Secondary Logo

Journal Logo

Basic and Clinical Research

Treatment of Periimplant Mucositis

A Systematic Review of Randomized Controlled Trials

Ata-Ali, Javier DDS, MS, MPH, PhD*; Ata-Ali, Fadi DDS, MS; Galindo-Moreno, Pablo DDS, PhD

Author Information
doi: 10.1097/ID.0000000000000190
  • Free

Abstract

In the same way as in the case of peri-implantitis,1 the definitions of periimplant mucositis vary in the literature, and no clear criteria have been established regarding the diagnosis and treatment of this disorder. The Sixth European Workshop in Periodontology2 held in 2008 in Göteborg (Sweden) defined periimplant mucositis as inflammation of the periimplant mucosa, without signs of supporting bone loss. Later, the Seventh European Workshop in Periodontology3 held in Segovia (Spain) established the presence of bleeding on probing (BOP) as the key parameter for diagnosing periimplant mucositis. According to the latest definition of the American Academy of Periodontology,4 periimplant mucositis is a disease in which the presence of inflammation is confined to the soft tissues surrounding a dental implant, with no signs of loss of supporting bone after initial bone remodeling during healing.

Experimental studies in humans have shown that the accumulation of bacterial plaque during a period of 3 weeks exhibits a similar effect in both teeth (gingivitis) and dental implants (periimplant mucositis).5,6 Accordingly, periimplant mucositis appears as a host response to bacterial invasion, in the same way as gingivitis in relation to natural teeth.7 Histological studies of soft tissues have shown that inflammatory infiltrations in the mucosa around implants and the gingiva around natural teeth have many features in common.8–10 However, if bacterial plaque accumulates for more than 3 months, the inflammatory infiltrate of the periimplant mucosa is almost 3 times as great as in the case of natural teeth.7,9 A meta-analysis conducted by Atieh et al11 found periimplant mucositis to affect 63.4% of the patients and 30.7% of the implants.

The protocols used to treat gingivitis and periimplant mucositis are similar. However, very few studies have addressed the treatment of periimplant mucositis.12–17 A number of therapies have been used in application to periimplant mucositis, including antiseptic agents,15,16,18–20 the administration of antibiotics,17 the use of glycine powder air polishing (GPAP),21 or sodium carbonate abrasive air powdering.14,22

The purpose of this study was to systematically review the current literature and determine the most effective treatment for periimplant mucositis in patients with dental implants compared with a control group.

Material and Methods

The Preferred Reporting Items for Systematic Reviews and Meta-Analysis statement was used in this report.

Search Strategy for the Identification of Studies

The PubMed (MEDLINE) database of the United States National Library of Medicine was used to conduct a literature search of articles published up until October 2013. The following search terms were used in different combinations: “peri-implant mucositis,” “peri-implant mucositis treatment,” “humans,” “mechanical debridement,” “non-surgical treatment,” “RCT,” and “controlled clinical study”. Two examiners read the titles and abstracts of all studies, and no blinding was carried out regarding the names of the authors, journals and publication date. The search was completed with a review of the references of the selected articles to identify additional studies not found in the initial literature search.

In addition, a manual search (up until October 2013) was made of the following journals: Clinical Implant Dentistry and Related Research, Clinical Oral Investigations, Clinical Oral Implants Research, European Journal of Oral Implantology, Implant Dentistry, International Journal of Oral and Maxillofacial Implants, Journal of Clinical Periodontology, Journal of Oral Implantology, Journal of Periodontology, Medicina Oral, Patología Oral y Cirugía Bucal, and Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology.

Study Screening Criteria

Before starting the study, a series of inclusion and exclusion criteria were established. Full-text articles chosen were assessed for the following inclusion criteria: (1) patients with at least 1 dental implant presenting signs of periimplant mucositis; (2) follow-up for at least 3 months; and (3) randomized controlled trials (RCTs). The following exclusion criteria were applied: (1) non-randomized studies; (2) case series, retrospective studies, and articles published as abstracts only; (3) studies on peri-implantitis; (4) studies failing to specify the diagnostic criteria of periimplant mucositis or the duration of follow-up. No restrictions were placed on the year or language of publication. Authors were contacted for clarification of missing information when necessary.

