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MANAGEMENT OF PERI-IMPLANT DISEASE: A CURRENT APPRAISAL

Oksana P. Mishler, RDH, MS, and Harlan J. Shiau, DDS, DMSc

SORT SCORE ABSTRACT ABCNA While the clinical science of managing peri-implant diseases is progressing, careful SORT, Strength of Recommendation Taxonomy and preventive care of peri-implant tissue health during maintenance is paramount. LEVEL OF EVIDENCE 1 2 3 Background See page A8 for complete details regarding SORT and Implants have become a routine treatment option for missing dentition. The bio- LEVEL OF EVIDENCE grading system logical complications of restored dental implants and associated supra-structures share similarities with the biofilm of natural dentition. Our existing par- adigms of treatment can partially be applied to management of peri-implant disease. Approach A critical analysis of the peri-implant disease literature was conducted, anchored by a search on the MEDLINE database (2005 to present) by way of Ovid Medline . Search terms peri-implantitis, peri-implant mucositis and peri-implant diseases were utilized. Select references within bibliographies of review articles were sought. Conclusion The dental team must play a critical role in educating patients to control plaque-biofilm associated with peri-implant tissues and associated restorations. Routine assessments at maintenance appointments allow early treatment intervention to prevent escalation of peri-implant disease. Given the infancy of clinical science surrounding peri- implantitis treatment, further, high-quality evidence based studies are expected.

Department of Periodontics, Key words: Peri-implantitis, peri-implant University of Maryland Dental School, Baltimore, MD 21201, ith the unfavorable prognosis of a tooth, the clinician and patient may be USA Wconfronted with decisions of tooth replacement. Dental implants and asso- ciated restorations have become an increasingly common treatment option in clinical Corresponding author: Department of Peri- practice. A recent systematic review has determined the 5- and 10-year implant odontics, University of Maryland Dental School, 1 Room 4213, Baltimore, MD 21201, USA. survival rate to be 97.7% and 92.8%, respectively. Nevertheless, the osseointegrated Tel.: 11 410 706 7152; fax: 11 410 implant is susceptible to complications. Notably, implants may develop infections 706 7201. E-mail: [email protected] similar to the biological complications that afflict natural dentition. Biofilm infections J Evid Base Dent Pract 2014;14S: of the peri-implant tissues challenge epithelial health and connective tissue sur- [53-59] rounding the implant—and potentially the underlying, supporting bone. 1532-3382/$36.00 ª 2014 Elsevier Inc. All rights reserved. Peri-implant disease is classified in part by anatomical involvement: peri-implant http://dx.doi.org/10.1016/j.jebdp.2014.04.010 mucositis and peri-implantitis. These specific pathologies can develop subsequent to a normal implant wound healing phase and . Peri-implant mucositis is characterized by inflammation of the gingival soft tissue surrounding the implant. Peri-implantitis is defined by loss of crestal bone surrounding the implant in addition to inflammation of the peri-implant tissues clinically noticeable as . Additional clinic parameters associated with peri-implantitis include suppuration, deepened probing depths, and recession of mucosal tissues. In particular,

