to combine searches. Searching the OpenGRAY database identified unpublished studies, and reference lists of any potential articles were examined. Four dental implant journals, namely Clinical Implant Dentistry and Related Research, Clinical Oral Implants Research, International Journal of Oral & Maxillofacial Implants, and Journal of Oral and Maxillofacial Surgery, were identified as important to this review, and their electronic databases were searched. Assessment of Validity and Data Extraction Two independent reviewers (MSZ and CAD) screened the titles, abstracts, and full texts of the papers that were identified. Disagreement between the reviewers was resolved by discussion. When agreement could not be reached, a third reviewer (LC) was consulted. When important data for the review were missing, the authors were contacted when possible to resolve ambiguity from the trials. The following data were extracted and recorded in duplicate: 1) citation, publication status, and year of publication; 2) location of the trial; 3) study design; 4) characteristics of the participants (age, sex, and smoking habit) and procedures (periodontal treatment, periodontal maintenance, loading protocol, and implant-supported restoration); 5) periodontal parameters and implant outcomes measures; 6) methodologic quality of the trials; and 7) conclusions. Quality Assessment and Risk of Bias in Included Studies The methodologic quality of observational studies was evaluated with the assistance of an adapted version4-6,11 of the Newcastle–Ottawa scale (NOS)19 (Fig. 1). ‘‘Stars’’ (points) were given for each methodologic quality criterion, and each included study could receive a maximum of 14 points. Studies with 11 to 14 points (80% or more of the domains satisfactorily fulfilled) were arbitrarily considered to be of high quality, studies with eight to 10 stars were of medium quality, and studies with less than eight stars were of low methodologic quality. Data Synthesis The data were pooled into evidence tables, and a descriptive summary was created to determine the quantity of data and study variations (characteristics/results).
J Periodontol • February 2015
Zangrando, Damante, Sant’Ana, Rubo de Rezende, Greghi, Chambrone
full text of 28 potentially eligible publications was screened, but 18 did not meet inclusion criteria (Fig. 2). Five studies were excluded because of insufficient follow-up time,20-24 eight because of lack of periodontal/ peri-implant data,25-32 and five studies with data/type of study not of interest for the review.33-37 The k values for inter-reviewer agreement for study inclusion were 0.87 (95% CI 0.75, 0.99) for titles and abstracts and 1.00 for full-text articles, indicating strong agreement. A total of 10 papers regarding four prospective observational studies 12,13,15,38,39 and five retrospective studies 9,40-43 were included. One study was reported in two publications,12,13 so these were grouped under one study name (Roccuzzo et al.12,13). Characteristics of included prospective and retrospective studies are presented in Tables 1 and 2, respectively. 44-55 A total of 748 patients and 1,403 implants were evaluated, and of these, 556 patients were classified as having some degree of periodontal disease.
Figure 1. Modified NOS scale adapted for the purpose of this review.
Raw data and percentages on implant loss were presented for each included study. RESULTS The search resulted in 959 papers, and of them 931 were excluded after title/abstract assessment. The
Periodontal Treatment and Maintenance All studies indicated that patients in the periodontitis group received periodontal treatment before implant placement. However, the details of the treatment provided and/or periodontal status at the moment of the implant surgery were reported infrequently. 38,39,41,42 Some authors9,12,13,15,40,43 carefully described periodontal care. Roccuzzo et al. 12,13,15 described that initial therapy and periodontal surgery was performed as needed after re-evaluation. No implant was placed before the assurance of good motivation and compliance from each patient. In the study of Pjetursson et al.,43 after re-evaluation of the outcomes of initial therapy, periodontal surgery was performed if indicated in 203
Implants in Patients With Periodontitis
Figure 2. Flowchart of manuscripts screened through the review process.
