The International Journal of Periodontics & Restorative Dentistry ...

The International Journal of Periodontics & Restorative Dentistry © 2018 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.

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Retrospective Evaluation of Factors Related to the Outcomes of Regenerative Therapy for Implants Affected by Peri-implantitis Stuart J. Froum, DDS1 Paul S. Rosen, DMD, MS2 Wendy C. W. Wang, BDS, MSc3 Scott H. Froum, DDS4 Shalin Vinayak, DDS5 The aim of this retrospective study was to examine the histories of 100 patients with 170 implants that were consecutively treated and reported in a previous study to identify which patient and implant factors might have affected the outcomes of therapy. Patient factors included history of periodontitis, hypertension, cardiac problems, rheumatoid arthritis, smoking, and penicillin allergy. Implant factors included whether the prosthesis was cemented or screw retained and initial bone loss (≤ 50% or > 50% of implant length). Frequency of maintenance visits (≤ 3 months or > 3 months) were recorded, as was patient age (≤ 60 years or > 60 years). On the patient level, only postoperative maintenance (≤ 3 months) showed a statistically significant effect on radiographic bone gain (RBG) compared to patients with > 3 months maintenance frequency. Nondiabetic patients showed a trend toward soft tissue gain. On an implant level, screw-retained prostheses demonstrated a statistically significant RBG compared to those with cement-retained prostheses. Significant favorable differences were seen in all outcomes when evaluating presurgical bone level loss (> 50% of the implant length). Further studies with larger groups of patients are necessary to substantiate the findings in this report. Int J Periodontics Restorative Dent 2018;38:181–187. doi: 10.11607/prd.3489

Adjunct Clinical Professor and Director of Clinical Research, Department of Periodontology and Implant Dentistry, New York University College of Dentistry, New York, New York, USA; Private Practice, New York, New York, USA. 2Clinical Professor of Periodontics, Department of Periodontology, Baltimore College of Dental Surgery, University of Maryland, Baltimore, Maryland, USA; Clinical Professor of Periodontics & Dental Implantology, Temple University Dental School, Philadelphia, Pennsylvania, USA; Private Practice, Yardley, Pennsylvania, USA. 3Fellow, Department of Periodontology and Implant Dentistry, New York University College of Dentistry, New York, New York, USA. 4Clinical Associate Professor in the Department of Periodontics at State University of New York at Stony Brook School of Dental Medicine, New York, New York, USA; Private Practice, New York, New York, USA. 5Resident, Department of Periodontology and Implant Dentistry, New York University College of Dentistry, New York, New York, USA. 1

Correspondence to: Dr Stuart J. Froum, 17 W 54th Street, Suite 1C/D, New York, NY 10019, USA. Fax: 212-246-7599. Email: [email protected] ©2018 by Quintessence Publishing Co Inc.

While high long-term survival rates of dental implants (> 90%) have been reported in the literature, many implants are still affected by biologic complications.1–3 One such complication is peri-implantitis, with reported prevalence rates at 10 years post–implant placement ranging from 10% to 43% of implants.4–6 Peri-implantitis has been defined as an inflammatory disease affecting the soft tissue surrounding an implant with bone loss that exceeds the extent seen with normal physiologic remodeling.7,8 Its primary etiology has been attributed to bacteria.9,10 Risk factors have been identified, including poor oral hygiene, a history of periodontitis, cigarette smoking, diabetes with poor metabolic control, alcohol consumption, genetic traits, and the implant surface.7 Emerging evidence suggests that the presence of retained subgingival cement be added to any list of risk factors.11 For the long-term maintenance of implants, it has been suggested that risk factors should be identified early and strategies employed to limit the development of periimplant diseases.12 Two recent systemic reviews on the treatment of peri-implantitis concluded that the available evidence does not allow any specific recommendations to be made and that there is a lack of high-quality

Volume 38, Number 2, 2018 © 2018 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.

