Manoj Muthukuru Arbia Zainvi Enrique O. Esplugues Thomas F.

Flemmig

Non-surgical therapy for the management of peri-implantitis: a systematic review

Authors afliations: Manoj Muthukuru, Arbia Zainvi, Enrique O. Esplugues, Thomas F. Flemmig, Department of Periodontics, University of Washington, Seattle, WA, USA Corresponding author: Thomas F. Flemmig Department of Periodontics, School of Dentistry, University of Washington, Box 35774, Seattle, WA 98195-7444, USA Tel.: +1 206 616 9671 Fax: +1 206 616 7478 e-mail: emmig@uw.edu
Conicts of interest: The authors have not declared any potential conicts.

Key words: dental polishing, dental scaling, drug therapy, laser therapy, peri-implantitis Abstract Peri-implantitis is characterized by mucosal inammation and loss of supporting peri-implant bone. Objective: The objective of this systematic review was to evaluate the efcacy and safety of non-surgical treatment of peri-implantitis. Materials and methods: MEDLINE, Embase, and Web of Science were searched to identify randomized clinical trial studies that assessed non-surgical treatment of peri-implantitis with a minimum follow-up period of 3 months. Results: From a total of 29 abstracts, nine trials were included in this systematic review. Adjunctive local delivery of antibiotics, submucosal glycine powder air polishing, or Er:YAG laser treatment resulted in greater reduction in bleeding on probing compared with submucosal debridement using curettes with adjunctive irrigation with chlorhexidine. In addition, greater reductions in probing depths were found following adjunctive local delivery of antibiotics. The evidence neither supported nor refuted the clinical efcacy of submucosal debridement using curettes or ultrasonic scalers alone. No progressive bone loss was found following any of the assessed treatments over a maximum observation period of 12 months. Only two studies reported implant survival rates, which were 100% over 6 months. Conclusions: The available evidence suggested that submucosal debridement with adjunctive local delivery of antibiotics, submucosal glycine powder air polishing, or Er:YAG laser treatment may reduce clinical signs of peri-implant mucosal inammation to a greater extent relative to submucosal debridement using curettes with adjunctive irrigation with chlorhexidine. Long-term randomized controlled trials are needed to assess the efcacy of non-surgical therapy on progressing bone loss, implant survival rates, and measures of oral health-related quality of life.

Date: Accepted 09 June 2012

To cite this article: Muthukuru M, Zainvi A, Esplugues EO, Flemmig TF. Nonsurgical therapy for the management of peri-implantitis: a systematic review. Clin. Oral Implants Res. 23(Suppl. 6), 2012, 7783 doi: 10.1111/j.1600-0501.2012.02542.x

Peri-implantitis is dened as loss of crestal peri-implant bone in conjunction with bleeding on probing (Lang & Berglundh 2011). It is often associated with increased peri-implant pocket probing depths, mucosal recession, or suppuration (Fransson et al. 2008). Periimplantitis has been found in as many as 28 56% of subjects and in 1243% of implants with 5 years or more of functional loading (Zitzmann & Berglundh 2008). In implants that had developed peri-implantitis, a retrospective assessment found that the average bone loss in the rst year of function was 1.68 mm with 68% of implants demonstrating bone loss of 1 mm or greater and 32% of implants showing bone loss of 2 mm or greater in the rst year. A multilevel analysis predicted a mean bone loss of 0.15 mm per year in sites with peri-implantitis (Fransson et al. 2010). If peri-implantitis progresses,

it may result in the loss of the implant (Leonhardt et al. 2003). The inammatory cell inltrate in peri-implantitis lesions was more pronounced and located further apical of the pocket epithelium and comprised a greater proportion of neutrophils and macrophages when compared with periodontitis lesions (Berglundh et al. 2011). Fibroblasts in peri-implantitis lesions exhibited a distinct cytokine prole that may contribute to matrix breakdown (Bordin et al. 2009). These features of peri-implantitis suggest a more acute inammatory response when compared with periodontitis. For instance, in experimental dog models (Ericsson et al. 1992), that assessed biolm induced host response, the inammatory inltrate was similar in the gingiva and periimplant mucosa when analyzed during the third week. However, analysis during the