areas with PD ‡6 mm. However, in some cases,38,42,43 isolated residual pockets (RPs) were still present at the end of the periodontal therapy. Lee et al.42 considered RPs as at least one periodontal pocket with PD ‡6 mm and Pjetursson et al.43 as PD ‡5 mm. All studies indicated that patients enrolled in a periodontal maintenance program, but details of the treatment provided, attendance, and frequency of the appointments were occasionally reported.12,13,15,41 These studies12,13,15,41 compared clinical parameters of periodontally compromised patients (PCPs) with PHPs and their attendance to a maintenance program. A higher percentage of individuals in the moderate and severe PCP groups did not comply with periodontal maintenance.12,13,15 PCPs that complied with periodontal maintenance presented periodontal and peri-implant conditions similar to PHPs.41,42 Periodontal and Peri-Implant Clinical/ Radiographic Evaluation at Follow-Up Periodontal and peri-implant status were reported with different parameters (Tables 1 and 2). The presence of PI and bleeding index (BI) in teeth and implants at follow-up were variable among included studies, but overall, implant survival was high. The implant survival rate was described in seven studies.9,12,13,15,38-40,43 The mean percentage of implant survival considering just patients with periodontitis evaluated after 10 years of follow-up was 92.1%.9,12,13,15,38-40 Leonhardt et al.38 showed that almost 50% of the individuals were positive for plaque and presented BOP at 35.3% of the evaluated tooth sites and 61% of implant surfaces. Of the tooth surfaces, 15.7% had PD ‡4 mm and 3.1% had PD ‡6 mm. Although mean – SD BL around teeth (0.8 – 1.5 204
Volume 86 • Number 2
mm) was lower compared with implants (1.7 – 1.2 mm), the survival rate for implants was higher (94.7% versus 87%). Karoussis et al.39 found lower mean – SD values for PI (PI)48 and BI (BI)48 for implants (0.36 and 0.19, respectively) when compared with teeth (0.40 and 0.28, respectively). Conversely, the mean percentage of BOP was higher (42.2%) for implants when compared with teeth (30.2%),39 and PD and CAL for implants also present higher values (2.78 and -3.33 mm) as does mean BL (4.65 mm [mesial] and 4.66 mm [distal]) compared with teeth. The study did not provide the implant survival rate, but tooth survival rate was 95%.39 Roccuzzo et al.12,13 separated patients into three groups: 1) PHP; 2) moderate PCP; and 3) severe PCP. The mean plaque score, full-mouth plaque score (FMPS), and full-mouth bleeding score (FMBS) for the moderate and severe PCP groups were >20%, whereas BOP exceeded 30% in these groups. Higher mean PD and deepest PD around implants were observed in the moderate and severe PCP groups. Mean BL and percentage of sites with BL ‡3 mm around implants were also superior in the moderate and severe PCP groups. The percentage of implant survival rate was 92.8% for moderate and 90% for the severe PCP group. In the study by Roccuzzo et al.,15 FMPS and FMBS for the moderate and severe PCP groups were from 20% to 30%. Mean percentages of plaque and BOP around implants were >30%. The percentage of implants with at least one site with PD ‡6 mm was higher for the moderate and severe PCP groups, and implant survival rate was lower (96.9% and 97.1%). The mean PI in the study by Mir-Mari et al.41 tooth and implants was 25.1%, whereas the gingival BI was 10.5%. When considering the PCP group, those who complied with periodontal maintenance presented mean BL around implants of 0.32 – 0.77 mm, but for those who were not compliant with periodontal maintenance visits, the mean BL was 2.50 – 2.19 mm. Lee et al.42 presented percentage of plaque and BOP around implants in the PCP group 20% to 30%. In the PCP group with RPs (PD ‡6 mm) around teeth, the mean PD and BL around implants was higher compared with the nonresidual pockets (NRPs) group. A peri-implant PD ‡5 mm with BOP was used as a threshold to define periimplantitis. There were more implant sites with periimplantitis in the RP subgroup than in the NRP subgroup. Two studies9,40 used the same methodology to evaluate
Karoussis et al., 2004
39
Leonhardt et al., 200238
Study
Prospective study, 10 years of follow-up
Longitudinal follow-up study, 10 years of follow-up
Methods
89 partially dentate patients with periodontal disease, aged 28 to 88 years
Regular maintenance checkup program44
Inclusion of smokers NR Treatment of advanced periodontitis, but details NR
Implant-supported restoration NR
Clinical and radiographic evaluation of teeth and implants
Correlations between marginal bone loss at implants versus teeth were assessed by Spearman rankcorrelation test
57 implants/261 teeth were evaluated
Loading protocol: two-stage surgery
Clinical and radiographic evaluation of teeth and implants
Outcomes Measures
15 (8 males, 7 females) partially dentate patients with advanced periodontitis, aged 39 to 79 years
Participants and Procedures
Characteristics of Included Prospective Studies
Table 1.