Quality Assessment

The methodological quality of the studies was assessed according to the levels of evidence (University of Oxford Centre for Evidence Based Medicine)23 and the Jadad scale, referred to the method of randomization, allocation concealment, blindness of examiners, and completeness of follow-up.24 Two authors independently assessed the methodological quality of the studies, and discrepancies were discussed between them to reach consensus. Those studies scoring ≤2 points were considered to be of low quality, whereas ≥3 points were indicative of high quality.24

Results

Study Screening

The combinations of search terms resulted in a list of 371 titles. Of these, 257 were found to be duplicated. To avoid reviewing duplicate articles, we remove any articles that appear more than once. As a result, 114 references were finally reviewed. All articles included in the review were RCTs and were published in English. One publication was excluded on applying the defined screening criteria: the study published by Corbella et al25 was not an RCT. Finally, 7 RCTs were seen to meet the inclusion criteria and were thus selected for inclusion in the systematic review (Fig. 1). The characteristics of these 7 studies are summarized in Table 1.

Fig. 1
Fig. 1:
Prisma flow diagram of the searching processes and results. Seven RCTs were seen to meet the inclusion criteria and were thus selected for inclusion in the systematic review.
Table 1
Table 1:
Description of the 7 Studies Included in the Systematic Review

Assessment of Study Quality

The assessment of the methodological quality of each article is summarized in Table 2. Of the 7 RCTs included in the systematic review, 3 studies19–21 were considered to be of low quality, with Jadad scores of ≤2. Four studies15–18 were of relatively high quality, with Jadad scores of ≥3. As regards the level of evidence assessment, 4 studies15–18 were ranked as level 1b and 3 studies19–21 as level 2b.

Table 2
Table 2:
Assessment of the Methodological Quality of Each Article

Description of the Studies

Porras et al19 placed 28 implants in 16 patients; the study group underwent mechanical cleaning, and instructions were provided on oral hygiene, with the prescription of 0.12% chlorhexidine as a gel and rinse. The control group likewise underwent mechanical cleaning, and instructions were provided on oral hygiene, but without the use of chlorhexidine. After a follow-up period of 3 months, no statistically significant differences were observed between the 2 groups. Heitz-Mayfield et al18 placed 29 implants in 29 patients and studied the effect of 0.5% chlorhexidine gel versus the administration of placebo gel (control group). After a follow-up period of 3 months, a decrease in periimplant mucositis was observed in both groups, with no statistically significant differences associated with the use of chlorhexidine. Thöne-Mühling et al16 in turn placed 36 implants in 13 patients. The study group received 1% chlorhexidine gel applied once subgingivally, the dorsum of the tongue was brushed for 1 minute with 1% chlorhexidine gel, each tonsil was sprayed 4 times with 0.2% chlorhexidine spray, rinsing was performed twice for 1 minute with 0.2% chlorhexidine solution, and the implants were cleaned using plastic scalers and polyetheretherketone-coated ultrasonic instruments. The control group received the same treatment but without the administration of chlorhexidine. Although a decrease in bacterial flora was observed in the first 24 hours in the patients treated with chlorhexidine, no statistically significant results were obtained after 8 months of follow-up. De Siena et al20 studied the effect of chlorhexidine in 23 patients, comparing 2 forms of presentation: 1% chlorhexidine gel twice a day for 10 days and 0.2% chlorhexidine rinse twice a day for 10 days. After a follow-up period of 3 months, plaque accumulation was found to differ significantly between the 2 groups. The bleeding index and probing depth (PD) were not significantly different between the 2 groups. Another study15 involving 59 patients analyzed the effect of toothpaste with 0.3% triclosan (in 30 patients) versus sodium fluoride toothpaste (in 29 controls). After a follow-up period of 6 months, BOP was seen to have decreased in the study group from 53.8% to 29.1%, whereas in the control group, the values increased from 52.3% to 58.8%. The changes in BOP and PD were statistically significant. Plaque accumulation was not significantly different between the 2 groups. The authors concluded that the continuous use of toothpaste with 0.3% triclosan results in significant reduction of periimplant inflammation.

