Secondary Logo

Journal Logo

Consensus

Surgical Treatment of Periimplantitis With Augmentative Techniques

Ramanauskaite, Ausra DDS*; Obreja, Karina DDS, Dr. med.dent.; Sader, Robert Prof., Dr.med.dent.mult; Khoury, Fouad DDS; Dr. med. dent, PhD§; Romanos, Georgios DDS, Dr. med.dent., PhD; Tae Koo, Ki DDS, MS, PhD#; Keeve, Philip Leander DMD, Dr. med.dent**; Sculean, Anton DMD, Dr. med. dent, MS, PhD††; Schwarz, Frank Prof., Dr. med. dent.‡‡

Author Information
doi: 10.1097/ID.0000000000000839
  • Free

Abstract

The diagnosis of periimplantitis describes a pathological condition occurring in tissues around dental implants, characterized by inflammation in the periimplant connective tissue and the progressive loss of supportive bone.1 As substantial evidence supports the bacterial etiology of periimplantitis,2 the treatment of the disease should include anti-infective measures.

Based on the current evidence, nonsurgical treatments, including mechanical debridement with or without adjunctive (ie, local antibiotics, antimicrobial photodynamic therapy) or alternative measures (eg, air abrasive devices, Er:YAG laser monotherapy), have demonstrated limited efficacy for the management of periimplantitis and were particularly compromised at advanced defect sites.3,4 These findings may be mainly attributed to the limit access of nonsurgical measures to advanced pockets and the inability to completely remove bacterial deposits from structured implant surfaces.

In contrast, surgical interventions have been shown to improve the efficacy of periimplantitis treatment.4 They provide better access to the periimplant defect, which, in turn, allows for a more effective implant surface decontamination.4 Although nonaugmentative surgical treatment approaches including open-flap debridement (OFD) alone or with adjunctive resective therapy (eg, pocket elimination, bone recontouring, and implantoplasty) primarily aims at resolving inflammation and arresting the further progression of the disease, augmentative treatments additionally seek to reconstruct the osseous defect compartment.5

Numerous augmentation protocols using various methods for surface decontamination, along with autogenous bone and various bone replacement materials with or without barrier membranes, have been proposed for the management of periimplantitis. Until now, it remains difficult to draw conclusions concerning which augmentative protocol is superior as well as to evaluate its clinical efficacy over nonaugmentative treatments.6,7

Therefore, the aim of the present review is to evaluate the existing evidence regarding the effectiveness of surgical augmentative therapy for periimplantitis management and to compare it with nonaugmentative therapy alone.

Materials and Methods

The reporting of this systematic analysis adhered to the Preferred Reporting Items for Systematic Review and Meta-Analyses (PRISMA) statement.8

Focus Questions

The following questions were developed according to the population, intervention, comparison, and outcome (PICO) study design:

“In patients with osseointegrated implants diagnosed with periimplantitis, what are the clinical and radiographic outcomes of augmentative surgical interventions compared with nonaugmentative surgical measures?”

Population: Patients diagnosed with periimplantitis based on case definitions used in respective publications;

Intervention: Surgical augmentative periimplantitis measures;

Comparison: Surgical nonaugmentative measures.

Outcomes: primary: changes in clinical parameters (ie, bleeding on probing [BOP %] and periimplant probing depth [PD {mm}]; secondary: radiographic defect fill [%] and/or defect reduction (mm).

Search Strategy

A literature search was performed in MEDLINE through the PubMed database of the US National Library of Medicine, for articles published until January 1, 2018. The combination of Medical Subject Heading search terms (ie, MeSH) and free-text terms included:

“peri-implant disease” OR “periimplant disease” OR “peri-implant infection” OR “periimplant infection” OR “peri-implantitis” OR “Periimplantitis (MeSH)”

AND

“treatment” OR “surgical treatment” OR “regenerative treatment” OR “augmentative treatment” OR “augmentative therapy” OR “surgical therapy” OR “regenerative therapy” OR “reconstructive treatment” OR “reconstructive therapy” OR “augmentative therapy” OR “augmentative treatment”.

