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Home , Gingival fibers, Implant (medicine), Junctional epithelium

Health, Maintenance, and Recovery of Soft Tissues around Implants Yulan Wang, MD; Yufeng Zhang, PhD; Richard J. Miron, PhD

ABSTRACT Background: The health of peri-implant soft tissues is one of the most important aspects of necessary for the long-term survival of dental implants. Purpose: To review the process of soft tissue healing around osseointegrated implants and discuss the maintenance requirements as well as the possible short-comings of peri-implant soft tissue integration. Materials and Methods: Literature search on the process involved in osseointegration, soft tissue healing and currently available treatment modalities was performed and a brief description of each process was provided. Results: The peri-implant interface has been shown to be less effective than natural teeth in resisting bacterial invasion because gingival fiber alignment and reduced vascular supply make it more vulnerable to subsequent peri-implant disease and future bone loss around implants. And we summarized common procedures which have been shown to be effective in preventing peri-implantitis disease progression as well as clinical techniques utilized to regenerate soft tissues with bone loss in advanced cases of peri-implantitis. Conclusion: Due to the difference between peri-implant interface and natural teeth, clinicians and patients should pay more attention in the maintenance and recovery of soft tissues around implants. KEY WORDS: osseointegration, peri-implant soft tissue, peri-implantitis, peri-mucositis

INTRODUCTION recently, evidence has demonstrated that the long-term When dental implants were first discovered and used to survival of osseointegrated implants was also partly replace missing teeth, most clinicians focused primarily dependent on the transmucosal healing and stability on implant stability as the biggest factor in and predictor around the implant collar, termed “peri-implant 11 for future success, and this trend has in part continued mucosa.” This attachment of the soft tissue to the as the primary research criterion for implants. 1–6 coronal portion of an implant acts to provide a protec- Osseointegration was and still is considered as the most tive seal which prevents the development of bacterial 12,13 important factor in maintaining implant stability, invasion and future inflammation. Thus, the soft whereas the role of soft tissue healing and maintenance tissue seal is necessary for stable osseointegration and 14–16 around implants has been somewhat neglected. 7–10 More long-term survival of implants. One of the key findings relating to peri-implant The State Key Laboratory Breeding Base of Basic Science of Stoma- mucosa was the direction of gingival fibers compared tology (Hubei-MOST), Key Laboratory of Oral Biomedicine Ministry with the natural (Figure 1). This key diffe- of Education, School & Hospital of Stomatology, Wuhan University, rence explained the increased ability of to pen- Wuhan, China etrate the epithelial layer and subsequent connective Corresponding Author: Prof.Yufeng Zhang, The State Key Laboratory tissue thus increasing the breakdown of soft tissues Breeding Base of Basic Science of Stomatology (Hubei-MOST), Key 17 Laboratory of Oral Biomedicine Ministry of Education, School & around implants. Therefore, if patient compliance is Hospital of Stomatology, Wuhan University, 237 Luoyu Road, Wuhan not fully obtained and proper is not 430079, China; e-mail: [email protected] maintained, inflammatory changes in the soft tissues © 2015 Wiley Periodicals, Inc. surrounding dental implants will develop. 18 This DOI 10.1111/cid.12343 inflammatory process in the peri-implant mucosa