PI mean = 0.40 (Silness and Lo¨e, 1964)47 for all teeth
Implant survival = 94.7%
No significant correlation between marginal bone loss of implant and teeth (P >0.05) Tooth loss = 13%
PD: 15.7% of tooth surfaces with PD ‡4 mm and 3.1% with PD ‡6 mm BL: teeth mean BL = 0.8 – 1.5 mm, implant mean BL = 1.7 – 1.2 mm
BOP: 61% implant surfaces/ 35% tooth sites
Presence of plaque: 7 individuals positive for plaque (50%)
Main Results
These results present evidence for the association between periodontal and periimplant conditions and the changes in these tissues over 10 years in partially edentulous patients.
Titanium implants ad modum Branemark can be maintained with excellent results over a 10-year period in patients treated previously for advanced periodontitis.
Conclusions
J Periodontol • February 2015 Zangrando, Damante, Sant’Ana, Rubo de Rezende, Greghi, Chambrone
205
206
Study
Methods
Outcomes Measures
Main Results
179 implants/179 teeth were Changes between the 1- and mPI mean = 0.36 (Mombelli et al., 1987)48 for all evaluated 10-year examinations were analyzed using implants Wilcoxon matched-pairs sign-rank tests. The statistical unit was always a pair of an implant with the contralateral tooth. Multiple stepwise regression analyses were run to detect periodontal and patient factors influencing the periimplant tissue conditions at 10 years. Loading protocol: two-stage GI mean = 0.28 (Lo¨e and surgery Silness, 1963)49 for all teeth mBI mean = 0.19 (Mombelli Implant-supported et al., 1987)48 for all restoration: single crowns/ fixed partial restorations implants BOP mean = 30.2% for Inclusion of light smokers teeth (Lang et al., 1986)50 (
Review Long-Term Evaluation of Periodontal Parameters and Implant Outcomes in Periodontally Compromised Patients: A Systematic Review Mariana Schutzer Zangrando,* Carla Andreotti Damante,* Adriana Campos Sant’Ana,* Maria Lu´cia Rubo de Rezende,* Sebastia ˜o Luiz Greghi,* and Leandro Chambrone†
Background: The aim of this systematic review is to evaluate the long-term outcomes of patients with periodontitis submitted to periodontal therapy/maintenance and implant placement. Methods: Studies reporting clinical and/or long-term implant outcomes from partially edentulous patients with periodontitis who were treated and followed periodontal maintenance for ‡5 years were considered eligible for the review. Screening of the articles, data extraction, and quality assessment were conducted independently and in duplicate. Results: Search of MEDLINE, EMBASE, and CENTRAL databases resulted in 959 papers, and of them 931 were excluded after title/abstract assessment. The full texts of 28 potentially eligible publications were screened, but only 10 studies met inclusion criteria. Most of the included studies (77.8%) presented a medium/high methodologic quality. The results demonstrated that patients with a diagnosis of periodontitis had satisfactory implant outcomes. Implant survival was high (92.1%) within studies reporting 10 years of follow-up. Parameters related to probing depth, clinical attachment level, and bone loss around teeth increased the occurrence of peri-implantitis and implant loss. Non-attendance to periodontal maintenance and smoking habits were also associated with less favorable implant outcomes. Conclusions: This systematic review confirmed that implant therapy can be successfully used in patients with a diagnosis of periodontitis who underwent proper therapy and regular periodontal maintenance. Residual pockets, nonattendance to the periodontal maintenance program, and smoking were considered to be negative factors for the long-term implant outcomes. J Periodontol 2015;86:201-221. KEY WORDS Dental implants; osseointegration; peri-implantitis; periodontitis; systematic review. * Division of Periodontics, Department of Prosthodontics, School of Dentistry at Bauru (Faculty of Odontology of Bauru), University of Sa˜o Paulo, Bauru, Sa˜o Paulo, Brazil. † Unit of Basic Oral Investigation, Faculty of Dentistry, El Bosque University, Bogota´, Colombia.