Selection of Studies

Two independent reviewers (A.R. and K.O.) conducted the literature search. Disagreements regarding inclusion during the first and second stages of the study selection were resolved by discussion.

During the first stage of study selection, the titles and abstracts were screened and evaluated according to the following inclusion criteria:

  1. Prospective, randomized, controlled clinical trials (RCTs), case-control studies, prospective cohort studies, cross-sectional studies, and case series in humans reporting changes in clinical parameters (ie, BOP and PD), and/or presenting radiographic data (defect reduction [mm] and/or defect fill) after surgical augmentative treatment and/or comparing augmentative and nonaugmentative surgical approaches with a follow-up of at least 3 months;
  2. Studies that include patients with at least one osseointegrated implant affected by periimplantitis;
  3. Studies describing the definition of periimplantitis;
  4. Studies presenting a surgical augmentative intervention aimed at the treatment of periimplantitis;
  5. Publications in English language in an international, peer-reviewed journal.

At the second stage of selection, all full-text articles identified during the first stage were acquired and evaluated according to the following exclusion criteria:

  1. Review papers, case reports, letters, editorials, and abstracts on in vitro and animal studies;
  2. Studies not providing data on clinical and/or radiographic data or treatment protocols;
  3. Studies not providing a definition of periimplantitis;
  4. Studies published not in international peer-reviewed journal.

The initial electronic search resulted in the identification of 1218 titles (Fig. 1). At the first stage, 1187 publications were excluded based on the title and abstract. At the second stage, the remaining 31 full-text articles were evaluated. The reasons for excluding studies after full-text assessment were as follows: retrospective studies,8,9 nonaugmentative surgical treatment was performed (n = 4),10–13 and information on the augmentation protocol was lacking (n = 1).14 Finally, 24 studies were identified for inclusion in the review.

Fig. 1
Fig. 1:
The flowchart presenting literature search.

Data Collection

Data extraction templates were used to retrieve general information on the study design, periimplantitis case definitions, follow-up periods, number of implants and patients, implant type, patient sex, age, and smoking status (Tables 1 and 2). The treatment methods applied in the test and control groups, the mode of healing (ie, submerged or nonsubmerged), information on the use of systemic antibiotics, and clinical and/or radiographic treatment outcomes are presented in Tables 3 and 4. The mean values and SDs of BOP, PD values, radiographic bone defect fill, or defect reduction after the respective treatment were extracted for the data analysis.

Table 1-a
Table 1-a:
Study and Patient Characteristics: Comparative Studies
Table 1-b
Table 1-b:
Study and Patient Characteristics: Comparative Studies
Table 1-c
Table 1-c:
Study and Patient Characteristics: Comparative Studies
Table 2-a
Table 2-a:
Study and Patient Characteristics: Observational Studies
Table 2-b
Table 2-b:
Study and Patient Characteristics: Observational Studies
Table 3-a
Table 3-a:
Treatment Protocols, Outcomes, and Complications: Comparative Studies
Table 3-b
Table 3-b:
Treatment Protocols, Outcomes, and Complications: Comparative Studies
Table 3-c
Table 3-c:
Treatment Protocols, Outcomes, and Complications: Comparative Studies
Table 3-d
Table 3-d:
Treatment Protocols, Outcomes, and Complications: Comparative Studies
Table 3-e
Table 3-e:
Treatment Protocols, Outcomes, and Complications: Comparative Studies
Table 3
Table 3:
f. Treatment Protocols, Outcomes, and Complications: Comparative Studies
Table 3
Table 3:
g. Treatment Protocols, Outcomes, and Complications: Comparative Studies
Table 4-a
Table 4-a:
Treatment Protocols, Outcomes and Complications: Observational Studies
Table 4-b
Table 4-b:
Treatment Protocols, Outcomes and Complications: Observational Studies
Table 4-c
Table 4-c:
Treatment Protocols, Outcomes and Complications: Observational Studies
Table 4-d
Table 4-d:
Treatment Protocols, Outcomes and Complications: Observational Studies

Information on further disease progression/treatment complications and treatment success based on the criteria that the authors used is presented in Tables 3–5.