53 June 2014 JOURNAL OF EVIDENCE-BASED DENTAL PRACTICE SPECIAL ISSUE—ANNUAL REPORT ON DENTAL HYGIENE peri-implantitis refers to a post-osseointegration event, dis- peri-implant disease progression.7,8 Suppuration at peri- tinguishing it from dynamic bone level changes associated with implant pockets is associated with and implies an in- remodeling immediately following implant placement. flammatory reaction present in the peri-implant tissues. Sup- puration has also been correlated to implant bone loss. Peri-implant diseases represent a common finding in contem- porary clinical practice. Mombelli and colleagues reviewed peri- Periodontal probing and related attachment level changes implant disease occurrence, focusing on studies spanning a represent an essential means of diagnosing and monitoring minimum of 5 years; the prevalence of peri-implantitis was re- peri-implant disease. Increased pocket probing depth is a ported to be in 10% of implants and 20% of patients.2 The clinical sign consistent with a finding of peri-implantitis, though authors point out, similar to other systematic reviews, that this finding alone is insufficient to fully establish a diagnosis. heterogeneity in disease definitions in studies makes it difficult Nonetheless, the finding of a probing depth $5 mm should to offer an unequivocal statement on prevalence of peri- be further assessed by the clinician, utilizing current and past implantitis. Another concern is whether the convenience radiographs. Note that major epidemiological studies have samples of clinical studies can be generalized to the overall used peri-implantitis definitions that incorporate a probing population seeking implant . Overall, the prevalence of depth (either a 4 or 5 mm threshold), radiographic criteria of peri-implant mucositis is higher than that of peri-implantitis; it bone loss, and an inflammatory measure (bleeding on prob- occurs in about 50% of implants and just under 80% of patients.3 ing, or suppuration).2 Studies have allayed fears that probing would cause long-term damage to the peri-implant tissues. Peri-implant diseases are generally thought to represent Gingival mucosa surrounding a differs from that inflammatory conditions in response to bacterial plaque. Other of natural dentition. The peri-mucosal seal that forms after factors, such as aberrant occlusal forces, may also contribute to surgical placement provides a barrier against bacterial invasion the initiation and/or progression of peri-implant disease but from the oral cavity but is lacking some strength of attachment remain incompletely understood. The composition of these when compared to a natural sulcus. Thus, a plastic probe with biofilms is similar to the subgingival of chronic peri- minimal force (0.25 N) is recommended around an implant to odontitis, dominated by Gram-negative bacteria. Notably, avoid long-term damage to the peri-implant tissue. Etter et al studies have generally reported Porphorymonas gingivalis and verified that a complete reformation of the peri-mucosal seal other bacteria at higher frequencies in peri- 9 – resulted at 5 days following gentle probing. Caution must be implantitis sites than healthy sites.4 6 In healthy implants with applied to probing measurements, as they alone are not stable probing depths of 5 mm or less the flora is characterized by indicative of disease around an implant. The presence of gram-positive cocci and small number of gram-negative species.6 prosthetic reconstructions attached to the implant—the While the objective of this article is to present the current profile of abutments or associated crowns may increase treatment options for peri-implant disease, it should be probing depth readings. Radiographic interpretation should prefaced by a discussion on assessment and diagnosis. What either confirm or dispute peri-implant diagnosis when will be apparent is that many treatment and management bleeding or inflammation is associated with increased probing paradigms are in their infancy; consequently, implementing depth. Use of a radiograph, in conjunction with periodontal strategies of early detection and maintenance of implants probing will greatly aid the clinician in interpreting a ‘large’ becomes essential. probing depth; for example, a radiograph that displays a sig- nificant amount of implant supra-structure cantilevered off of IS THE IMPLANT HEALTHY? ASSESSMENT OF the implant should alert the clinician to cautiously consider ‘ ’ PERI-IMPLANT CONDITION large clinical probing depth results. The clinical assessment tools used in monitoring periodontal Mobility of an implant is a terminal clinical sign—removal of health of natural teeth are used in monitoring peri-implant the failed implant is warranted. The osseointegrated dental tissues, though some considerations must be made given implant does not have any connective tissue fiber attachments the obvious structural differences (Figure 1). between the bone and the implant. As a result, mobility is a concerning finding suggesting the loss of direct bone-implant fl Assessment of mucosal in ammation is primarily made by contact that leads to the loss of stability. There is minimal observing bleeding following light probing (0.25 N) of the clinical science at this time indicating any ability to achieve a implant sulcus/pocket. As with periodontitis, the absence of stable long-term therapeutic outcome from treating implant — bleeding on probing has a high negative predictive value mobility. providing the clinician a predictor of stable peri-implant con- ditions. A prospective study detailed the utility of this param- Radiographic assessment is important in identifying bone loss eter during the maintenance phase of restored dental implants. associated with peri-implantitis. Again, in conjunction with Bleeding on probing at implant sites during more than 50% of probing, radiographs aid in developing a proper picture of the recall visits over a two-year period was strongly associated with underlying osseous topography of putative peri-implantitis