B
ecause an increasing number of patients receive implants to replace missing teeth lost as a result of periodontitis, the question arises as to whether a history of periodontitis may increase the risk of peri-implant disease (e.g., mucositis and peri-implantitis) and implant loss. The term ‘‘implant survival’’ refers to the presence of an implant with or without complications, and ‘‘implant success’’ refers to the presence of an implant in the absence of complications of either a biologic or technical nature.1 Some review papers clearly indicated that partially and completely edentulous patients can be rehabilitated predictably by oral implants with high implant survival rate.2-6 When evaluating implant success criteria, several reviews concluded that patients with a history of treated chronic periodontitis (CP) exhibited significantly greater longterm probing depth (PD) and marginal bone loss and a higher incidence of periimplantitis compared with periodontally healthy patients (PHPs).2,3,7-9 Quirynen et al.10 reported a higher incidence of late implant loss and/or marginal bone loss in patients with a history of treated periodontitis. When periodontal maintenance was not provided, the number of implant losses was almost three times higher for patients with a history of treated periodontitis.11 However, in patients doi: 10.1902/jop.2014.140390
201
Implants in Patients With Periodontitis
with a history of treated periodontitis who received periodontal maintenance, the rates of implant failure seem to be low.12-15 However, one question remains: Are the diagnosis of periodontitis and the control of periodontal and peri-implant parameters during periodontal maintenance the key factors for implant longevity? Thus, the aim of this systematic review is to evaluate the long-term (‡5 years) clinical/radiographic outcomes of patients with periodontitis submitted to periodontal therapy and implant placement. The following focused questions were addressed: What are the longterm outcomes of periodontitis patients submitted to periodontal therapy/maintenance and implant placement? Can the original periodontal diagnosis influence the implant prognosis? MATERIALS AND METHODS This review is conducted in accordance with PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses),16 the Cochrane Handbook for Systematic Reviews of Interventions,17 and Check Review18 guidelines. Type of Studies and Inclusion Criteria Observational studies, randomized controlled trials, and/or controlled clinical trials were performed. Studies reported outcomes from titanium implants placed in partially edentulous patients with a history of treated periodontitis. To be included, there has to be evidence that patients with periodontitis had undergone active periodontal treatment and/or maintenance therapy for ‡5 years. Exclusion Criteria Studies not reporting that patients with periodontitis received periodontal therapy before implant placement and periodontal maintenance after implant placement were excluded from the review. Outcome Measures Primary and secondary outcome measures. Primary outcome measures included implant survival and clinical/radiographic peri-implant bone changes (e.g., PD, clinical attachment level [CAL], bleeding on probing [BOP], suppuration, plaque index [PI], and radiographic bone level [BL]). Clinical and/or radiographic periodontal parameters (e.g., PD, CAL, BOP, suppuration, PI, and BL) were secondary outcome measures. Search Strategy Comprehensive search strategies were established to identify studies for this systematic review. The MEDLINE, EMBASE, and CENTRAL databases were searched for papers published before December 15, 2013 based on the following search strategy prepared for MEDLINE: ((((implant OR dental implant 202
Volume 86 • Number 2
OR osseointegration)) OR (attachment loss OR bone remodeling OR bone resorption OR bone loss OR bone defect OR implant failure))) AND (((periodontitis OR chronic periodontitis OR alveolar bone loss OR periodontal treatment OR scaling and root planing OR periodontal therapy))) AND (maintenance OR periodontal maintenance OR supportive periodontal therapy OR maintenance and control). Databases were searched without language restrictions using MeSH terms, key words, and other free terms, and Boolean operators (OR, AND) were used to combine searches. Searching the OpenGRAY database identified unpublished studies, and reference lists of any potential articles were examined. Four dental implant journals, namely Clinical Implant Dentistry and Related Research, Clinical Oral Implants Research, International Journal of Oral & Maxillofacial Implants, and Journal of Oral and Maxillofacial Surgery, were identified as important to this review, and their electronic databases were searched. Assessment of Validity and Data Extraction Two independent reviewers (MSZ and CAD) screened the titles, abstracts, and full texts of the papers that were identified. Disagreement between the reviewers was resolved by discussion. When agreement could not be reached, a third reviewer (LC) was consulted. When important data for the review were missing, the authors were contacted when possible to resolve ambiguity from the trials. The following data were extracted and recorded in duplicate: 1) citation, publication status, and year of publication; 2) location of the trial; 3) study design; 4) characteristics of the participants (age, sex, and smoking habit) and procedures (periodontal treatment, periodontal maintenance, loading protocol, and implant-supported restoration); 5) periodontal parameters and implant outcomes measures; 6) methodologic quality of the trials; and 7) conclusions. Quality Assessment and Risk of Bias in Included Studies The methodologic quality of observational studies was evaluated with the assistance of an adapted version4-6,11 of the Newcastle–Ottawa scale (NOS)19 (Fig. 1). ‘‘Stars’’ (points) were given for each methodologic quality criterion, and each included study could receive a maximum of 14 points. Studies with 11 to 14 points (80% or more of the domains satisfactorily fulfilled) were arbitrarily considered to be of high quality, studies with eight to 10 stars were of medium quality, and studies with less than eight stars were of low methodologic quality. Data Synthesis The data were pooled into evidence tables, and a descriptive summary was created to determine the quantity of data and study variations (characteristics/results).