Table 5
Table 5:
Success of the Surgical Augmentative Treatment Indicated in the Studies

Quality Assessment

The Cochrane Collaboration's tool for assessing risk of bias was used in the case of controlled clinical trials.15 Methodological quality assessment of the observational studies was based on the Newcastle-Ottawa Quality Assessment Scale for Cohort studies16 (Table 6 and 7).

Table 6
Table 6:
Assessment of the Risk of Bias for Included Controlled Clinical Studies
Table 7
Table 7:
Assessment of the Risk of Bias for Included Observational Studies

Data Synthesis

Due to the heterogeneity among the studies regarding study designs, treatment protocols applied, and outcome variables, no quantitative analysis was performed.

Results

Presented in Tables 1–4 are 13 comparative and 11 observational clinical studies that reported on the surgical treatment of periimplantitis by using augmentative therapies. The follow-up time ranged from 6 months to 7 years for comparative studies and from 6 months to up to 2 to 1017 years for observational studies. Out of the 12 comparative clinical studies included, 7 appeared to be randomized controlled clinical trials.18–23 All controlled clinical studies were judged to have high to unclear risk of bias (Table 6). The included observational studies scored between 5 and 7 stars (out of 9) based on the Newcastle-Ottawa Scale (Table 7).

Patient Characteristics

Five hundred and ninety patients were treated with the augmentative surgical approach. The mean age of the patients ranged from 45.36 to 70.1 years. Seventeen studies (10 controlled and 7 observational studies) reported on the smoking statuses of the patients. Particularly, although one observational study included only nonsmoking patients,24 5 investigations (3 controlled23,25,26 and 2 observational27,28) involved both nonsmokers and light smokers (<10 cig./d). In the rest of the controlled and observational studies, the number of smokers ranged from 23.3% to 76.9%, and from 15% to 66.7%, respectively (Tables 1 and 2).

Implant Characteristics

In total, 840 implants of various surfaces (379 in controlled and 417 in observational studies) were included in the review. Although the majority of the implants had moderately rough surfaces (5 controlled18–20,22,25 and 5 observational24,27,29–31 studies), 2 studies were conducted with smooth-surface implants (one observational32 and one comparative study33), and 3 studies (one comparative34 and 2 observational35,36 studies) focused on rough-surface implants only. Seven investigations included both smooth, rough, and moderately rough,21,23,26,28,37 or rough and moderately rough38,39 implants. Two observational studies did not provide information on the surfaces of the implants.17,40

Case Definitions

Definitions of the periimplantitis cases selected for the augmentative treatment varied widely among the included studies (Tables 1–4). Except for the 2 studies, where periimplantitis diagnosis was based only on radiographical evaluation,34,40 the rest of the investigations defined periimplantitis by the presence of BOP and/or PD >5 mm, and radiographic bone loss. In addition, the majority of the cases presented intrabony periimplant defect configurations.18–23,25–29,31,33–40

Comparison of Augmentative and Nonaugmentative Approaches

Three RCTs assessed the clinical efficacy of augmentative therapy over the OFD approach alone.18–20 Two studies included the same patient sample and reported the treatment outcomes at 12 months and 7 years of follow-up.18,19 At 12 months after the treatment, two 1-year clinical investigations demonstrated a significantly higher percentage of radiographic fill of the intrabony defect treated with titanium granules when compared to nonaugmentative treatment.18,20 However, the clinical treatment outcomes, in terms of PD and BOP reduction, did not differ between the 2 treatment approaches at both 12-month and 7-year follow-up.18–20 In the 7-year investigation, due to the small number of the patients (6 test and 6 control), statistical analysis between the groups was not performed.19 Nevertheless, the results indicated a minimal difference in osseous defect depth changes between the groups.19