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Figure 1. Components of routine peri-implant tissue assessment. Diagnostics that assess inflammatory status and architectural changes of underlying bone allow clinician to monitor health of peri-implant tissues. (A.) A routine implant assessment protocol involves monitoring inflammation via appearance of tissues and, or, bleeding on probing. Probing depths should be regularly recorded; relative attachment level (RAL) can also be monitored. Similar to clinical attachment level, RAL utilizes a fixed reference point (e.g. implant crown margin) to more accurately monitor peri-implant support. (B.) Peri-implant health is described. Radiographs should be taken bi-annually at minimum with comparisons drawn to time of prosthetic attachment. (C.) Key features of Peri-implant mucositis are listed. Probing depths in combination with inflammatory changes are associated with peri-implant mucositis. (D.) Peri-implantitis will often have suppuration, in addition to clinical signs of inflammation. Radiographs establish definite destruction of implant supporting bone.

cases (see Figure 3). In the progression of the peri-implantitis, cup/polishing brushes and air powder flow devices. Air abrasive severe bone lesions and crater-like defects may form.10 powder systems, originally used for removal of bacterial biofilm Comparisons should be made to a baseline radiograph from on teeth, have been applied to the treatment of peri-implantitis. the time of prosthetic ‘connection’ to the implant. Thus, Variants of this technique use a slurry of water/sodium bicar- stability confirmed by serial radiographs taken on an annual bonate or glycine powder delivered by pressurized air and basis during implant maintenance would be congruent with a water. A proper angulation of the tip, away from the implant clinician’s diagnosis of health or peri-implant mucositis. surrounding gingival tissue, is critical to avoid unwanted damage. Available studies indicate some efficacy in reducing probing 11 PERI-IMPLANT MUCOSITIS: NON-SURGICAL depths and bleeding at implant sites. MANAGEMENT The adjunctive use of chemotherapeutics, such as chlorhexi- The non-surgical management of peri-implant conditions is dine, has shown minimal or no additional benefit over me- focused on the reduction of inflammation by control of biofilm. chanical alone.12 Studies indicate that In general, studies have demonstrated the effectiveness of non- containing dentifrices effectively reduce the inflammation of surgical mechanical debridement and effective plaque biofilm peri-implant mucositis.13 Here, in addition to improvements control in treatment of peri-implant mucositis. Mechanical in plaque index and gingival inflammation, microbiological , whether managing mucositis or peri-implantitis, typi- benefit has been demonstrated; significantly fewer numbers cally involves the use of curettes to for supra- and sub-gingival of Gram-negative anaerobes were identified in the subjects biofilm removal. The implant literature describes the use of using tricolosan compared to controls, with more than 90% resin, carbon or curettes and special tips for ultrasonic reduction in P. gingivalis, Campylobacter rectus, Aggregatibacter instrumentation; the general principle is that titanium surfaces actinomycetemcomitans, and .14 Therefore, should be cleaned with implements less hard than titanium. it may be appropriate to assume that twice-daily use of Other devices used in mechanical approaches include rubber triclosan-containing toothpaste may enhance dental implant

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Figure 2. Peri-implantitis case. (A.) The radiographs present with bone loss around implant #29 is approaching the third thread. Note defective implant-abutment connection at #28. (B.) Clinical presentation. A minimal amount of keratinized gingival tissue is observed at the buccal. Probing depths are 6-7 mm in depth associated with #29. (C. and D.) Following initial periodontal therapy, surgical access demonstrates the destruction in bone. In part, due to the crater-like form of the bone damage, a decision was made to attempt regeneration.