J Periodontol • February 2015
Zangrando, Damante, Sant’Ana, Rubo de Rezende, Greghi, Chambrone
full text of 28 potentially eligible publications was screened, but 18 did not meet inclusion criteria (Fig. 2). Five studies were excluded because of insufficient follow-up time,20-24 eight because of lack of periodontal/ peri-implant data,25-32 and five studies with data/type of study not of interest for the review.33-37 The k values for inter-reviewer agreement for study inclusion were 0.87 (95% CI 0.75, 0.99) for titles and abstracts and 1.00 for full-text articles, indicating strong agreement. A total of 10 papers regarding four prospective observational studies 12,13,15,38,39 and five retrospective studies 9,40-43 were included. One study was reported in two publications,12,13 so these were grouped under one study name (Roccuzzo et al.12,13). Characteristics of included prospective and retrospective studies are presented in Tables 1 and 2, respectively. 44-55 A total of 748 patients and 1,403 implants were evaluated, and of these, 556 patients were classified as having some degree of periodontal disease.
Figure 1. Modified NOS scale adapted for the purpose of this review.
Raw data and percentages on implant loss were presented for each included study. RESULTS The search resulted in 959 papers, and of them 931 were excluded after title/abstract assessment. The
Periodontal Treatment and Maintenance All studies indicated that patients in the periodontitis group received periodontal treatment before implant placement. However, the details of the treatment provided and/or periodontal status at the moment of the implant surgery were reported infrequently. 38,39,41,42 Some authors9,12,13,15,40,43 carefully described periodontal care. Roccuzzo et al. 12,13,15 described that initial therapy and periodontal surgery was performed as needed after re-evaluation. No implant was placed before the assurance of good motivation and compliance from each patient. In the study of Pjetursson et al.,43 after re-evaluation of the outcomes of initial therapy, periodontal surgery was performed if indicated in 203
Implants in Patients With Periodontitis
Figure 2. Flowchart of manuscripts screened through the review process.
areas with PD ‡6 mm. However, in some cases,38,42,43 isolated residual pockets (RPs) were still present at the end of the periodontal therapy. Lee et al.42 considered RPs as at least one periodontal pocket with PD ‡6 mm and Pjetursson et al.43 as PD ‡5 mm. All studies indicated that patients enrolled in a periodontal maintenance program, but details of the treatment provided, attendance, and frequency of the appointments were occasionally reported.12,13,15,41 These studies12,13,15,41 compared clinical parameters of periodontally compromised patients (PCPs) with PHPs and their attendance to a maintenance program. A higher percentage of individuals in the moderate and severe PCP groups did not comply with periodontal maintenance.12,13,15 PCPs that complied with periodontal maintenance presented periodontal and peri-implant conditions similar to PHPs.41,42 Periodontal and Peri-Implant Clinical/ Radiographic Evaluation at Follow-Up Periodontal and peri-implant status were reported with different parameters (Tables 1 and 2). The presence of PI and bleeding index (BI) in teeth and implants at follow-up were variable among included studies, but overall, implant survival was high. The implant survival rate was described in seven studies.9,12,13,15,38-40,43 The mean percentage of implant survival considering just patients with periodontitis evaluated after 10 years of follow-up was 92.1%.9,12,13,15,38-40 Leonhardt et al.38 showed that almost 50% of the individuals were positive for plaque and presented BOP at 35.3% of the evaluated tooth sites and 61% of implant surfaces. Of the tooth surfaces, 15.7% had PD ‡4 mm and 3.1% had PD ‡6 mm. Although mean – SD BL around teeth (0.8 – 1.5 204
Volume 86 • Number 2