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third month demonstrated three times higher inltration of inammatory cells at the periimplant mucosa relative to gingival tissues. Submucosal (subgingival) biolms in peri-implantitis have been found to exhibit greater bacterial diversity compared with biolms associated with healthy peri-implant mucosa. Phyla Chloroexi, Tenericutes, Synergistetes, and species Parvimonas micra, Peptostreptococcus stomatis, Pseudoramibacter alactolyticus, and Solobacterium moorei and some of the putative periodontal pathogens including, Porphyromonas gingivalis, Prevotella intermedia, Prevotella nigrescens, and Aggregatibacter actinomycetemcomitans have been associated with periimplantitis (Leonhardt et al. 1999; Koyanagi et al. 2010). Although the primary etiology is infectious in nature, risk indicators such as poor oral hygiene, smoking, history of periodontitis, diabetes mellitus, genetic traits, excessive alcohol consumption, and the type of implant surface may contribute to the development of peri-implantitis (HeitzMayeld 2008; Heitz-Mayeld & Huynh-Ba 2009; Renvert & Persson 2009). Recent systematic reviews about the treatment of peri-implantitis found that mechanical submucosal debridement alone had very limited effect on the clinical signs of peri-implantitis (Renvert et al. 2008a,b). Adjunctive locally delivered or systemically administered antibiotics have been found to improve clinical outcomes relative to submucosal debridement alone, however, this did not resolve all lesions (Esposito et al. 2008, 2010; Renvert et al. 2008a,b). The outcomes following laser treatment or ultrasonic scaling were not found to be statistically signicantly different from those following submucosal debridement (Esposito et al. 2010). The objective of this systematic review was to evaluate the clinical efcacy and safety of non-surgical therapy in the treatment of peri-implantitis.

implantitis AND (Humans[Mesh] AND randomized controlled trial[ptyp] AND English [lang]))) AND (((((((((((((((non-surgical therapy) OR scaling) OR antimicrobial) OR antimicrobial) OR anti-bacterial) OR antibiotic) OR laser) OR non-surgical therapy) OR nonsurgical) OR antiseptic)) OR photodynamic therapy) OR air polishing) OR sonic) OR ultrasonic AND (Humans[Mesh] AND randomized controlled trial[ptyp] AND English [lang])).
Study selection

reported in clinical trials (Faggion et al. 2010), clinical peri-implant attachment level (CAL), bone level (BL), pocket probing depth (PPD), peri-implant mucosal inammation, and plaque index (PLI) were used as secondary outcome variables.
Data extraction and analysis

Titles and abstracts from the three search engines were downloaded to EndNote software. EndNote X was used to search remote databases, to import the reference data, and to manage the imported references. Two reviewers (MM, TFF) screened titles and abstracts independently of each other. Disagreement regarding inclusion was resolved by discussion. Full text manuscripts of the selected studies were obtained and further reviewed for inclusion.
Population

Three reviewers (MM, AZ, EOE) extracted pertinent information from the selected manuscripts and entered into an excel work sheet independently from each other. Data were grouped based on the assessed interventions and the reported outcomes presented in a tabulated form. Due to lack of uniformity in the assessed treatment regimens, no metaanalysis was performed.