1 2 Clinical Implant Dentistry and Related Research, Volume *, Number *, 2015

Figure 1 Differences between the connection of soft tissues to natural teeth and dental implants. Note the arrangement of gingival fibers in a parallel orientation on implant surfaces. begins with reddening and swelling, and once bleeding Interestingly, more recent evidence has demon- on probing is initiated, the condition is then termed strated that a gap of about 60 μm between the implant peri-implant mucositis. If this condition is left surface and host bone is created, 24,25 and it may extend to untreated, it may lead to progressive and irreversible 100 to 500 μm over time. 26 This gap typically contains a destruction of implant-surrounding tissues including oxide layer which comes into contact with the loss of alveolar bone around dental implants and blood plasma proteins and body fluids and is later ultimately lead to implant failure. 19 Thus, the structure adsorbed onto the implant surfaces immediately after and biological events that take place during implantation, forming a “conditioning film.” 23,27 Several osseointegration and soft tissue attachment are impor- factors such as surface roughness 28 as well as surface tant components of implant survival and maintenance. hydrophilicity 29 are key determining factors influencing This review article aims to describe the composition of protein adsorption and are subsequently able to stimu- soft tissues around implants, how to maintain their late and induce attachment on the implant surface. 30 health and survival, and how to deal with peri-mucositis The cell population which first occupies the implant and peri-implantitis progression and its reversibility. surface is primarily composed of inflammatory cells, and many investigators refer to this original phase BIOLOGICAL EVENTS DURING of implant healing as the “immune-inflammatory OSSEOINTEGRATION response.” 23 Within 24 hours following implant inser- Osseointegration, which has also been called“functional tion, neutrophils dominate the implant site. In the 2 to 4 ankylosis,” 20 was initially defined as “a direct structural days following, an increasing number of infiltrating and functional connection between ordered, living bone macrophages and monocytes appear in the peri-implant and the surface of a load-bearing implant.” 21 More gap. These cells are responsible for removing the debris, recently, authors have modified the definition of as well as secreting large quantities of cytokines and osseointegration. In 2012, Zarb and Koka defined growth factors responsible for stimulating future mes- osseointegration as “a time-dependent healing process enchymal cell recruitment and proliferation, angiogen- whereby clinically asymptomatic rigid fixation of esis, and collagen matrix deposition. 31,32 alloplastic materials is achieved and maintained in bone A simultaneous and equally important event that during functional loading.” 22 The definition explains takes place during osseointegration is the formation of a in more detail that the stages of osseointegration blot clot and future stimulation of angiogenesis. On the are divided into three overlapping steps: early first day after implantation, a blood clot is formed adja- immune-inflammatory response, angiogenesis, and cent to the implant surface, 23 and neovascularization osteogenesis. 23 begins within 24 hours. While infiltrating macrophages Soft Tissues around Implants 3

Figure 2 Timeline for osseointegration of dental implants with respect to changes over time.

and monocytes migrate to the bone wound by day 4, the during healing abutments, final abutments, imprints, blood clot is gradually replaced by differentiating mes- and final restorations, offering numerous opportunities enchymal cells recruited from the bone marrow around for inflammation to develop during each of these pro- newly developing blood vessels. 33 These mesenchymal cedures. Immediately after insertion, the cells differentiate into osteoblasts which are influenced implant-mucosa interface also forms a blood clot that is by both growth factors and surface topography where infiltrated by incoming neutrophils. If bacterial invasion they begin to attach to the implant surface and deposit is not present, the initial mucosa begins forming a peri- collagen matrix. 24,34 New bone formation on the implant implant seal by the fourth day postimplantation. This surface is observed in 5 to 7 days 23,24 when calcification healing process takes 8 weeks to complete the peri- from the host bone onto the implant surface is also mucosa seal, 38–40 whereby leucocytes are typically con- observed. 35 By 4 weeks, new bone formation is observed fined to the coronal portion of the implant, and on the implant surface (contact osteogenesis) connect- collagen-producing fibroblasts are typically found in the ing with bone formed on the host bone (distant osteo- apical portion of the peri-implant interface. genesis). 36,37 After 8 to 12 weeks, the peri-implant Histologically, the peri-implant mucosa is com- interface is completely replaced by mature lamellar bone posed of a well-keratinized oral , sulcular epi- in direct contact with the implant surface, thus complet- thelium, and a thin barrier epithelium facing the ing the initial phase of osseointegration 23,31,32 (Figure 2). abutment equivalent to the around teeth, termed the peri-implant junctional epi- THE SHORTCOMINGS OF SOFT TISSUE thelium. The height of the peri-implant junctional epi- HEALING AROUND IMPLANTS thelium is approximately 2 mm, and the connective One of the issues often overlooked during implant tissue underlying this junctional epithelium is around placement is the fact that implant insertion creates a 1.0 to 1.5 mm. 13 Thus, the mean biological width wound in both hard and soft tissue. It is also noteworthy (including the sulcus depth) may often exceed 3 mm. 41 that soft tissues suffer more drastic changes than their When biological width is reduced at any site of the peri- bony counterparts. Typically, soft tissues need to regen- implant mucosa, marginal bone resorption is typically erate a greater amount of tissue, and subsequent surger- observed so that the biological width is adjusted to com- ies and/or temporary changes further aggravate pensate for these changes. 42 Many factors have been soft tissues with a number of new adaptation periods shown to influence biological width around implants. 4 Clinical Implant Dentistry and Related Research, Volume *, Number *, 2015