182 comparative studies to support any one treatment over others.13,14 Decision trees and a prognosis system for peri-implant diseases have been proposed to guide clinicians toward predictable therapy based on the morphology of the hard tissue defect or the amount of peri-implant bone loss.15–17 In the later decision tree, implant prognoses in the algorithm varied from favorable (implant bone loss ≤ 25% of the implant length) to unfavorable or hopeless (implant bone loss > 50% of the implant length) based on the Froum and Rosen18 classification of disease severity with the Kwok and Caton19 system used to ascertain prognosis. According to this decision tree, the recommendation for treating dental implants with an unfavorable prognosis (bone loss > 50% of the implant length) was removal of the implant, site development, and subsequent replacement of the implant. This option often entails multiple surgeries, pain, morbidity, risk of complications, and tremendous cost overrides to the initial care, and results in a decreased implant success rate according to studies that have evaluated survival rates of replacement implants.20,21 In a recent systematic review and meta-analysis by Khoshkam et al,22 the authors concluded that there is limited evidence in the literature reporting long-term results of the regenerative approach and that this approach may be considered with other options for treatment, including implant removal.22 A more desirable option might focus on retaining an implant affected by peri-implantitis with moderate to se-

vere bone loss using a regenerative treatment approach, considering the time and expense involved with the explantation option to restore the patient back to health, comfort, and function. Positive predictability has been demonstrated with a regenerative protocol where 51 dental implants affected with peri-implantitis were consecutively treated and followed for 3 to 7.5 years.23 Most recently, the outcomes of the aforementioned successful regenerative treatment study were reported and expanded on, with 170 peri-implantitis–affected implants in 100 patients treated with this same regenerative approach.24 The outcomes continued to be positive for decrease in bleeding on probing (BoP) (91%), average probing depth (PD) reduction (5.03 mm), mean gain in radiographic bone levels (1.77 mm), and mean gain in marginal soft tissue levels (0.52 mm). During the follow-up period of 2 to 10 years, only 2 of the 170 treated implants were lost, yielding a 98.8% survival rate. The purpose of the present retrospective study was to examine the history of each of the 100 patients to identify the patient and implant factors, if any, that might have affected the outcomes of therapy.

Materials and Methods Charts were searched for 100 patients with 170 peri-implantitis– affected implants that were treated with a regenerative approach and reported on in a previous publication.24 The study was undertaken with Internal Review Board approval

under exempt status, since all data gleaned from these charts were reported anonymously with no identifiers. Although in the previous report the number of smokers and median patient age (and age range) at the time of treatment were reported, they were again documented in the present study as ≤ 60 years or > 60 years. This threshold was based on growth and development studies with year increments (ie, 41 to 50 years, 51 to 60 years, and ≥ 61 years, with the latter serving as the last group).25 Patient factors including a history of periodontitis, hypertension/cardiac problems, diabetes, rheumatoid arthritis, smoking, and penicillin allergy and implant factors including whether the prosthesis was cemented or screw-retained and initial bone loss ≤ 50% or > 50% of implant length were documented for all patients and reported. The frequency of postsurgical maintenance visits (≤ 3 months or > 3 months) was also recorded for each patient. Outcomes including posttreatment PD reduction, radiographic bone fill (RBF) of the defects and soft tissue marginal recession or gain were evaluated to determine if there were statistically significant correlations between any of these and the above-mentioned patient and implant factors. Methods used to determine these outcomes were described in previous papers.23,24,26 Each of the documented factors was evaluated to determine which were present in the total pool of patients. In addition, the clinical outcomes in millimeters of PD reduction, radiographic bone gain (RBG), and soft tissue gain (ST+) or loss (ST−) were


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Table 1 Effect of Patient Factors on Treatment Outcomes (Mean ± SD) Total population (n)

Total implants (n)

100 59 41 72 28 48 52 16 84 13 87 14 86 7 93 60

170 94 76 122 48 82 88 24 146 26 144 22 148 17 153 101

5.56 ± 1.94 5.81 ± 2.12 5.28 ± 1.74 5.54 ± 1.90 5.51 ± 2.07 5.43 ± 1.81 5.69 ± 2.07 5.91 ± 2.11 5.51 ± 1.92 6.11 ± 2.02 5.48 ± 1.93 5.95 ± 1.72 5.52 ± 2.00 7.19 ± 2.51 5.41 ± 1.79 5.55 ± 1.91

1.96 ± 1.79 2.45 ± 1.90 1.45 ± 1.48 2.1 ± 1.77 1.46 ± 1.55 1.48 ± 1.41 2.42 ± 2.00 1.91 ± 1.90 1.98 ± 1.79 2.34 ± 1.53 1.91 ± 1.83 2.30 ± 2.13 1.94 ± 1.76 1.28 ± 1.62 2.04 ± 1.82 2.34 ± 1.95**

0.58 ± 1.45 0.79 ± 1.38 0.39 ± 1.52 0.76 ± 1.43 0.11 ± 1.46 0.51 ± 1.43 0.66 ± 1.48 0.05 ± 1.13* 0.67 ± 1.48* 1.32 ± 1.25 0.49 ± 1.45 0.76 ± 1.46 0.56 ± 1.45 0.38 ± 1.20 0.59 ± 1.48 0.79 ± 1.52*