Results
A total of 29 abstracts were retrieved and evaluated independently by two reviewers. A total of 11 publications were selected for the purpose of the systematic review. Cohens kappa coefcient of inter-rater agreement was 0.78. Out of the 11 studies, one study (Tang et al. 2002) was excluded from the review, as the manuscript was not written in English. Another study (Persson et al. 2011) was excluded as this manuscript reported the same clinical data that were presented in another study that was included in this review (Renvert et al. 2011). Figure 1 presents the overall schematic of the selection of the studies for the purpose of this systematic review. For comparison, the included manuscripts were grouped by the assessed test treatment, i.e. mechanical submucosal debridement, adjunctive antimicrobial agents, and laser treatment. The overall designs of the included studies are presented in Table 1. Only two studies (Renvert et al. 2011) provided information about the selected primary outcome measure survival rate of implants. Secondary outcome measures including, CAL, BL, PPD, mucosal inammation, and plaque index were reported to varying extent.

Subjects in the included trials must have had at least one osseointegrated implant with a denitive restoration that presented with signs of peri-implantitis. Peri-implantitis was dened as peri-implant crestal bone loss at osseointegrated dental implants in conjunction with inammation of peri-implant mucosa (Lang & Berglundh 2011).
Types of intervention

Materials and methods

Search method for identication of studies

The intervention of interest was non-surgical treatment of peri-implantitis. Non-surgical treatment was dened as any treatment performed without deliberately injuring the epithelial integrity of the peri-implant mucosa, e.g. an incision. Non-surgical treatment included mechanical submucosal debridement using hand instruments, sonic instruments, ultrasonic instruments, and air polishing; locally applied antiseptics; local delivery or systemic administration of antibiotics; use of lasers; and host modulation therapy.
Control intervention

Randomized controlled trials that had assessed non-surgical treatment of peri-implantitis were searched in Medline, Embase, and Web of Science. The Boolean operators such as AND/OR were employed along with the keywords for the purpose of the literature search. Manuscripts published until November 2011 were included. The following query was used: (((Peri-implantitis) OR peri-

As there is no established standard of care in the treatment of peri-implantitis, any control treatment used in randomized controlled trials was included.
Outcome measures

Characteristics of evaluated peri-implantitis lesions

As primary outcome variable, the survival rate of implants was used. As it was expected that mostly surrogate endpoints had been

The amount of peri-implant bone loss of evaluated peri-implantitis lesions in the included clinical trials ranged from 1.5 mm (Karring et al. 2005) to greater than 50% of the length of the implant as assessed by radiographs (Buchter et al. 2004). With the exception of one study, which only used radiographic bone loss as inclusion criterion
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Adjunctive antimicrobial treatment

Er:YAG laser treatment

Fig. 1. Schematic of screening and selection of manuscripts.

(Buchter et al. 2004), all studies used periimplant bone loss, increased probing depths, and signs of peri-implant mucosal inammation such as BOP and/or suppuration as inclusion criteria (Karring et al. 2005; 2Schwarz et al. 2005, 2008; Renvert et al. 2006, 2008a,b, 2009, 2011; Renvert & Persson 2009).
Machine driven submucosal debridement