In an RCT17 involving 43 patients with periimplant mucositis, the study group received mechanical debridement with titanium curettes, polishing using rubber cups, polishing paste, and the administration of azithromycin during 4 days (500 mg the first day, and 250 mg the next 3 days). The control group received mechanical debridement with titanium curettes, polishing using rubber cups and polishing paste. No decrease in bacterial burden was observed after 3 months of follow-up. After 6 months, BOP and PD were seen to have decreased as a result of improved oral hygiene. These authors17 advised nonsurgical debridement without the administration of systemic antibiotics as the treatment of choice for periimplant mucositis. Finally, Ji et al21 placed 33 implants in 24 patients and studied the effect of GPAP versus a control group subjected to supragingival scaling, root debridement, and polishing. No statistically significant results were observed after a follow-up period of 3 months.

Discussion

The purpose of this study was to determine the most effective treatment for periimplant mucositis in patients with dental implants compared with a control group. Four16,18–20 of the 7 RCTs included in the systematic review examined the effect of chlorhexidine in the treatment of periimplant mucositis, and none of them obtained statistically significant results. Of the remaining 3 RCTs included in the review, significant reduction of the signs of periimplant inflammation were only recorded after the continuous use during 6 months of toothpaste with 0.3% triclosan.15 In contrast, no statistically significant results were obtained in the treatment of periimplant mucositis with either GPAP21 or the administration of azithromycin through the systemic route.17 We contacted the authors of the article published by De Siena et al,20 who confirmed that the study was an RCT, despite the fact that the article describes the work as an “observational study”. We finally included this publication in the systematic review as an RCT.

Lang et al26 concluded that gingivitis and periimplant mucositis are not clearly different from the pathogenic perspective. Both diseases represent a host response to the bacterial challenge generated by biofilm formation. The infectious etiology of periimplant mucositis is well documented.26–28 A study29 involving 34 patients with 77 dental implants (comprising 23 mucositis and 54 healthy periimplant sites) concluded that bacterial plaque induces an inflammatory response that can lead to the development of periimplant mucositis. Adequate plaque control is therefore able to increase periimplant health, avoiding the risk of future complications.29 Because periimplant mucositis represents the obvious precursor of peri-implantitis, in the same way that gingivitis is a precursor to periodontitis, the treatment of mucositis must be the prerequisite for the prevention of peri-implantitis.26

In an experimental study conducted by Trejo et al10 in cynomolgus monkeys comparing mechanical debridement versus mechanical debridement with 0.12% chlorhexidine application, no statistically significant differences were found between the 2 groups. Another study25 demonstrated that a strict implant maintenance protocol can prevent the development of peri-implantitis, and that periimplant mucositis can be successfully treated through professional oral hygiene combined with the use of chlorhexidine as an antimicrobial agent. Other authors30,31 consider that GPAP can eliminate bacterial plaque in areas that are scantly accessible to mechanical debridement (situations with deep pockets or narrow defects). Máximo et al14 and Duarte et al22 in turn reported sodium carbonate abrasive air powdering to be an effective treatment. The mechanical elimination of bacterial plaque improves but does not fully eliminate inflammation of the periimplant mucosa.13 For this reason, the use of coadjuvant treatments such as chlorhexidine16,18,20 or sodium carbonate abrasive air powdering has been proposed.14,22 The meta-analysis published by Gunsolley32 on the effect of triclosan demonstrated both antiplaque and antigingivitis effects in 18 studies, in concordance with our own observations.