Characteristics of Interventions

Decontamination

Methods to decontaminate the implant surface included mechanical,17,20,21,23–25,30,35,37,39 chemical,17–19,22,31–34,38,40 laser therapy,21,26,28,29,39 or their combinations (Tables 3 and 4). In addition, one comparative and 3 observational studies, in adjunct to mechanical,21,27,28 air-powder abrasive,30 or laser (Er:YAG)21 decontamination methods, involved the performance of implantoplasty to supracrestally and buccally exposed implant parts.

Comparative studies

When considering the effectiveness of different implant surface decontamination protocols after augmentative periimplantitis surgery, Deppe et al39 did not find a difference between the use of a carbon dioxide laser and air polishing on a long-term basis (5 years) in terms of the clinical attachment, PD, and radiographic marginal bone level changes. Moreover, clinical outcomes (eg, clinical attachment gain and BOP reduction) obtained by using laser decontamination (Er:YAG) were comparable with the conventional decontamination (plastic curettes + cotton pellets soaked in saline) approaches as demonstrated in the findings of the 7-year investigation.21

Augmentation protocols

Bone substitutes alone

Four observational24,31,35,40 and one controlled clinical study38 reported on augmentative periimplantitis treatment using bone substitute materials without a barrier membrane. Besides, 3 comparative studies included control groups treated with bone filler alone.23,33,34 A variety of bone replacement materials were applied (autogenous bone,34,35 alloplastic bone filler,23 and xenograft24,31,33,38). Moreover, in 4 controlled clinical studies, intrabony periimplant defects were filled using titanium granules.18–20,25

Guided bone regeneration

The guided bone regeneration concept including the application of a bone substitute material and a barrier membrane was performed in 7 observational17,27–30,32,36 and 8 comparative studies.21–23,25,26,33,34,39 Resorbable17,21–23,25–30,32–34 and nonresorbable34,36,39 membranes were used. In addition to the use of a collagen membrane, in one observational study, connective tissue graft was placed on the buccal aspect of the implant, which at the 6-month follow-up was associated with minimal mucosal height changes.28

Addition of biologically active materials

Addition of biologically active materials were applied in 2 observational (enamel matrix derivative [EMD] or platelet-derived growth factor,17 and xenograft containing native bone morphogenetic protein and vascular endothelial growth factor40) and 2 controlled clinical trials (platelet-rich fibrin [PRF] membranes25 and EMD37). In addition, one observational study used allogenic bone substitutes impregnated in antibiotics.27

Comparative studies
Type of bone filler

Surgical treatment outcomes using different bone filler materials were compared in the 3 clinical studies.22,23,25 Accordingly, after 12 months of healing, significantly higher radiographic bone level gain and mean BOP and PD reduction were obtained with the use of xenograft in comparison to autogenous bone.22 However, when interpreting these results it should be taken into consideration that xenogenic bone is more radiopaque than autogenolus bone. Furthermore, improved clinical outcomes, in terms of BOP and PD reduction, were noted for slowly resorbing bovine-derived minerals over hydroxyapatite particles.23 Increased radiographic bone defect fill was detected in the sites treated with the porous titanium granules compared to xenograft, while the clinical outcomes (ie, PD reduction and clinical attachment changes [CAL]) did not differ between the groups.25

Adjunctive use of barrier membrane

Augmentative periimplantitis treatments with and without a barrier membrane were evaluated in 3 comparative studies.23,33,34 The mean radiographic fill of an intrabony defect obtained by the use of autogenous bone and a nonresorbable membrane was indicated to be 2.8 mm, followed by the use of autogenous bone alone (2.4 mm), and amounted to 1.1 mm when autogenous bone particles were applied in conjunction with a resorbable membrane.34 The comparison among the 3 investigated groups did not reach a significant difference.34 These findings corroborate the data presented in the 5-year investigation, where the additional use of a resorbable membrane did not improve the treatment outcome.33 On the contrary, a 4-year clinical study revealed better clinical outcomes when a combination of bone-grafting material and a membrane were used in comparison to the use of grafting material alone.23