Two studies compared the efcacy of a piezoelectric ultrasonic scaler that oscillated along the axis of the working tip with that of hand instrumentation using either carbon ber or titanium curettes for submucosal debridement (Karring et al. 2005; Renvert et al. 2009). Reduced bleeding on probing (BOP) scores from baseline to 6 months were found following both treatments in one of the study; in the test group this nding was accompanied by an improvement in plaque scores (Renvert et al. 2009). No signicant changes over time were found for PPD and bone levels. One study (Renvert et al. 2009) reported 100% implant survival rates in both treatment groups over a 6-months observation period. No differences between treatments were found in any of the assessed outcome parameters at 3 months or 6 months (Table 2).
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Four studies (Buchter et al. 2004; Renvert et al. 2006; Sahm et al. 2011; Renvert et al. 2008a,b) assessed antimicrobials as an adjunct to submucosal debridement in the treatment of peri-implantitis. Among these, two studies assessed the efcacy of locally delivered minocycline microspheres (1 mg minocycline and 3 mg polyglycolide-codi-lactate) as an adjunct to submucosal debridement in comparison with submucosal debridement with subgingival irrigation with 0.1% chlorhexidine digluconate gel (Renvert et al. 2006, 2008a,b). The third study assessed submucosal debridement with carbon curettes and adjunctive subgingival irrigation with 0.1% chlorhexidine digluconate solution compared with subgingival air polishing using a low-abrasive glycine powder (Sahm et al. 2011). The fourth study in this category evaluated local delivery of 8.5% doxycycline hyclate as an adjunct to submucosal debridement and compared it to submucosal debridement using plastic hand instruments and adjunctive submucosal irrigation with 0.2% chlorhexidine digluconate solution (Buchter et al. 2004). A single application of adjunctive minocycline microspheres resulted in reduced BOP compared with adjunctive 1% chlorhexidine gel application up to 6 months. When the adjunctive applications were repeated every 3 months, the difference between groups was seen after 12 months (Renvert et al. 2006, 2008a,b). Probing depths were found to be signicantly lower in sites treated with adjunctive minocycline microspheres compared with those receiving adjunctive 1% chlorhexidine gel up to 12 months in one study (Renvert et al. 2006), but not in the other (Renvert et al. 2008a,b). Adjunctive local delivery of 8.5% doxycycline hyclate resulted in signicantly lower BOP scores and PPDs and greater CALs when compared with submucosal debridement alone at 18 weeks. Submucosal glycine powder air polishing without the use of any antimicrobial agent resulted in signicantly lower BOP values compared with mechanical debridement with carbon curettes and adjunctive submucosal application of 1% chlorhexidine gel at 3 months follow-up (Sahm et al. 2011). Bone levels were reported in only one study that assessed adjunctive minocycline microspheres in comparison with adjunctive 1% chorhexidine gel. No signicant change in bone levels was found during the 12months observation period in either group (Renvert et al. 2008a,b) (Table 3).

All three selected studies employed Er:YAG lasers at 100 mJ/pulse (12.7 J/cm10), 10 Hz with a pulse energy at the tip of approximately 85 mJ/pulse (Schwarz et al. 2005; Schwarz et al. 2006; Renvert et al. 2011). Among these studies, one of them employed submucosal glycine powder air polishing as control treatment (Renvert et al. 2011) and the other two studies used submucosal debridement using plastic curettes with adjunctive submucosal irrigation with 0.2% chlorhexidine digluconate solution (Schwarz et al. 2005; Renvert et al. 2011). Following Er:YAG laser irradiation lower BOP scores were found compared with submucosal debridement with adjunctive chlorhexidine application. All other clinical parameters demonstrated a signicant improvement at 6 months following either treatment without any signicant differences between groups. At 12 months, clinical parameters returned to baseline values (Schwarz et al. 2006). Both, Er:YAG laser treatment and submucosal glycine powder air polishing resulted in reduced BOP and reduced PPD values at 6 months without signicant difference between treatment groups (Renvert et al. 2011) (Table 4). In one subject, perforation of the buccal peri-implant mucosa occurred following Er:YAG laser treatment, which required suturing and resulted in mucosal recession following healing (Schwarz et al. 2006).

Discussion
Peri-implantitis following successful osseointegration of functionally loaded implants results due to microbial load in the form of dental plaque biolm formation around the implants that provoke the host inammatory/ immune response (Zitzmann & Berglundh 2008). The incidence of peri-implantitis could be underestimated and if left untreated would likely lead to implant failure (Esposito et al. 2002, 2003). This is clinically relevant due to the increased number of dental implants that are being placed that are susceptible to longer follow-up periods and therefore could predispose to more cases of peri-implantitis. The goal of treating peri-implantitis is to reduce the microbial burden, achieve a state of periimplant mucosal health, and if possible regenerate peri-implant bone that is lost during the inammatory process. The efcacy of the assessed non-surgical treatments could not be evaluated using a true outcome measure as only two studies reported implant survival rates over a rather
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Table 1. General information