maintenance and contribute to long-term success. Adequate treatment of peri-implantitis.15 Hence, clinical science has plaque control by the patient and enrollment into a contin- explored adjunctive benefits of local chemotherapeutics. uous maintenance program represent a key component of Adjunctive antiseptic agents, such as , have peri-implant disease treatment. Customized hygiene strategies been suggested for use in peri-implant disease therapy. (recommendation of specific brushes or interproximal However, with respect to chlorhexidine as an adjunct, only devices) should consider the prosthetic supra-structure and limited short-term (6 months or less) improvements in clinical the patient’s manual dexterity (see Louropoulou, Slot, van der parameters have been presented.16 In studies of non-surgical Weijden, Mechanical Self-Performed Of Implant approaches to peri-implantitis management, adjunctive anti- Supported Restorations: A Systematic Review, this publication). microbials, such as microspheres and doxycycline hyclate, in conjunction with mechanical debridement have PERI-IMPLANTITIS: NON-SURGICAL shown improvements in gingival inflammation and probing MANAGEMENT depths compared to instrumentation with chlorhexidine irri- gation.16,17 Further, long-term and randomized controlled The same mechanical therapies utilized in peri-implant investigations are warranted. mucositis management are employed in treating peri- implantitis (Figure 4). Again, these modalities aim to reduce Given the untenable long-term results of non-surgical treat- bacterial colonization on the surface of the implant; future ment of peri-implantitis, a surgical intervention, flap access seems corrective surgical phases depend on a relatively appropriate as the next step in managing peri-implantitis. The inflammation and plaque free environment for ideal results. surgeon managing peri-implantitis will rely upon approaches In general, non-surgical mechanical debridement has been analogous to periodontal surgical approaches—ranging from reviewed and found alone to be ineffective in the long-term resection to regeneration.

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Figure 3. Examples of peri-implant bone loss. (A.) #30 presents Figure 4. A Summary of the management of peri-implant disease. with saucer-like defect down to the third implant thread. The defect at #30 was grafted at the time of implant placement into site #29. (B.) Mesial of implant #12 demonstrates bone loss. Clinically, there was a corresponding probing depth of 7 mm and suppuration at the mesial site.

Note. The management of peri-implantitis and peri-implant mucositis both rely upon a non-surgical phase that aims to reduce or eliminate inflammation. Many of the paradigms applied to decision-making in surgical management of teeth with periodontal lesions can be drawn upon in the surgical management of peri-implantitis. As the clinical science develops one may expect this treatment algorithm to evolve and provide a greater PERI-IMPLANTITIS: SURGICAL MANAGEMENT specificity of actions. (*) The algorithm assumes a standard diameter 11.5 mm length implant. Shorter implants may warrant removal at earlier bone loss thresholds. When implant associated probing depth and bone loss is Abbreviations: APF –Apically positioned flap with minor osseous bone re-contouring, advanced or persists, despite the initial non-surgical treatment Bn – bone, ScRP – , AB – . provided, a surgical intervention of peri-implantitis is required (Figure 2). Surface decontamination strategies used in non- Surgical access will usually involve a full-thickness flap to allow surgical approaches may be applied now with the benefitof access and cleaning of the contaminated implant surface. Here, open access, created by an elevated gingival flap. Also, the the goal is to remove biofilm and create a theoretically removal of diseased granulation tissue and access to under- compatible surface for re-osseointegration. Literature supports lying bony architecture is facilitated. Bone morphology guides the use of various agents (e.g., saline, abrasive pumice, citric acid, the selection and composition of the surgical procedure. With chlorhexidine, and ) in surface decontami- only mild horizontal bone loss around implant(s), an apically nation as adjunct to surgical debridement. While these sup- positioned flap coupled with implantoplasty is suggested. In plements had favorable influence on re-osseointegration, no implantoplasty, high quality diamond burs and adequate irri- agent was found to be superior19 (see Table 1). Lasers have gation/evacuation are used to smooth the roughened implant also been used to decontaminate peri-implant sites once sur- surface to become less plaque retentive, thus reducing the gical access has been established. Human clinical studies have 18 progression of peri-implant bone loss. investigated CO2 and Er:YAG lasers used as a surgical adjunct in