Addition of biologically active materials

The results of RCT, that attempted to evaluate the effect of EMD for the management of periimplantitis compared to OFD, showed that the use of EMD did not result in improved PD and BOP after 12 months, but was associated with increased marginal bone level and increased prevalence of Gram +/aerobic bacteria.37

Healing Mode and Systemic Antibiotics

Submerged postoperative healing was performed in 4 controlled18,19,34,39 and 2 observational studies.32,36 One observational study included both healing modes.29

Systemic antibiotics were prescribed in 15 studies, except 5 controlled21,23,26,37,39 and 3 observational studies.17,29,40 Preoperative prophylactic antibiotics were used in one observational study.40 None of the included studies compared neither the potential influence of modes of healing (ie, nonsubmerged vs submerged) nor the effect of additional systemic antibiotics after periimplantitis augmentative therapy.

Clinical and Radiographic Treatment Outcomes

Augmentative periimplantitis therapy was shown to result in significant improvements in BOP20–23,26–28,30,31,38 and PD values18,20–31,33,34,38 in comparison to the baseline. In particular, the mean BOP reduction ranged from 25.9%25 to 89.99%21 and 91%17 in 1- to 7-year period, and the mean PD reduction ranged from 0.7421 to 5.4 mm.34

The reported mean radiographic fill of the intrabony defect ranged between 57%18 and 93.3%.30 In addition, the radiographic reduction of the intrabony defect height varied from 0.222 and 2.8 mm,34 up to 3.7035 and 3.77 mm.27

Success of Augmentative Therapy

Composite outcomes for the treatment success were indicated in 5 of the studies (Table 5). Depending on the criteria that was applied, treatment success ranged between 11% and 38.5% of the implants in a 1-year period20,22 and between 14.3% 38 and 66.7%33 of the implants, and 60% of the patients,21 in the long-term investigations (5–7 years).

Further Disease Progression and Other Complications

Despite the successful clinical and radiographic clinical performance of augmentative therapies, cases of implant loss, disease recurrence, and further progression were reported17–19,21,23,31,33,35,37–40 (Tables 3 and 4). Exposure of the barrier membrane (nonresorbable34,36 and resorbable25,30,32), fistula, or sequester formation were reported in 58.6% of the cases when barrier membrane (resorbable and nonresorbable) was used.34.

Factors Influencing Augmentative Treatment Outcomes

The clinical outcomes of surgical augmentative therapy were reported to be influenced by the implant surface characteristics,38 as well as by the periimplant defect configuration.26 Particularly, moderately rough surface implants demonstrated superior clinical treatment outcomes in comparison to rough surface implants,38 and circumferential-type defects were shown to perform in a superior manner in conjunction with a dehiscence-type defect.26

Conclusions/Recommendations

  • Surgical augmentative periimplantitis therapy resulted in improved clinical and radiographic treatment outcomes compared to the baseline in the majority of studies with 6 months to 7 to 10 years of follow-up.
  • Augmentative surgical techniques with the application of the titanium granules did not demonstrate superior clinical treatment outcomes when compared to a nonaugmentative approach (3 RCTs).
  • There is no evidence to support the superiority of a specific material, product, or membrane in terms of long-term clinical treatment benefits.
  • The method of implant surface decontamination did not influence the clinical outcomes of surgical augmentative periimplantitis therapy (1 RCT and 1 controlled comparative study).
  • Clinical augmentative treatment outcomes were shown to be influenced by factors such as periimplant bone defect morphology and implant surface characteristics (2 controlled clinical studies).
  • Due to the lack of comparative studies, no clinical recommendations can be given for the mode of healing (ie, nonsubmerged vs submerged) as well as for the adjunctive use of systemic antibiotics.
  • Periimplantitis recurrence requiring retreatment or leading to implant loss was reported.

