IMPLANT DENTISTRY / VOLUME 0, NUMBER 0 2015

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Plaque Score Change as an Indicator for Periimplant Health in Periodontal Patients With Immediately Restored Dental Implants Eran Gabay, DMD, PhD,* Liran Levin, DMD,† Otman Zuabi, DMD,‡ and Jacob Horwitz, DMD§

atients with a history of periodontal disease, or periodontally compromised patients, are a subgroup of special interest within implant patients. A moderate level of evidence, as suggested in numerous publications, systematic reviews, and a critical appraisal of systematic reviews, indicates that subjects with a history of periodontitis might be at significantly higher risk for implant failure and greater marginal bone loss, compared with periodontally healthy subjects.1–3 Implant survival and success rates, the ultimate and most significant outcome variables, may take years to evaluate. Therefore, shorter term surrogate outcome variables, such as probing depth (PD) and bleeding on probing (BOP) changes, may be useful for monitoring implant health.4 These variables may

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*Attending Physician, Department of Periodontology, School of Graduate Dentistry, Rambam Health Care Campus, Haifa, Israel. †Former Head of Research, Department of Periodontology, School of Graduate Dentistry, Rambam Health Care Campus, Haifa, Israel; Ruth and Bruce Rappaport Faculty of Medicine, Technion Israel Institute of Technology, Haifa, Israel. ‡Former Head of Research, Department of Periodontology, School of Graduate Dentistry, Rambam Health Care Campus, Haifa, Israel; Ruth and Bruce Rappaport Faculty of Medicine, Technion Israel Institute of Technology, Haifa, Israel. §Director, Postgraduate Program in Periodontology, Department of Periodontology, School of Graduate Dentistry, Rambam Health Care Campus, Haifa, Israel; Ruth and Bruce Rappaport Faculty of Medicine, Technion Israel Institute of Technology, Haifa, Israel.

Reprint requests and correspondence to: Eran Gabay, DMD, PhD, Department of Periodontology, School of Graduate Dentistry, Rambam Health Care Campus, P.O. Box 9602, Haifa 3109601, Israel, Phone: 972-48542983, Fax: 972-4-8543057, E-mail: e_gabay@ rambam.health.gov.il ISSN 1056-6163/15/00000-001 Implant Dentistry Volume 0  Number 0 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved. DOI: 10.1097/ID.0000000000000236

Background: Patients with a history of periodontitis might have a higher risk for implant failure as compared with periodontally healthy subjects. The aim of the present study was to look into this risk factor by examining the association between plaque scores, probing depths (PD), and bleeding on probing (BOP) around teeth and immediately restored dental implants up to 1 year after implant surgery. Methods: Patients with partial edentulism, diagnosed with and previously treated for generalized chronic periodontitis, received dental implants, abutments, and cemented provisional prostheses up to 72 hours after implant surgery. Plaque scores, PD, and BOP were recorded and evaluated 6 and 12 months postsurgery. Results: Plaque scores deteriorated slightly around teeth and

improved around implants. No significant change was observed in the distribution of PD around teeth. The proportion of shallow pockets increased around implants. Improvement in plaque scores was associated with a stable/reduced PD, whereas deterioration in plaque scores was associated with increased PD around implants and teeth. Conclusions: A direct relationship was found between plaque score improvement and stable/reduced PD. Therefore, partially edentulous patients with a history of periodontitis should be encouraged to improve their plaque scores to maintain shallower pockets around implants. (Implant Dent 2015;0:1–5) Key Words: dental implants, periodontitis, periimplantitis

be a reflection of gingival and periimplant infection.5 Periimplant soft tissue conditions are usually monitored using PD, gingival margin level, suppuration, BOP, swelling,6 and oral hygiene status.7–9 Higher plaque scores are associated with increased gingival and periimplant tissue inflammation manifesting as gingivitis10 and periimplant mucositis.11 In a 9- to 14-year follow-up study of implant patients, periimplant mucositis was present in 48% of the implants and 13.3% of

the implants had a bone-level decrease of 3 to 4 threads.12 Because early detection of periimplant soft tissue changes is considered a valuable tool in the monitoring and management of implant therapy, the aim of this prospective study was to look at the association between changes in patient plaque score, PD, and BOP and those changes around dental implants. More specifically, aims were as follows: (1) to evaluate soft tissue parameters up to 1 year postsurgery,

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including plaque scores, PD, and BOP around teeth and around immediately restored dental implants in partially edentulous patients with treated periodontal disease, and (2) to examine the association between plaque scores and PD and between plaque scores and BOP around teeth and around implants up to 1 year after implant surgery.