Various implant system (e.g., tissue-level vs bone level first quantifiable differences between these two struc- implants, one-piece vs two-piece), 43–45 implant material tures is the significantly deeper mean in probing depth (e.g., titanium, zirconium gold alloy), 46 implant surface at implant sites compared with tooth sites. 59,60 This dif- characteristics (macro design, topography, hydrophilic- ference occurs irrespective of probing pressure, and it is ity, and surface coating), 47,48 loading protocol (e.g., also noted that the mean percent- immediate vs early or delayed), 49 and implant protocol age at implant sites is much higher than that of normal (e.g., soft tissue flap design, flapless procedure) 50,51 all teeth. 59,60 Furthermore, it has been documented that have different effects on biological width. However, changes in probing depth forces around peri-implants more in-depth research is needed to verify the signifi- are more sensitive to slight variations, making accurate cance of each of these factors. analysis more difficult. 59,60 This phenomenon may With regard to the structure of the peri-implant reduce the efficacy of peri-implant probing and provide mucosa, the amount and distribution of fibroblasts, col- less reliable evaluation of the inflammatory situation. lagen, and blood vessels is quite different from those of Furthermore, slight increases in pressure may some- a natural tooth (Figure 1). In the supra-crestal soft times result in injury when the probe goes beyond the connective tissue around implants, fewer fibroblasts and peri-implant seal. It is important, however, to note that collagen fibers oriented in the axis of the implant are not all investigators agree with the drastic changes of present than in natural teeth. Interestingly, mesenchy- probing depth between implants and teeth, 61 although mal cells with a high number of fibroblasts are found the general consensus is that probing depth is increased near the implant surface, typically interposed between in implant sites, BOP is also more sensitive to minor collagen fibrils. 52 One of the main differences among changes in pressure in implant sites. these collagen fibers is their orientation relative to natural teeth. In most cases, the collagen fibers are found Fiber Orientation and Distribution oriented parallel or parallel-oblique to the smooth As noted earlier, collagen fibers in natural teeth are per- implant surface, whereas in natural teeth, the fibers are pendicularly oriented, attaching from the tooth cemen- found perpendicular to the tooth embedded within tum to the alveolar bone serving as a barrier to epithelial as Sharpey’s fibers. 13,53,54 Some research has downgrowth and bacterial invasion. 62 Since dental shown that rougher surfaces with either microgrooves implants lack a cementum layer, collagen fibers typically or porous plasma-sprayed surfaces form collagen fibrils orient themselves in a parallel manner to the implant that are oriented slightly more to the perpendicular than surface, making them much weaker and more prone to their smooth surface counterparts. 55–57 Although more periodontal breakdown and subsequent bacterial inva- perpendicular, these surfaces still fail to provide the pro- sion. 17,63 The lack of a proper is also a tection barrier provided by natural teeth. Another dis- potential reason for faster inflammation progress, as dis- cernible difference between soft tissue around natural cussed below. 64 teeth and that of dental implants is the number of blood vessels around both. Typically, few to no blood vessels Microbiota and Inflammatory Response are found in the zone adjacent to the implant surface. 53 When implant surfaces began to show signs of peri- A clearing technique visualizing carbon-stained blood odontal plaque and biofilm accumulation, researchers vessels showed that the vascular networks of the peri- began to determine the periodontal pathogens respon- implant mucosa are derived from the terminal branches sible for peri-implantitis. 65,66 It is now well understood of larger blood vessels originating from the periosteum that the formation of a biofilm on an implant surface is of the bone at the implant site. 58 Because of the numer- influenced by the surface properties of the implant, such ous differences between soft tissues around natural teeth as chemical composition, roughness, and surface free and around implant surfaces, several key components as energy. 67 Studies have demonstrated that Staphylococcus listed below differ greatly between the systems. aureus is common in deep peri-implant pockets closely linked to suppuration and bleeding on probing. 68,69 Peri-Implant Probing Interestingly, S. aureus is not closely related to chronic The importance of either tooth or peri-implant probing periodontitis and seems to be more specific to implant has been well documented in the literature. One of the surface contamination. 