Disclosure

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

Roles/Contributions by Authors

A. Ramanauskaite made substantial contribution to the data collection, conception, and interpretation of data as well as manuscript writing. K. Obreja contributed to the data collection, interpretation and data discussion. R. Sader contributed to critical evaluation of the manuscript and data discussion. F. Khoury contributed to critical evaluation of the manuscript and data discussion. G. Romanos contributed to critical evaluation of the manuscript and data discussion. K. T. Koo contributed to critical evaluation of the manuscript and data discussion. P. L. Keeve contributed to critical evaluation of the manuscript and data discussion. A. Sculean contributed to critical evaluation of the manuscript and data discussion. S. Frank made substantial contribution to the interpretation of data and manuscript writing.

Acknowledgments

Ausra Ramanauskaite and Karina Obreja equally contributed to the present work and share the first authorship.

References

1. Schwarz F, Derks J, Monje A, et al. Peri-implant diseases and conditions: Peri-implantitis. J Periodontol. 2018 [epub ahead of print].
2. Lang NP, Berglundh T. Periimplant diseases: Where are we now? Consensus of the seventh European Workshop on Periodontology. J Clin Periodontol. 2011;38:178–181.
3. Klinge B, Meyle J. Peri-implant tissue destruction. The third EAO consensus conference 2012. Clin Oral Implants Res. 2012;23:108–110.
4. Schwarz F, Schmucker A, Becker J. Efficacy of alternative or adjunctive measures to conventional treatment of peri-implant mucositis and peri-implantitis: A systematic review and meta-analysis. Int J Implant Dent. 2015;1:22–56.
5. Renvert S, Polyzois IN. Clinical approaches to treat peri-implant mucositis and peri-implantitis. Periodontol 2000. 2015;68:369–404.
6. Khoshkam V, Chan HL, Lin GH, et al. Reconstructive procedures for treating peri-implantitis: A systematic review. J Dent Res. 2013;92:131s–138s.
7. Esposito M, Grusovin MG, Worthington HV. Interventions for replacing missing teeth: Treatment of peri-implantitis. Cochrane Database Syst Rev. 2012;1:Cd004970.
8. Mijiritsky E, Yatzkaier G, Mazor Z, et al. The use of porous titanium granules for treatment of peri-implantitis lesions: Preliminary clinical and radiographic results in humans. Br Dent J. 2013;214:E13.
9. Lagervall M, Jansson LE. Treatment outcome in patients with peri-implantitis in a periodontal clinic: A retrospective study. J Periodontol. 2013;84:1365–1373.
10. Serino G, Turri A. Outcome of surgical treatment of peri-implantitis: Results from a 2-year prospective clinical study in humans. Clin Oral Implants Res. 2011;22:1214–1220.
11. De Angelis N, Felice P, Grusovin MG, et al. The effectiveness of adjunctive light-activated disinfection (LAD) in the treatment of peri-implantitis: 4-month results from a multicentre pragmatic randomised controlled trial. Eur J Oral Implantol. 2012;5:321–331.
12. Carcuac O, Derks J, Abrahamsson I, et al. Surgical treatment of peri-implantitis. 3-year results from a randomized controlled clinical trial. J Clin Periodontol. 2017;44:1294–1303.
13. Toma S, Lasserre JF, Taieb J, et al. Evaluation of an air-abrasive device with amino acid glycine-powder during surgical treatment of peri-implantitis. Quintessence Int. 2014;45:209–219.
14. Caccianiga G, Rey G, Baldoni M, et al. Clinical, radiographic and microbiological evaluation of high level laser therapy, a new photodynamic therapy protocol, in peri-implantitis treatment; a Pilot Experience. Biomed Res Int. 2016;2016:6321906.
15. Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. J Clin Epidemiol. 2009;62:1006–1012.