MATERIALS

AND

METHODS

Patients presenting with partial edentulism, who were previously diagnosed and treated for generalized chronic periodontitis, and expressed their wish to receive dental implants with immediate restoration were invited to participate in the study. Upon initial acceptance, patients signed a consent form. The following inclusion criteria were further used: (1) age between 18 and 75 years; (2) good general health, no complicating systemic conditions that contraindicated surgical periodontal and implant treatment and/or radiographic evaluation (eg, pregnancy, uncontrolled diabetes, cancer/radiation therapy, bisphosphonate therapy), and no allergy to antibiotics; (3) active periodontal therapy completed; (4) plaque score #1, according to a modification of the Silness and Löe13 Plaque Index, whereby recording only the highest score for each tooth/dental unit and dividing the sum by the number of teeth/dental units; and (5) BOP14 #10% (6 recordings per tooth). Smoking was not considered an exclusion factor. The study was approved by Institutional Review Board of the hospital (approval no. 2301), and the study design and partial results, including implant survival and success and radiographic changes, have been previously described.15 Briefly, patients received their dental implants, followed by the installation of abutments and cemented provisional prostheses up to 72 hours after implant surgery.16,17 Patients were seen for suture removal 10 to 14 days after surgery and then at 4 weeks and 3, 6, and 12 months postsurgery for maintenance appointments consisting of plaque control and motivation, tooth and implant cleaning, and scaling and root planning as necessary. Soft tissue measurements were performed at 6 and 12

ET AL

Table 1. Distribution of Plaque Scores, PD, and BOP Around Teeth Baseline Total Plaque score

Total PD

PD Total BOP

BOP Interproximal

0 1 2 3 1–3 4–6 7+ 1–4 5+ 0 1 2+ 0 1 2+

6 mo

12 mo

No.

%

No.

%

No.

%

342 228 96 17 1 316 215 96 5 277 39 316 195 81 40 216 76 24

100 67 28 5 0 100 68 30 2 88 12 100 37 15 8 41 14 5

279 189 73 15 2 275 208 65 2 257 18 275 176 69 30 194 59 22

100 68 26 5 1 100 76 24 1 93 7 100 38 15 6 41 13 5

299 182 88 29 0 302 224 74 4 268 34 301 162 91 48 183 84 34

100 61 29 10 0 100 74 25 1 89 11 100 33 19 10 38 17 7

months and included the following variables: plaque score was recorded for each tooth consisting of the highest score measured anywhere on the tooth/implant circumference. PD (in millimeters) and BOP were recorded at 6 sites per tooth at baseline and 6 and 12 months postsurgery. PD measurements around implants were performed after completion of the healing phase to avoid disruption of the epithelial and connective tissue attachment.18 Implant PD, BOP, and plaque scores were recorded at 6 and 12 months. After the 6-month visit and verification of implant stability, patients were referred to their dentists for fabrication and delivery of the final fixed prostheses. Patients were discharged from the study after completion of the 12-month examination. Data Management and Analyses

Data analysis was performed using IBM SPSS Advanced Statistics software (IBM Corporation, Armonk, NY). Plaque scores: Teeth and implants were divided into 4 categories according to their plaque scores (0–3). PD: Teeth and implants were categorized according to the highest measured PD around them into shallow (1– 3 mm), medium (4–6 mm), and deep ($7 mm) groups. Additionally, they

P (6 vs 12 mo) 0.02

0.82

,0.001

0.028

0.005

were subcategorized into 2 groups of 1 to 4 mm and $5 mm. BOP: Teeth and implants were categorized according to the number of bleeding points found around them (maximum 6 points) into 3 groups: 0 bleeding points, 1 bleeding point, and $2 bleeding points. In addition, they were similarly subcategorized according to the number of only interproximal bleeding sites. Six- and 12-month plaque scores, PD, and BOP around implants and around teeth were compared using x2 test. Associations between plaque scores and PD and between plaque scores and BOP were tested using Spearman nonparametric correlation. Changes over time around teeth and around implants in plaque scores, PD, and BOP were calculated, and changes in plaque scores were compared with changes in PD and BOP using x2 test. Significance was set at 5%.