The main limitation of our study is the small number of articles that were available for review. A variable to be taken into account in the interpretation of the results is the fact that 4 of the 7 RCTs were of high quality, with level of evidence 1b. The aim was to conduct a meta-analysis to evaluate the effectiveness of periimplant mucositis treatment. This was not possible mainly due to the following: (1) Lack of homogeneity in defining periimplant mucositis. In effect, each study used a different definition, and we therefore accepted the definition used by the authors in each publication; (2) The treatments used in the studies differed in relation to the mechanical procedures involved, the form of presentation, dosage, the treatments of the control groups, and the duration of follow-up.

Conclusion

In conclusion, the analysis of the 7 RCTs included in the present systematic review shows that chlorhexidine, the administration of azithromycin through the systemic route, and GPAP are not effective for the treatment of periimplant mucositis over the long term. The only effective treatment identified was the use of toothpaste with 0.3% triclosan. An adequate level of oral hygiene is needed. Definitions of periimplant mucositis vary in the literature, and no clear criteria have been established regarding the diagnosis and treatment of these disorders. More RCTs involving larger sample sizes will be needed to establish the most effective treatment option for this disease.

Disclosure

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

References

1. Ata-Ali J, Candel-Marti ME, Flichy-Fernández AJ, et al.. Peri-implantitis: Associated microbiota and treatment. Med Oral Patol Oral Cir Bucal. 2011;16:e937–e943.
2. Lindhe J, Meyle J; Group D of European workshop on periodontology. Peri-implant diseases: Consensus report of the sixth European workshop on periodontology. J Clin Periodontol. 2008;35:282–285.
3. Lang NP, Berglundh T; Working group 4 of seventh European workshop on periodontology. Periimplant diseases: Where are we now?–Consensus of the seventh european workshop on periodontology. J Clin Periodontol. 2011;38:178–181.
4. American academy of periodontology report. Peri-implant mucositis and peri-implantitis: A current understanding of their diagnoses and clinical implications. J Periodontol. 2013;84:436–443.
5. Pontoriero R, Tonelli MP, Carnevale G, et al.. Experimentally induced peri-implant mucositis. A clinical study in humans. Clin Oral Implants Res. 1994;5:254–259.
6. Zitzmann NU, Berglundh T, Marinello CP, et al.. Experimental peri-implant mucositis in man. J Clin Periodontol. 2001;28:517–523.
7. Heitz-Mayfield LJ, Lang NP. Comparative biology of chronic and aggressive periodontitis vs. peri-implantitis. Periodontol 2000. 2010;53:167–181.
8. Berglundh T, Lindhe J, Marinello C, et al.. Soft tissue reaction to de novo plaque formation on implants and teeth. An experimental study in the dog. Clin Oral Implants Res. 1992;3:1–8.
9. Ericsson I, Berglundh T, Marinello C, et al.. Long-standing plaque and gingivitis at implants and teeth in the dog. Clin Oral Implants Res. 1992;3:99–103.
10. Trejo PM, Bonaventura G, Weng D, et al.. Effect of mechanical and antiseptic therapy on peri-implant mucositis: An experimental study in monkeys. Clin Oral Implants Res. 2006;17:294–304.
11. Atieh MA, Alsabeeha NH, Faggion CM Jr, et al.. The frequency of peri-implant diseases: A systematic review and meta-analysis. J Periodontol. 2013;84:1586–1598.
12. Heitz-Mayfield LJ, Lang NP. Antimicrobial treatment of peri-implant diseases. Int J Oral Maxillofac Implants. 2004;19:128–139.
13. Renvert S, Roos-Jansaker AM, Claffey N. Non-surgical treatment of peri-implant mucositis and peri-implantitis: A literature review. J Clin Periodontol. 2008;35:305–315.