40

69

5.65 ± 2.00

1.41 ± 1.40**

0.29 ± 1.31**

Total number of patients Age ≤ 60 y Age > 60 y History of periodontal disease No history of periodontal disease Hypertension No hypertension Diabetics Nondiabetics Smoker Nonsmoker Penicillin allergy No penicillin allergy Rheumatoid arthritis No rheumatoid arthritis Frequency of postoperative visits ≤ 3 mo Frequency of postoperative visits > 3 mo

Probing depth Radiographic Soft tissue reduction (mm) bone gain (mm) gain/loss (mm)

*P = .08. **P ≤ .05.

Table 2 Effect of Implant Factors on Treatment Outcomes Total population (n)

Total implants (n)

83 17 25 75

144 26 48 122

Cemented restoration Screw-retained restoration > 50% preoperative bone loss ≤ 50% preoperative bone loss

Probing depth Radiographic Soft tissue reduction (mm) bone gain (mm) gain/loss (mm) 5.63 ± 1.79 5.12 ± 2.70 6.33 ± 2.38* 5.28 ± 1.69*

1.78 ± 1.70* 3.28 ± 2.07* 3.68 ± 1.95* 1.30 ± 1.19*

0.61 ± 1.47 0.40 ± 1.55 1.21 ± 1.68* 0.35 ± 1.29*

*P ≤ .05.

compared with the average outcomes of these factors in the general patient population. The follow-up time averaged 3.60 months (range 2 to 10 years) from the time of surgery for the 170 peri-implantitis–affected implants in the study.

Results On the patient level, only one factor had a statistically significant effect

on outcomes. Patients with more frequent postoperative maintenance care (≤ 3 months) demonstrated significantly greater radiographic bone gain compared to patients with less frequent maintenance care (> 3 months) (P = .02). There was a trend toward significance with soft tissue gain in patients with more frequent maintenance care (P = .08). Although no significant difference was found between diabetic and nondiabetic patients, a trend toward

significance was demonstrated in soft tissue gain in nondiabetic compared to diabetic patients (P = .08) (Table 1). On the implant level, clinical outcomes showed statistically significant differences between cement- vs screw-retained restorations and initial bone loss around the implant (Table 2). Implants with screw-retained prostheses demonstrated significant RBG compared to those with cement-retained


184 Fig 1 (left) Patient presented with 10 to 12-mm probing depths, bleeding on light probing, purulent exudate, and radiographic bone loss. Fig 2 (right) Radiograph of the maxillary right lateral incisor implant.

Fig 3 Clinical view of the horizontal bone defect following flap reflection and implant surface decontamination. Note bone loss on the teeth adjacent to the implant.

prostheses (P = .03). Of the 170 implants treated, 48 (28.2%) had bone loss that exceeded 50% of the implant lenth. Significant differences were noted in all three outcomes in evaluating preoperative bone levels. Preoperative defects with > 50% bone loss showed significantly greater PD reduction (P = .01), RBG (P < .001), and soft tissue gain (P = .05) compared to preoperative defects with ≤ 50% bone loss. Although defect morphology has been suggested as a guide to determine treatment in one decision tree,15 in the present study more than half of the defects treated would be classified as one-wall or no-wall defects27 (Figs 1 to 9). Of the two implants lost, one had a pretreatment bone loss of < 50% while the other had bone loss of approximately 60%.

Discussion

Fig 4 Collagen membrane barrier tacked and contoured to cover the bone graft buccally and interproximally.

Fig 5 Flap repositioned and sutured.

In the present study of treatment outcome risk factors, only history of periodontal disease, age (≤ 60 years), and cementretained restorations were evident in more than 50% of the patients treated. A history of periodontitis and cigarette smoking have been identified as risk factors for peri-implant disease in two comprehensive reviews on indicators.28,29 These factors were also found to be significant for increased severity of peri-implantitis.30 In the present study, 72% of the patients treated had a history of periodontal disease. However, this data may have been biased since all three study authors are periodontists and may have seen patients specifically referred for periodontal disease after developing peri-implantitis. One publication has suggested that subjects with diabetes were more prone to develop peri-implantitis.31 However, the present study could not further validate this as one of its limitations was that the number of patients with known


185

Fig 6 Probing 14 months postoperative. Residual probing depth and defect

Fig 7 Bone fill was evident following flap reflection, but the residual defect was treated with a second regenerative procedure.