70 Apart from this difference, the Soft Tissues around Implants 5 bacteria species found in the subgingival microbiota in critical importance for the longevity of successful both natural tooth periodontal tissues and in peri- osseointegrated implants. A study which purposely implant soft tissue are similar in terms of the occurrence banned oral hygiene around dental implants for a short and frequency of periodontal pathogens. 71 period of time demonstrated a cause–effect relationship Another important difference in the inflammatory between the accumulation of bacterial plaque and the response of soft tissues in natural teeth and implant development of peri-implant mucositis. 18 Recent studies surfaces is their different cellular responses. Inflamma- have shown that bacterial colonization occurrs within 30 tory lesions in peri-implant sites are infiltrated with a minutes following implantation 81 and becomes stable high proportion of B cells and plasma cells, which after a 2-week period. 82,83 Thus, the primary objective of is similar to and aggressive maintenance and recovery of any implant regiment is to periodontitis. 72–74 Although the development of peri- remove the bacterial plaque and/or . implantitis and periodontitis follows a similar pattern, the dynamics are quite different. Studies in human and MAINTAINING THE HEALTH OF PERI-IMPLANT animals show that there is very little difference in host SOFT TISSUE response between natural and implant-supported teeth Of course, the dental provider has a role in guiding 75 in the initial phase, but disease progression occurs more implant stability following osseointegration; however, rapidly with subsequent bone loss in the peri-implant proper maintenance of the peri-implant soft tissue 64,76 lesions than in natural teeth. The reason might lie in health is largely in the control of the patient’s own oral the lack of an intact supra-crestal connective tissue fiber hygiene regimen. Patient self-management includes 77,78 compartment in peri-implant soft tissue which is able mechanical methods and chemical ways to control to wall off the lesions; the inflammatory cell infiltrates biofilm formation and subsequent plaque/calculus generally do not penetrate the alveolar bone marrow in accumulation. periodontal tissues. 79 Furthermore,the vascular supply as discussed below is reduced, decreasing the number of PATIENT SELF-MANAGEMENT infiltrating neutrophils and B cells. Mechanical Methods Vascular Supply Tooth Brushing. Manual and power brushes are both The vasculature of the periodontal soft tissues is derived excellent and necessary means to remove dental from two sources. One source is the supra-periosteal plaque. These include manual squish grip brushes, 84,85 vessels lateral to the , and the other is the sonic tooth brushes, ionic , 86 and counter- vessels of the periodontal ligament. When the natural rotational powered toothbrushes. 87 Each is effective in tooth is extracted, the future implants have lost their plaque reduction and maintaining the gingival health vascular supply from the periodontal ligament. 58 Fur- of peri-implant soft tissues, and it is advised that thermore, because of the dense fibers adjacent to the patients brush a minimum of twice daily. Swierkot inner zone of the implant surface, there is also less vas- and colleagues 88 found no significant difference cular structure in the soft connective tissue directly adja- between the various brushes utilized, but other inves- cent to the implant surface compared with the natural tigators found that powered brushes were more effec- tooth. 52 As a sufficient vascular supply is necessary for tive in reducing plaque and . 89,90 Since the wound healing and tissue repair by delivering numerous comparison of manual and powered toothbrushes does cell types and growth factors, the lack of an abundant not show a definitive advantage of one type over blood supply has been suggested as one of the key reasons another, it is typically advised that patients with good for the extensive progression of inflammation and lack of dexterity can choose either option, but as the patient healing in soft tissues surrounding implants. 80 ages, it is increasingly important to suggest powered toothbrushes. MAINTENANCE AND RECOVERY OF SOFT TISSUE HEALTH AROUND IMPLANTS Interdental Cleaning. Interdental cleaning devices are Because of the vast differences between natural used to improve the efficacy of toothbrushes, especially teeth and dental implants, their maintenance is of in regions with small interspaces. Traditional string 6 Clinical Implant Dentistry and Related Research, Volume *, Number *, 2015