16. Wells GA, Schea B, O'Connell D, et al The Newcastle—Ottawa Scale (NOS) for Assessing the Quality of Nonrandomized Studies in Meta-analyses; 2009. Available at: http://wwwohrica/programs/clinical_epidemiology/oxfordhtm.
17. Froum SJ, Froum SH, Rosen PS. A regenerative approach to the successful treatment of peri-implantitis: A consecutive series of 170 implants in 100 patients with 2- to 10-year follow-up. Int J Periodontics Restorative Dent. 2015;35:857–863.
18. Wohlfahrt JC, Lyngstadaas SP, Ronold HJ, et al. Porous titanium granules in the surgical treatment of peri-implant osseous defects: A randomized clinical trial. Int J Oral Maxillofac Implants. 2012;27:401–410.
19. Andersen H, Aass AM, Wohlfahrt JC. Porous titanium granules in the treatment of peri-implant osseous defects-a 7-year follow-up study. Int J Implant Dent. 2017;3:50–57.
20. Jepsen K, Jepsen S, Laine ML, et al. Reconstruction of peri-implant osseous defects: A multicenter randomized trial. J Dent Res. 2016;95:58–66.
21. Schwarz F, John G, Schmucker A, et al. Combined surgical therapy of advanced peri-implantitis evaluating two methods of surface decontamination: A 7-year follow-up observation. J Clin Periodontol. 2017;44:337–342.
22. Aghazadeh A, Rutger Persson G, Renvert S. A single-centre randomized controlled clinical trial on the adjunct treatment of intra-bony defects with autogenous bone or a xenograft: Results after 12 months. J Clin Periodontol. 2012;39:666–673.
23. Schwarz F, Sahm N, Bieling K, et al. Surgical regenerative treatment of peri-implantitis lesions using a nanocrystalline hydroxyapatite or a natural bone mineral in combination with a collagen membrane: A four-year clinical follow-up report. J Clin Periodontol. 2009;36:807–814.
24. Rotenberg SA, Steiner R, Tatakis DN. Collagen-coated bovine bone in peri-implantitis defects: A Pilot study on a novel approach. Int J Oral Maxillofac Implants. 2016;31:701–707.
25. Guler B, Uraz A, Yalim M, et al. The comparison of porous titanium granule and xenograft in the surgical treatment of peri-implantitis: A prospective clinical study. Clin Implant Dent Relat Res. 2017;19:316–327.
26. Schwarz F, Sahm N, Schwarz K, et al. Impact of defect configuration on the clinical outcome following surgical regenerative therapy of peri-implantitis. J Clin Periodontol. 2010;37:449–455.
27. Nart J, de Tapia B, Pujol A, et al. Vancomycin and tobramycin impregnated mineralized allograft for the surgical regenerative treatment of peri-implantitis: A 1-year follow-up case series. Clin Oral Investig. 2017;22:2199–2207.
28. Schwarz F, Sahm N, Becker J. Combined surgical therapy of advanced peri-implantitis lesions with concomitant soft tissue volume augmentation. A case series. Clin Oral Implants Res. 2014;25:132–136.
29. Romanos GE, Nentwig GH. Regenerative therapy of deep peri-implant infrabony defects after CO2 laser implant surface decontamination. Int J Periodontics Restorative Dent. 2008;28:245–255.
30. Matarasso S, Iorio Siciliano V, Aglietta M, et al. Clinical and radiographic outcomes of a combined resective and regenerative approach in the treatment of peri-implantitis: A prospective case series. Clin Oral Implants Res. 2014;25:761–767.
31. Roccuzzo M, Gaudioso L, Lungo M, et al. Surgical therapy of single peri-implantitis intrabony defects, by means of deproteinized bovine bone mineral with 10% collagen. J Clin Periodontol. 2016;43:311–318.
32. Roos-Jansaker AM, Renvert H, Lindahl C, et al. Submerged healing following surgical treatment of peri-implantitis: A case series. J Clin Periodontol. 2007;34:723–727.