mm) was lower compared with implants (1.7 – 1.2 mm), the survival rate for implants was higher (94.7% versus 87%). Karoussis et al.39 found lower mean – SD values for PI (PI)48 and BI (BI)48 for implants (0.36 and 0.19, respectively) when compared with teeth (0.40 and 0.28, respectively). Conversely, the mean percentage of BOP was higher (42.2%) for implants when compared with teeth (30.2%),39 and PD and CAL for implants also present higher values (2.78 and -3.33 mm) as does mean BL (4.65 mm [mesial] and 4.66 mm [distal]) compared with teeth. The study did not provide the implant survival rate, but tooth survival rate was 95%.39 Roccuzzo et al.12,13 separated patients into three groups: 1) PHP; 2) moderate PCP; and 3) severe PCP. The mean plaque score, full-mouth plaque score (FMPS), and full-mouth bleeding score (FMBS) for the moderate and severe PCP groups were >20%, whereas BOP exceeded 30% in these groups. Higher mean PD and deepest PD around implants were observed in the moderate and severe PCP groups. Mean BL and percentage of sites with BL ‡3 mm around implants were also superior in the moderate and severe PCP groups. The percentage of implant survival rate was 92.8% for moderate and 90% for the severe PCP group. In the study by Roccuzzo et al.,15 FMPS and FMBS for the moderate and severe PCP groups were from 20% to 30%. Mean percentages of plaque and BOP around implants were >30%. The percentage of implants with at least one site with PD ‡6 mm was higher for the moderate and severe PCP groups, and implant survival rate was lower (96.9% and 97.1%). The mean PI in the study by Mir-Mari et al.41 tooth and implants was 25.1%, whereas the gingival BI was 10.5%. When considering the PCP group, those who complied with periodontal maintenance presented mean BL around implants of 0.32 – 0.77 mm, but for those who were not compliant with periodontal maintenance visits, the mean BL was 2.50 – 2.19 mm. Lee et al.42 presented percentage of plaque and BOP around implants in the PCP group 20% to 30%. In the PCP group with RPs (PD ‡6 mm) around teeth, the mean PD and BL around implants was higher compared with the nonresidual pockets (NRPs) group. A peri-implant PD ‡5 mm with BOP was used as a threshold to define periimplantitis. There were more implant sites with periimplantitis in the RP subgroup than in the NRP subgroup. Two studies9,40 used the same methodology to evaluate
Karoussis et al., 2004
39
Leonhardt et al., 200238
Study
Prospective study, 10 years of follow-up
Longitudinal follow-up study, 10 years of follow-up
Methods
89 partially dentate patients with periodontal disease, aged 28 to 88 years
Regular maintenance checkup program44
Inclusion of smokers NR Treatment of advanced periodontitis, but details NR
Implant-supported restoration NR
Clinical and radiographic evaluation of teeth and implants
Correlations between marginal bone loss at implants versus teeth were assessed by Spearman rankcorrelation test
57 implants/261 teeth were evaluated
Loading protocol: two-stage surgery
Clinical and radiographic evaluation of teeth and implants
Outcomes Measures
15 (8 males, 7 females) partially dentate patients with advanced periodontitis, aged 39 to 79 years
Participants and Procedures
Characteristics of Included Prospective Studies
Table 1.
PI mean = 0.40 (Silness and Lo¨e, 1964)47 for all teeth
Implant survival = 94.7%
No significant correlation between marginal bone loss of implant and teeth (P >0.05) Tooth loss = 13%
PD: 15.7% of tooth surfaces with PD ‡4 mm and 3.1% with PD ‡6 mm BL: teeth mean BL = 0.8 – 1.5 mm, implant mean BL = 1.7 – 1.2 mm
BOP: 61% implant surfaces/ 35% tooth sites
Presence of plaque: 7 individuals positive for plaque (50%)
Main Results
These results present evidence for the association between periodontal and periimplant conditions and the changes in these tissues over 10 years in partially edentulous patients.
Titanium implants ad modum Branemark can be maintained with excellent results over a 10-year period in patients treated previously for advanced periodontitis.
Conclusions
J Periodontol • February 2015 Zangrando, Damante, Sant’Ana, Rubo de Rezende, Greghi, Chambrone
205
206
Study
Methods
Outcomes Measures
Main Results
179 implants/179 teeth were Changes between the 1- and mPI mean = 0.36 (Mombelli et al., 1987)48 for all evaluated 10-year examinations were analyzed using implants Wilcoxon matched-pairs sign-rank tests. The statistical unit was always a pair of an implant with the contralateral tooth. Multiple stepwise regression analyses were run to detect periodontal and patient factors influencing the periimplant tissue conditions at 10 years. Loading protocol: two-stage GI mean = 0.28 (Lo¨e and surgery Silness, 1963)49 for all teeth mBI mean = 0.19 (Mombelli Implant-supported et al., 1987)48 for all restoration: single crowns/ fixed partial restorations implants BOP mean = 30.2% for Inclusion of light smokers teeth (Lang et al., 1986)50 (