floss and interdental brushes are useful devices, and rinses 99 ; however, very few studies have been conducted the width of the interdental space determines which to particularly on implants. is also available use.91 Other methods to remove interdental plaque in form, which has also been demonstrated as include using water floss; however, a lack of controlled effective. 100 clinical trials makes it difficult to speculate on its effectiveness. 92 PROFESSIONAL MANAGEMENT It is important that patients receiving implants be placed Chemical Methods on a strict recall programme so professional manage- Chemical agents may provide additional benefits to ment can assess changes over time, which will help mechanical plaque control. Of course, it must be borne maintain the health of dental implants. Professional in mind that although they are not able to replace management may include mechanical , mechanical brushing, they may be utilized in combina- application of phosphoric acid etching, or injections tion approaches. with chlorhexidine.

Triclosan/Copolymer Toothpaste. (0.3%) Mechanical Debridement together with methyl vinyl ether-maleic anhydride A qualified dentist is required to assess the state of the polymer (2.0%) in a sodium fluoride silica-based osseointegrated implant and make decisions on the toothpaste has been demonstrated to reduce plaque and mechanical debridement program most suitable for gingival inflammation. 93,94 each placement. Typically, patients may be placed on recall every 6 to 12 months for supra and subgingival Fluoride-Containing Mouth Rinses. Amino fluoride/ debridement of calculus and plaque around implants stannous fluoride mouth rinses are an excellent choice with carbon fiber curettes. In general, patients with a as a . In one study, it was shown that single tooth crown or bridge with two implant abut- the results for plaque control were comparable with ments should be on recall once per year with risk factors those for chlorhexidine gluconate mouth rinses, and the analyzed. Typically, if a bridge has more than two patients enrolled in the study preferred the taste. 95 Fur- implants, it is advised to place the patient on a 6-month thermore, fluoride-containing mouth rinses are able to recall program which also includes patients with full reduce pro-inflammatory molecules in peri-implant arch bridgework retained by implants or implant- crevicular fluid. 96 retained dentures. In patients with or at a higher risk of developing peri-implant disease caused by systemic Essential Oils Mouth Rinse. Listerine, Pfizer Inc, Man- factors such as smoking, personal factors such as bad hattan, New York, United States, used twice daily for 30 oral hygiene, or genetic factors, the recall interval should seconds directly after standard oral hygiene mechanical be shorter (usually half of the suggested time). If, for brushing, has been shown to provide a reduction in some reason, peri-implant soft tissue becomes infected plaque index, gingival index, and bleeding index. 97 More or shows signs of attachment loss, a much stricter recently, a variety of oils such as cinnamon oil and clove regimen may then be necessary for implant health, typi- oil have been studied for their long-term antibacterial cally with recall once every 12 weeks until soft tissue effect, although more research is necessary to character- healing is observed. It is up to the healthcare provider to ize their beneficial effects on implants fully. 98 make optimal decisions for the long-term survival of implants.101 Chlorhexidine. Chlorhexidine gluconate (0.12%) is used to control plaque and maintain oral hygiene in Phosphoric Acid Etching Gel postrestorative phases following implant placement. 87,95 The application of phosphoric etching gel in the peri- Furthermore, irrigation with 0.06% chlorhexidine using implant sulcus has been used as an alternate method for a powered oral irrigator (Water Pik, Water Pik Inc, Fort improving peri-implant soft tissue. Strooker and col- Collins, Colorado, United States) with a special leagues have demonstrated that application of a 35% subgingival irrigation tip has been shown to be more phosphoric etching gel at pH 1 results in an instant effective than chlorhexidine gluconate (0.12%) mouth reduction of colony-forming units, proving that it is an Soft Tissues around Implants 7 effective way to fight against bacteria. 