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Table 1. Examples of implant surface decontamination strategies Given the greater clinical success achievable in managing peri- implant mucositis compared to the compromised osseo-  Mechanical means integration of peri-implantitis, the contemporary dental prac-  Implantoplasty with rotary instrumentation  Air powder abrasives tice must establish protocols to assess restored implants and  Curettes (e.g., resin, carbon-fiber) associated peri-implant tissues. Prevention and early inter-  Power instrumentation with specialized plastic tips ception of etiology and contributing factors associated with  Chemical means peri-implant disease should be emphasized.  Saline  Hydrogen peroxide  Chlorhexidine  Citric acid REFERENCES  Tetracycline 1. Albrektsson T, Donos N. Implant survival and complications. The Third EAO  Lasers consensus conference 2012. Clin Oral Implants Res 2012;23(suppl 6):63-5.  Photodynamic therapy 2. Mombelli A, Muller N, Cionca N. The epidemiology of peri-implantitis. A summary of current major implant surface decontamination strategies is Clin Oral Implants Res 2012;23(suppl 6):67-76. presented. Photodynamic therapy (PDT), though not commonly employed in fi private practice, has a growing body of clinical investigations into its use as an 3. Zitzmann NU, Berglundh T. De nition and prevalence of peri-implant implant decontamination strategy. PDT employs a photo-sensitizer dye that diseases. J Clin Periodontol 2008;35(8 suppl):286-91. reacts to low intensity visible light, between 660 nm and 905 nm, that forms a 4. Shibli JA, Melo L, Ferrari DS, Figueiredo LC, Faveri M, Feres M. cytotoxic species in the presence of oxygen. DNA or cytoplasmic membrane Composition of supra- and subgingival biofilm of subjects with healthy damage of bacteria are likely mechanisms of PDT. and diseased implants. Clin Oral Implants Res 2008;19(10):975-82. 5. Cortelli SC, Cortelli JR, Romeiro RL, et al. Frequency of periodontal decontamination; currently, it is difficult to conclude what pathogens in equivalent peri-implant and periodontal clinical statuses. additional benefit or contribution laser decontamination pro- Arch Oral Biol 2013;58(1):67-74. 17 vides to surgical access. 6. Mombelli A, Decaillet F. The characteristics of biofilms in peri-implant Regenerative approaches can be used in conjunction with sur- disease. J Clin Periodontol 2011;38(suppl 11):203-13. gical access, drawing upon the paradigms used in managing 7. Jepsen S, Ruhling A, Jepsen K, Ohlenbusch B, Albers HK. Progressive periodontal defects associated with teeth. Containable bony peri-implantitis. Incidence and prediction of peri-implant attachment loss. defects—walled defects associated with the implant—should be Clin Oral Implants Res 1996;7(2):133-42. more amenable by grafting to favorable gains in bone fill and 8. Luterbacher S, Mayfield L, Bragger U, Lang NP. Diagnostic characteristics reductions in probing depth. Debridement and implant surface of clinical and microbiological tests for monitoring periodontal and peri- decontamination are still essential prior to regenerative treat- implant mucosal tissue conditions during supportive periodontal therapy (SPT). Clin Oral Implants Res 2000;11(6):521-9. ment, as the infection must be completely eliminated before application of bone graft.20 Patient risk factors, such as smoking, 9. Etter TH, Hakanson I, Lang NP, Trejo PM, Caffesse RG. Healing after poorly controlled diabetes, and unsatisfactory oral hygiene, standardized clinical probing of the periimplant soft tissue seal: a histomorphometric study in dogs. Clin Oral Implants Res 2002;13(6): may hamper the success of peri-implant defect regeneration. 571-80. At present, heterogeneity of study designs and study quality prevent strong conclusions on the efficacy of regeneration in 10. Schwarz F, Herten M, Sager M, Bieling K, Sculean A, Becker J. Com- 21 parison of naturally occurring and ligature-induced peri-implantitis bone treating peri-implantitis. Still, there is promise in surgical studies defects in humans and dogs. Clin Oral Implants Res 2007;18(2):161-70. demonstrating the maintenance of probing depth improvements or bone fill at almost three years out.16,22 Notably in these 11. Renvert S, Lindahl C, Roos Jansaker AM, Persson GR. Treatment of peri- implantitis using an Er:YAG laser or an air-abrasive device: a randomized studies, implant maintenance was a crucial component of peri- clinical trial. J Clin Periodontol 2011;38(1):65-73. implantitis treatment, which presumably played a part in achieving the aforementioned results. Most recently, Chan and 12. Thone-Muhling M, Swierkot K, Nonnenmacher C, Mutters R, Flores-de- Jacoby L, Mengel R. Comparison of two full-mouth approaches in the colleagues conducted a systematic review and meta-analysis on treatment of peri-implant mucositis: a pilot study. Clin Oral Implants Res 23 the efficacy of surgical treatments for peri-implantitis. While the 2010;21(5):504-12. use of grafting and membranes tended to yield greater fi fi 13. Trombelli L, Farina R. Ef cacy of triclosan-based toothpastes in the improvements in probing depth and defect ll, the authors cite prevention and treatment of plaque-induced periodontal and peri- the need for higher quality and longer-term investigations. implant diseases. Minerva Stomatol 2013;62(3):71-88. 14. Sreenivasan PK, Vered Y, Zini A, et al. A 6-month study of the effects of CONCLUSION 0.3% triclosan/copolymer dentifrice on dental implants. J Clin Perio- Clinicians actively engaged in an implant maintenance pro- dontol 2011;38(1):33-42. gram play a crucial role in peri-implant disease assessment. 15. Renvert S, Roos-Jansaker AM, Claffey N. Non-surgical treatment of peri- Furthermore, the entire dental team must aim to rehabilitate implant mucositis and peri-implantitis: a literature review. J Clin Perio- the common that dental implants are invulnerable. dontol 2008;35(8 suppl):305-15.