33. Roos-Jansaker AM, Persson GR, Lindahl C, et al. Surgical treatment of peri-implantitis using a bone substitute with or without a resorbable membrane: A 5-year follow-up. J Clin Periodontol. 2014;41:1108–1114.
34. Khoury F, Buchmann R. Surgical therapy of peri-implant disease: A 3-year follow-up study of cases treated with 3 different techniques of bone regeneration. J Periodontol. 2001;72:1498–1508.
35. Behneke A, Behneke N, d'Hoedt B. Treatment of peri-implantitis defects with autogenous bone grafts: Six-month to 3-year results of a prospective study in 17 patients. Int J Oral Maxillofac Implants. 2000;15:125–138.
36. Haas R, Baron M, Dortbudak O, et al. Lethal photosensitization, autogenous bone, and e-PTFE membrane for the treatment of peri-implantitis: Preliminary results. Int J Oral Maxillofac Implants. 2000;15:374–382.
37. Isehed C, Holmlund A, Renvert S, et al. Effectiveness of enamel matrix derivative on the clinical and microbiological outcomes following surgical regenerative treatment of peri-implantitis: A randomized controlled trial. J Clin Periodontol. 2016;43:863–873.
38. Roccuzzo M, Pittoni D, Roccuzzo A, et al. Surgical treatment of peri-implantitis intrabony lesions by means of deproteinized bovine bone mineral with 10% collagen: 7-year-results. Clin Oral Implants Res. 2017;28:1577–1583.
39. Deppe H, Horch HH, Neff A. Conventional versus CO2 laser-assisted treatment of peri-implant defects with the concomitant use of pure-phase beta-tricalcium phosphate: A 5-year clinical report. Int J Oral Maxillofac Implants. 2007;22:79–86.
40. Wiltfang J, Zernial O, Behrens E, et al. Regenerative treatment of peri-implantitis bone defects with a combination of autologous bone and a demineralized xenogenic bone graft: A series of 36 defects. Clin Implant Dent Relat Res. 2012;14:421–427.
41. Schwarz F, Sculean A, Bieling K, et al. Two-year clinical results following treatment of peri-implantitis lesions using a nanocrystalline hydroxyapatite or a natural bone mineral in combination with a collagen membrane. J Clin Periodontol. 2008;35:80–87.
42. Schwarz F, Bieling K, Latz T, et al. Healing of intrabony peri-implantitis defects following application of a nanocrystalline hydroxyapatite (Ostim) or a bovine-derived xenograft (Bio-Oss) in combination with a collagen membrane (Bio-Gide). A case series. J Clin Periodontol. 2006;33:491–499.
43. Roos-Jansaker AM, Lindahl C, Persson GR, et al. Long-term stability of surgical bone regenerative procedures of peri-implantitis lesions in a prospective case-control study over 3 years. J Clin Periodontol. 2011;38:590–597.
44. Schwarz F, Hegewald A, John G, et al. Four-year follow-up of combined surgical therapy of advanced peri-implantitis evaluating two methods of surface decontamination. J Clin Periodontol. 2013;40:962–967.
45. Schwarz F, John G, Mainusch S, et al. Combined surgical therapy of peri-implantitis evaluating two methods of surface debridement and decontamination. A two-year clinical follow up report. J Clin Periodontol. 2012;39:789–797.
46. Schwarz F, Sahm N, Iglhaut G, et al. Impact of the method of surface debridement and decontamination on the clinical outcome following combined surgical therapy of peri-implantitis: A randomized controlled clinical study. J Clin Periodontol. 2011;38:276–284.
47. Roccuzzo M, Bonino F, Bonino L, et al. Surgical therapy of peri-implantitis lesions by means of a bovine-derived xenograft: Comparative results of a prospective study on two different implant surfaces. J Clin Periodontol. 2011;38:738–745.
Keywords:

periimplant disease; regeneration; management; augmentation

Copyright © 2019 Wolters Kluwer Health, Inc. All rights reserved.