102 Although long- Curettes. Typically, carbon curettes are advised again for term clinical studies are still lacking, the use of phos- the recovery of implants. Although metal curettes may phoric etching has been demonstrated at least in part to be acceptable for zirconia implants, 104 they leave too counteract infected peri-implant soft tissues by decreas- many scratches on the surface of titanium implants and ing bacterial counts and may be a viable option in thus should be avoided. 105 Although titanium curettes already infected implant sites. are an option, and one study has shown less damage observed by scanning electron microscopy, 106 nonmetal Chlorhexidine alternatives (carbon-fiber curettes, teflon curettes, Much like home mouth rinses with chlorhexidine, its plastic curettes) 107–109 are the preferred option. It is note- application by a professional dental provider via local worthy that a growing number of ultrasonic devices are injections has also been demonstrated as a means to being used for plaque and calculus removal in peri- improve peri-implant soft tissue healing following peri- implant tissues as discussed next and are therefore the implant contamination. Groenendijk and colleagues preferred method for mechanical debridement once showed that a 0.2% chlorhexidine to the inner plaque and calculus are found subgingivally. part of implants at second-stage surgery demonstrated a significant inhibition of growth and acquisition of bac- Ultrasonic Devices. A number of studies have shown the teria by the peri-implant interface. 103 efficacy of using ultrasonic devices for reducing bacterial plaque and BOP scores. Renvert and colleagues demon- RECOVERING THE HEALTH OF PERI-IMPLANT strated that plaque scores decreased from 73% to 53% SOFT TISSUE (p < .01), and bleeding scores were also significantly Because of the growing use of dental implants, more and reduced following ( p < .01).110 Park and col- more cases have now been reported as demonstrating leagues demonstrated on implants with an SLA surface signs of peri-implantitis and peri-mucositis. Of primary that metal scaler tips were more effective in eliminating importance in the recovery of these implants is promot- bacteria and reducing bacterial adherence by smoothing ing the health of the peri-implant soft tissue by elimi- the implant surface than plastic and carbon scaler tips. 111 nating biofilm and calculus. Once again, this may be With regard to machined surfaces, the scratches caused achieved through oral hygiene techniques at home, but by a metal scaler do not significantly affect the amount more emphasis is now placed on the healthcare provid- of biofilm that adheres, 112 and it has been demonstrated er’s efforts at disease resolution. Therefore, patient self- that a smoother surface for soft tissue attachment is management is identical to that mentioned in the preferred since bacterial adhesion is reduced on these section “maintaining the peri-implant soft tissue surfaces. It has been demonstrated that ultrasonic health”; however, we discuss next the professional means scalers do not show an increase in implant temperatures to improve peri-implant soft tissues once peri-implant when the cooling system is used properly. 113 soft tissue is present. Adjunctive PROFESSIONAL MANAGEMENT When the microbial count increases during acute infec- Mechanical Debridement tions of peri-implantitis, it may become necessary to To recover periodontal soft tissues around implants fol- treat with antibiotics. Antibiotics are used to enhance lowing peri-implantitis, it becomes vital that the patient the effect of the mechanical debridement and prevent is followed up regularly. During these appointments, the future recolonization of bacteria. Minocycline supra and subgingival debridement of the implant microspheres are used because of their sustained release surface becomes vital, as the main goal is to remove the of antibacterial ingredients up to 12 months, and studies biofilm and calculus without altering the topography have shown that they are effective in reducing plaque, of the implant surface. Curettes and ultrasonic devices and probing pocket depth as well as BOP. 114–116 with polyether-etherketone-coated tips are the most Amoxicillin, metronidazole, and their combination are common approaches, and patients are advised to be usually delivered as local applications. The placed on a recall program every 12 weeks until implant combination of amoxicillin and metronidazole showed inflammatory resolution is obtained. significant inhibition on the growth of adherent 8 Clinical Implant Dentistry and Related Research, Volume *, Number *, 2015