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Implants total per patient (SD)/Implants with periImplantitis per patient (SD) Intervention A SMD with ultrasonic scaler B 3 Months, 6 months 1 Months, 3 months, 6 months 3 Months, 6 months, 9 months, 12 months Follow-up period B Range 5078 At least 2/ at least 2 NK/1 NK/1 Nobel Biocare (24); Astra (6); NK (1)/NK NK NK SMD and minocycline microspheres NK SMD with ultrasonic scaler At least 2/ at least 2 Branemark (2), ITI (4), Astra (5)/7 screw-type/NK A B Implant type/ Mean age of Implants (SD) in years Type of restoration/ Time after restoration 62.7 (12.1) SMD with carbon ber curettes SMD with titanium curettes 62.40 (7.72) NK/3.35 (2.12) NK/2.37 (1.26) 60.6 (38.6) Screw-type/NK NK/at least1 NK/at least1 SMD with carbon curets and submucosal irrigation with 0.1% chlorhexidine SMD and submucosal irrigation with 1% chiorhexidine gel Subgingival glycine powder air polishing 3 Months, 6 months 56 NK/at the most 3 NK/at the most 3 BRA (2), CAM (5) FRI (2) ITI (5) TSV (6) NI (3)/BRA (4), CAM (7) FRI (0) ITI (4) TSV (3) NI (2)/ NK ITI, SLA/NK NK/ 5.2 2.1 years 18 weeks 61.6 (8.6) NK/3.1 NK/2.6 NK NK SMD with plastic scaler and submucosal irrigation with 0.2% CHX and 8.5% doxycycline hyclate SMD and minocyline microspheres SMD and submucosal irrigation with 0.2% CHX SMD and submucosal irrigation with 1% CHX gel Er:YAG laser irradiation 100 mJ/pulse (12.7 J/cm10), 10 Hz 3 Months, 6 months, 9 months, 12 months 3 Months; 6 months screw-type/NK 51 6 pts had 2 implants; 4 pts had 1 implants/At least 1 implant NK/At least 1 NK/At least 1 6 pts had 2 implants; 4 pts had 1 implants/At least 1 implant ERL-SLA (n = 9), TPS (n = 7)/C-SLA (n = 8), TPS (n = 8)/Test = 4.1; Control = 4.3 52 (11) screw-type/NK Er:YAG laser irradiation 100 mJ/pulse (12.7 J/cm10), 10 Hz Submucosal debridement (SMD) with plastic curettes + 0.2% Chlorhexidine (CHX) SMD with plastic curettes and submucosal irrigation with 0.2% CHX 3 Months, 6 months, 12 months 68.9 (12.5) NK/2.6 (0.2) NK/2.0 (0.2) IMZ, ITI (SLA, TPS). Spline Twist (MTX), ZLDuraplant. camlog/Test = 5.1 (2.2); Control = 4.2 (3.4) machined surface, medium rough surface NK/NK Er:YAG laser irradiation 100 mJ/pulse (12.7 J/cm10), 10 Hz Subgingival glycine powder air-polishing BOP: 6 Months; Pl: 2 weeks, 6 weeks, 12 weeks, 6 months; PD: 6 months

Subjects 1 number of implants

Age (SD) in year

Reference Treatment

Muthukuru et al Non-surgical therapy of peri-implantitis

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Machine driven submucosal debridement Karring 11 (11) 11 (11) Range 5078 et al. 2005 14 17 60.3 (12.9) Renvert et al. 2009; Adjunctive antimicrobial treatment Renvert 17 (57) 15 (38) 60.82 (12.72) et al. 2008a,b

Sahm et al. 2011

15 (19)

15 (22)

60.6 (38.6)

Buchter et al. 2004

14

14

54

Renvert et al. 2006

16

14

65.6 (8.6)

Er:YAG laser treatment 10 (16) 10 (16) Schwarz et al. 2005

48

Schwarz et al. 2006

10 (20)

8 (16)

56 (14)