RESULTS Eighteen patients (6 males [2 smokers] and 12 females [3 smokers]) were accepted and treated with a total of 50 implants, ranging between 1 and 8 implants per patient. Four implants failed: One was a single-unit implant

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IMPLANT DENTISTRY / VOLUME 0, NUMBER 0 2015 in a smoking patient and 3 implants in another smoking patient (of which one was a single unit and the other 2 were splinted in a 2-unit restoration). Periodontal data for these implants were therefore missing. Missing data also included 1 patient who did not show up for the 6-month evaluation, 1 patient who was not charted during the 6-month evaluation, and 1 patient who was not charted during the 12-month evaluation. The 12-month overall survival rate was 92% (46 of 50). Implant survival rate among nonsmokers was 100% (35 of 35), whereas among smokers, survival rate was 73% (11 of 15) (data previously published).15 Data for the distribution of plaque scores, PD, and BOP around teeth and implants at baseline, 6 months, and 12 months are presented in Tables 1 and 2. Plaque scores deteriorated slightly between 6 and 12 months around teeth (P ¼ 0.02) and improved, although not significantly, around implants (P ¼ 0.19). There was an increase in the percentage of teeth with PD $5 mm (P , 0.001), but no significant change was observed in the distribution of teeth into shallow, medium, and deep pockets. No significant increase in percentage of implants with PD $5 was observed; however, there was a significant increase in the proportion of shallow pockets (P , 0.001). There was a small significant increase in BOP around teeth (P ¼ 0.028) and a small significant decrease in BOP around implants (P ¼ 0.003). Correlations between plaque scores and PD and between plaque scores and BOP around teeth and implants are presented in Tables 3 and 4, respectively. There was a modest but significant correlation between plaque scores and PD and between plaque scores and BOP around teeth at baseline, 6 months, and 12 months. A significant correlation between plaque scores and PD around implants was found only at 12 months, whereas no correlation was found between plaque scores and BOP around implants at either 6 or 12 months. Because an increase in PD and BOP is of clinical concern, we looked at correlations between changes in plaque scores and increases in PD and

Table 2. Distribution of Plaque Scores, PD, and BOP Around Implants 6 mo Total Plaque score

Total PD

0 1 2 3 1–3 4–6 7+ 1–4 5+

PD Total BOP

BOP Interproximal

0 1 2+ 0 1 2+

12 mo

No.

%

No.

%

37 16 18 3 0 42 22 20 0 41 1 42 20 15 7 24 12 6

100 43 49 8 0 100 52 48 0 98 2 100 30 23 11 36 18 9

38 28 9 1 0 45 29 16 0 41 4 45 27 14 4 30 12 3

100 74 24 3 0 100 64 36 0 91 9 100 36 19 5 40 16 4

P (6 vs 12 mo) 0.019

,0.001

0.99

0.003

0.003

Table 3. Correlations Between Plaque Scores and PD and Between Plaque Scores and BOP Around Teeth at Baseline, 6 Months, and 12 Months Teeth Baseline 6 mo 12 mo

Spearman coefficient P Spearman coefficient P Spearman coefficient P

Plaque Scores vs PD

Plaque Scores vs BOP

0.165 0.003 0.184 0.003 0.226 0.000

0.116 0.040 0.154 0.013 0.224 0.000

Statistically significant P values are presented in bold.

Table 4. Correlations Between Plaque Scores and PD and Between Plaque Scores and BOP Around Implants at 6 Months and 12 Months Implants 6 mo 12 mo

Spearman coefficient P Spearman coefficient P

Plaque Scores vs PD

Plaque Scores vs BOP

0.207 0.218 0.417 0.009

0.257 0.125 −0.055 0.742

Statistically significant P values are presented in bold.

Fig. 1. Association between changes in plaque scores and increases in PD.

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ET AL

Fig. 2. Association between changes in plaque scores and changes in BOP.

BOP around teeth and around implants (Figs. 1 and 2). An increase in PD was found in 40% of teeth and 83% of implants in which plaque scores increased (P ¼ 0.01). An increase in BOP was found in 40% of teeth in which plaque scores increased but only 25% of teeth in which plaque scores decreased (P ¼ 0.034); no such correlation was found around implants.