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16. Nguyen-Hieu T, Borghetti A, Aboudharam G. Peri-implantitis: from microbiota and treatment. Med Oral Patol Oral Cir Bucal 2011;16(7): diagnosis to therapeutics. J Investig Clin Dent 2012;3(2):79-94. e937-43. 17. Muthukuru M, Zainvi A, Esplugues EO, Flemmig TF. Non-surgical ther- 21. Renvert S, Polyzois I, Claffey N. Surgical therapy for the control of peri- apy for the management of peri-implantitis: a systematic review. Clin implantitis. Clin Oral Implants Res 2012;23(suppl 6):84-94. Oral Implants Res 2012;23(suppl 6):77-83. 22. Roos-Jansaker AM, Lindahl C, Persson GR, Renvert S. Long-term stability 18. Romeo E, Ghisolfi M, Carmagnola D. Peri-implant diseases. A systematic of surgical bone regenerative procedures of peri-implantitis lesions in a review of the literature. Minerva Stomatol 2004;53(5):215-30. prospective case-control study over 3 years. J Clin Periodontol 2011;38(6):590-7. 19. Mellado-Valero A, Buitrago-Vera P, Sola-Ruiz MF, Ferrer-Garcia JC. Decontamination of dental implant surface in peri-implantitis treatment: a 23. Chan HL, Lin GH, Suarez F, Maceachern M, Wang HL. Surgical man- literature review. Med Oral Patol Oral Cir Bucal 2013 Nov 1;18(6):e869-76. agement of peri-implantitis: a systematic review and meta-analysis of treatment outcomes. J Periodontol; [Epub ahead of print]: doi:10.1902/ 20. Ata-Ali J, Candel-Marti ME, Flichy-Fernandez AJ, Penarrocha-Oltra D, jop.2013.130563. Balaguer-Martinez JF, Penarrocha Diago M. Peri-implantitis: associated

Acknowledgment The authors would like to thank and acknowledge Dr. Melody Daroogar Ward for providing some featured case materials.

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