14. Máximo MB, de Mendonça AC, Renata Santos V, et al.. Short-term clinical and microbiological evaluations of peri-implant diseases before and after mechanical anti-infective therapies. Clin Oral Implants Res. 2009;20:99–108.
15. Ramberg P, Lindhe J, Botticelli D, et al.. The effect of a triclosan dentifrice on mucositis in subjects with dental implants: A six-month clinical study. J Clin Dent. 2009;20:103–107.
16. Thöne-Mühling M, Swierkot K, Nonnenmacher C, et al.. Comparison of two full-mouth approaches in the treatment of peri-implant mucositis: A pilot study. Clin Oral Implants Res. 2010;21:504–512.
17. Hallström H, Persson GR, Lindgren S, et al.. Systemic antibiotics and debridement of peri-implant mucositis. A randomized clinical trial. J Clin Periodontol. 2012;39:574–581.
18. Heitz-Mayfield LJ, Salvi GE, Botticelli D, et al.; Implant complication research group. Anti-infective treatment of peri-implant mucositis: A randomized controlled clinical trial. Clin Oral Implants Res. 2011;22:237–241.
19. Porras R, Anderson GB, Caffesse R, et al.. Clinical response to 2 different therapeutic regimens to treat peri-implant mucositis. J Periodontol. 2002;73:1118–1125.
20. De Siena F, Francetti L, Corbella S, et al.. Topical application of 1% chlorhexidine gel versus 0.2% mouthwash in the treatment of peri-implant mucositis. An observational study. Int J Dent Hyg. 2013;11:41–47.
21. Ji YJ, Tang ZH, Wang R, et al.. Effect of glycine powder air-polishing as an adjunct in the treatment of peri-implant mucositis: A pilot clinical trial. Clin Oral Implants Res. 2014;25:683–689.
22. Duarte PM, de Mendonça AC, Máximo MB, et al.. Effect of anti-infective mechanical therapy on clinical parameters and cytokine levels in human peri-implant diseases. J Periodontol. 2009;80:234–243.
23. OCEBM levels of evidence working group. The Oxford 2011 Levels Evid. Oxford Centre for Evidence-Based Medicine. Available at: http://www.cebm.net/index.aspx?o=1025. Accessed October 4, 2013.
24. Jadad AR, Moore RA, Carroll D, et al.. Assessing the quality of reports of randomized clinical trials: Is blinding necessary? Control Clin Trials. 1996;17:1–12.
25. Corbella S, Del Fabbro M, Taschieri S, et al.. Clinical evaluation of an implant maintenance protocol for the prevention of peri-implant diseases in patients treated with immediately loaded full-arch rehabilitations. Int J Dent Hyg. 2011;9:216–222.
26. Lang NP, Bosshardt DD, Lulic M. Do mucositis lesions around implants differ from gingivitis lesions around teeth? J Clin Periodontol. 2011;11:182–187.
27. Renvert S, Roos-Jansåker AM, Lindahl C, et al.. Infection at titanium implants with or without a clinical diagnosis of inflammation. Clin Oral Implants Res. 2007;18:509–516.
28. Ata-Ali J, Flichy-Fernández AJ, Alegre-Domingo T, et al.. Analysis of the peri-implant microbiota in 90 dental implants and its relationship to crevicular fluid volume. Med Oral Patol Oral Cir Bucal. 2011;16:e944–e947.
29. Ata-Ali J, Flichy-Fernandez AJ, Ata-Ali F, et al.. Clinical, microbiologic, and host response characteristics in patients with peri-implant mucositis. Int J Oral Maxillofac Implants. 2013;28:883–890.
30. Sahrmann P, Ronay V, Sener B, et al.. Cleaning potential of glycine air-flow application in an in vitro peri-implantitis model. Clin Oral Implants Res. 2013;24:666–670.
31. Schär D, Ramseier CA, Eick S, et al.. Anti-infective therapy of peri-implantitis with adjunctive local drug delivery or photodynamic therapy: Six-month outcomes of a prospective randomized clinical trial. Clin Oral Implants Res. 2013;24:104–110.
32. Gunsolley JC. A meta-analysis of six-month studies of antiplaque and anti-gingivitis agents. J Am Dent Assoc. 2006;137:1649–1657.
Keywords:

dental implant; periimplant mucositis; periimplant diseases; inflammation; mechanical debridement; chlorhexidine

Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.