DISCUSSION The main finding in the present study was that improved plaque scores were associated with a stable/reduced PD, whereas deterioration in plaque scores was associated with increased PD around both implants and teeth. Improved plaque scores around teeth were also associated with a reduction in BOP, whereas deterioration was associated with increased BOP; however, no such association was found around dental implants. This lack of correlation between plaque score and BOP in implants might be explained by the high rate of BOP around implants in the present study, which corroborates previous reports of 69% to 92% BOP around dental implants in periodontitis patients.19,20 The short-term results of the present study are in accordance with the paradigm-associating adherence to supportive periodontal therapy (SPT) and longterm implant survival and success. Furthermore, the present study demonstrates a specific association between plaque scores and PD. Most recent publications support this idea: The influence of SPT on periimplantitis and implant loss was

assessed in 70 periodontitis-susceptible patients who received dental implants. The prevalence of periimplantitis was lower in the group that was in a wellorganized SPT program.21 In another group of patients with dental implants after 1 year in function, who had a history of treated chronic periodontitis and who did or did not attend SPT, a statistically significant relationship was demonstrated between bone loss around the implants and the patient’s plaque index.22 Implants placed both in patients treated for periodontitis and in periodontally healthy patients were monitored for periimplantitis in a 10-year prospective study. A statistically significant difference was found between periodontally healthy and periodontally compromised patients in plaque index, BOP, and PD around the implants, all of them demonstrating higher values in periodontally compromised patients.23 However, these findings are not unequivocal. In a group of 23 partially edentulous patients referred for the treatment of periimplantitis, no significant correlation was found between plaque index and the existence or absence of periimplantitis.24 The results of this short-term present study demonstrate the positive effect of proper plaque control by patient monitoring using PD and BOP. Short-term changes in oral hygiene can affect PD in both ways; improvement in plaque control may induce a decrease in PD, whereas deterioration may be associated with an increase in PD. Regarding BOP, contrary to natural teeth, no such association was found around

dental implants. This may be considered as evidence to a different behavior of the soft tissues around dental implants, which are, after all, foreign bodies25 with a different surrounding anatomy. Histomorphological research demonstrated that periimplant mucosa differs from gingival tissues in several aspects; collagen fibers in the periimplant supracrestal connective tissue are oriented parallel to the implant surface, whereas in the gingiva, the collagen fibers are perpendicular to the root cementum.26 Also, the connective tissue around implants contains more collagen fibers but fewer fibroblasts and vascular structures than the corresponding tissue around teeth.27 These anatomical and histological differences may reflect in a different expression of PD and BOP changes over time.28 Anatomical differences in soft tissue thickness may also influence probing in health. For example, palatal PD around maxillary anterior implants tends to be deeper than labial PD. Periimplantitis and soft tissue complications are the second most frequent complication associated with dental implant therapy (8.5%) preceded only by fractures of the veneering material (13.5%).29 Therefore, results of the present study may help to motivate patients and dental therapists to invest efforts in improving oral hygiene because this may result in shallower PD and decrease the risk for such complications. The present study is the first to demonstrate the association between plaque scores in the remaining dentition and PD around implants, but, yet, it has some drawbacks; the small sample size and short duration may diminish its power. Other factors might affect plaque scores, PD, and BOP, including stress, medications, smoking, and dental restorations.30–32 The influence of these factors should be addressed in future studies of longer duration and larger sample size. Also, the question whether short-term changes in PD and BOP correlate with long-term success/survival rates of dental implants still remains unanswered.

CONCLUSIONS Changes in plaque scores in the remaining dentition were inversely

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IMPLANT DENTISTRY / VOLUME 0, NUMBER 0 2015 associated with changes in PD around implants. Patients with a history of periodontitis should be encouraged to improve their full mouth plaque scores so that it may result in shallower pockets around their implants. This association may reflect upon occurrence of periimplantitis and, ultimately, implant survival. Further studies over longer periods of time with larger cohorts would help to further understand the association between plaque control changes and soft tissue changes around dental implants and their association with implant success.

DISCLOSURE The authors claim to have no financial interest, either directly or indirectly, in the products or information listed in the article.

ACKNOWLEDGMENTS The authors are deeply grateful to Ms. Tanya Mashiach from the Rambam Health Care Campus Statistical Unit for the statistical analysis. This study was partially supported by an educational grant from MIS Implants Technologies Ltd.

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Plaque score change as an indicator for periimplant health in periodontal patients with immediately restored dental implants.

Patients with a history of periodontitis might have a higher risk for implant failure as compared with periodontally healthy subjects. The aim of the ...
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