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Renvert et al. 2011

21 (45)

21 (55)

68.5 (6.4)

Muthukuru et al Non-surgical therapy of peri-implantitis

Table 2. Machine driven submucosal debridement

Table 3. Adjunctive antimicrobial treatments

Table 4. Er:YAG laser treatment

short observation period of 6 months (Renvert et al. 2009; Renvert et al. 2011). Limited information was available about the progression of bone loss in peri-implantitis following non-surgical treatment. When bone levels were assessed, no signicant changes were found during the observation period of up to 12 months (Karring et al. 2005; Renvert et al. 2006). However, based on the multilevel analysis that predicts a mean annual bone loss of 0.15 mm in peri-implantitis sites
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(Fransson et al. 2010) studies that employ long observation periods are essential to determine the outcomes such as peri-implant bone levels and implant survival. Gingival recession or patient-centered and dentistassessed outcomes such as esthetics were not consistently reported and therefore could not be conclusively evaluated. The exclusion criteria among the included trials were quite heterogeneous. Some studies excluded subjects who had used antibiotics

36 months prior to enrollment (Buchter et al. 2004; Karring et al. 2005; Schwarz et al. 2005; Schwarz et al. 2006). Peri-implantitis sites that had received mechanical debridement in the previous 3 months (Karring et al. 2005) or peri-implantitis treated during the past 6 months (Schwarz et al. 2006) were excluded. In other studies, active smoking, absence of keratinized mucosa around the implants, or systemic diseases were used as exclusion criteria (Schwarz et al. 2005, 2006).
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Factors related to implant design such as hollow cylinders were excluded (Schwarz et al. 2005, 2006). Furthermore, in a study (Karring et al. 2005), implants in the test and control groups that were not of the same brand or if these implants were approximal to each other or the amount of bone loss differed by more than 1 mm were excluded. Various non-surgical interventions or combinations of interventions had been assessed in the included studies making a direct comparison of the results difcult. Furthermore, the observation periods ranged from 3 months up to 12 months. The type and frequency of maintenance care during the follow-up phase of the trials were inconsistent. For instance, in one study (Buchter et al. 2004), oral hygiene instructions and repeated motivation was reinforced at weekly intervals and in another study, quarterly maintenance and oral hygiene instructions were given (Karring et al. 2005). The number of patients included in the included studies was relatively small, resulting in a low statistical power for detecting true differences between treatments. Given a predicted mean annual rate of bone loss of

0.15 mm per in untreated peri-implantitis (Fransson et al. 2010) clinical trials with larger sample sizes and longer follow-ups are needed to evaluate whether non-surgical treatment of peri-implantitis may arrest disease progression. Moreover, none of the included trials reported power calculation to achieve statistical signicance between the test and control groups. None of the included studies reported of assessing non-serious or serious adverse events, making it difcult to evaluate the safety of the non-surgical treatments that were evaluated. Only in one study, one adverse event was reported that had occurred in one patient following Er:YAG treatment (Schwarz et al. 2006). Withdrawal of subjects from the trials was reported (Schwarz et al. 2005, 2006) but no specic reasons for the withdrawal from the studies were presented.

Conclusions

an adjunct to submucosal debridement may result in greater reduction in BOP scores and PPDs compared with submucosal debridement with adjunctive submucosal irrigation with chlorhexidine digluconate. Er:YAG laser treatment may result in greater reduction in BOP scores compared with submucosal debridement with adjunctive submucosal irrigation with chlorhexidine digluconate. Submucosal glycine powder air polishing may reduce BOP scores to a greater extent than submucosal irrigation with chlorhexidine digluconate as an adjunct to submucosal debridement with hand instruments and showed no different clinical outcomes compared with Er:YAG laser treatment. The available information is insufcient to suggest whether or not any of the assessed non-surgical treatments arrest bone loss in implants with periimplantitis.

Locally delivered antibiotics (minocycline microspheres or doxycycline hyclate) as

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