Fig 8 (left) Radiograph 4.5 years after the second procedure. The crown that had been cemented with temporary cement was removed. Fig 9 (right) Clinical view of the final implant-supported restoration 4.5 years posttreatment.

risk factors was small (ie, diabetes [n = 16], rheumatoid arthritis [n = 7], smokers [n = 13]). Moreover, each patient received comprehensive periodontal treatment and home care instruction prior to surgery for peri-implantitis. These factors did not allow an evaluation of the effects of biofilm, smoking, diabetes, rheumatoid arthritis, and poor oral hygiene as risk indicators in the population included. An additional risk factor evaluated in the present study should be noted. To date, there has been little or no mention of hypertension (controlled) as a risk factor for peri-

implantitis. However, in the present study 48% of the patients presented for treatment with a history of cardiovascular disease (CV) and hypertension. Renvert et al32 found an odds ratio (OR) of 8.7 (95% CI: 1.9, 40.3; P < .006) for the association of cardiovascular disease with peri-implantitis, which exceeded the OR for periodontitis of 4.5 (95% CI: 2.1, 9.7; P < .001). The findings in the present study regarding a possible comorbidity between peri-implantitis and CV/hypertension and those suggested by Renvert et al32 seem to suggest the need for additional studies. Moreover, it appears that

the effect of CV/hypertension on peri-implantitis may be transcendent as the patients in the present study were controlled in their disease and had received medical clearance prior to all care. This possible link should be evaluated in future studies. At the patient level, diabetes demonstrated a trend toward a statistically significant effect on the soft tissue outcomes. This was seen in greater gain in soft tissue levels following the regenerative protocol used in the present study. While two comprehensive reviews, one in humans and the second in animals and


186 humans, suggested that diabetes was not a contraindication for implant placement, an impaired healing response was noted in diabetic animals compared with nondiabetic controls.33,34 Although bone level change (RBG) and PD reduction were not statistically different in patients with diabetes in the present study, the level of soft tissue healing appeared to be affected following the regenerative protocol, showing less gain in soft tissue height compared to nondiabetic patients. A prospective study on 27 patients with 149 implants treated for peri-implantitis reported stable PD reduction at the 5-year follow-up in patients with a high standard of oral hygiene who were recalled every 6 months.35 In the present study, patients with a postoperative maintenance visit interval of < 3 months demonstrated statistically significant improved bone level outcomes compared to the overall cohort as well as the > 3 months recall interval results. In this tightly maintained group, improved soft tissue healing (less marginal recession) also demonstrated a trend toward statistical significance. These trends seem to suggest that more frequent maintenance and monitoring posttreatment may be a factor in maintaining positive outcomes.36 Moreover, a narrative review of the literature on the effect on maintenance following peri-implantitis treatment concluded that individuals on regular maintenance are less likely to develop peri-implantitis and that successful treatment of periodontitis prior to implant placement lowers the risk of peri-implantitis.37 Finally, when

looking at outcomes according to the age of the patient (≤ 60 years or > 60 years), no significant differences were seen in the three parameters evaluated. Thus, a decision on whether to save an implant (with a regenerative protocol) or remove it should not be based on patient age. On an implant level, 84.7% of the restored peri-implantitisaffected implants were cementretained. The presence or absence of excess cement was not documented in the present study, but the potential of excess cement to be a risk factor and its prevention has been discussed in other publications.38,39 The statistically significant difference in RBG found in the present study would seem to imply better treatment outcomes for periimplantitis with screw-retained restorations. The finding that implants with > 50% initial bone loss showed statistically significant better outcomes for PD reduction, RBG, and ST gain when compared to defects with ≤ 50% bone loss should be further studied in light of decision trees recommending implant removal in this category.16,17 The fact that 47 of 48 implants with > 50% bone loss were successfully retained should inform clinical decisions on whether to remove implants with advanced periimplantitis. This too requires further study. In two recent meta-analyses and systemic reviews of regenerative treatment for peri-implantitis, types of bone graft and use or nonuse of membrane barriers were correlated with outcomes but initial bone loss around these implants was not related to outcomes.22,40

Conclusions The present evaluation of a successfully treated group of patients with peri-implantitis using a specific regenerative protocol suggests that more frequent maintenance, cement- rather than screw-retained restorations, and preoperative bone loss > 50% of implant length affected treatment outcomes. Further studies with larger groups of patients are necessary to substantiate these findings.

Acknowledgments The authors would like to thank Dr Malvin N. Janal, faculty at Department of Epidemiology and Health Promotion, for his assistance in the preparation of the statistics shown in this manuscript. The authors reported no conflicts of interest related to this study.

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