Streptococcus sanguinis and 117 NONSURGICAL DECONTAMINATION AND and much lower bacterial resistance. 118 Furthermore, INFECTION CONTROL systemic antibiotics may be used to increase the antimi- As peri-implantitis is a bacterial infectious disease, the crobial level in the peri-implant crevicular fluid to first thing to do before reconstructive therapy takes place 105 support the effect of mechanical debridement, but no is to control infection. To this end, and prior to surgical sound scientific basis has been found for the use of intervention, the peri-implantitis site should demon- 119 systemic antibiotics. strate no bleeding on probing and exhibit no suppura- tion. 11 The mechanical decontamination methods for HOW TO RECONSTRUCT THE IMPLANT SOFT peri-implantitis include mainly curettes, air-abrasive TISSUE FOLLOWING PERI-IMPLANTITIS devices, ultrasonic devices, and lasers (Table 1). Peri-implantitis is accompanied with crestal bone loss, bleeding on probing, and the possibility of suppuration. Air-Abrasive Systems It is very difficult for the clinician to manage such a Air-abrasive systems are based on the air spray of disease as the resulting implant surface has lower blood powders made from a variety of materials including supply than the natural surface, and if the disease is left sodium bicarbonate, sodium hydrocarbonate, 122 untreated, it may well lead to implant failure. 120 Various calcium phosphate, 123 erythritol-chlorhexidine, 124 and studies have revealed that the prevalence of peri- amino acid glycine. 125 They have been shown to be effec- implantitis ranges from 2.7% to 47.1% 121 and that as tive in eliminating biofilms and calculus both in vivo implants become more popular, the necessity for effec- and in vitro. 126 Typical devices include a specially tive strategies to reconstruct peri-implant tissues will be designed nozzle, which is used for horizontal exit of air equally important. powder mixture. 127 It is recommended that the nozzle be

TABLE 1 Different Options for Decontamination of Implant Surface Methods Kinds Introduction

Curettes Metal Efficient in reducing bacteria but causes obvious scratches on the surface of titanium implants Nonmetal Causes less damage to implant surface but is vulnerable and less efficient Ultrasonic Metal Better efficiency and less bacterial adhesion, does not cause temperature change device when cooling system is used properly Nonmetal Air abrasive Sodium bicarbonate, Efficient in bacterial reduction, but the high abrasiveness causes change in system sodium hydrocarbonate microstructure of implant surface and has remnants on the implant surface Calcium phosphate Efficient in bacterial reduction, has remnants on the implant surface Aminoacidglycine Mostacceptedpowders,lessdamagetoimplant surface Erythritol-chlorhexidine Newly founded method, more efficient in bacterial reduction than glycine Lasers Diode lasers Not to cause any damage to implant surface at 980 nm but useful in destruction of bacterial cells, cause temperature change when used continuously Nd:YAG Effectiveinbacterialreduction,butitcausesextensive melting and damage to the implant surface Er:YAG Capable of effectively removing plaque and calculus without injuring the implant surfaces, cause temperature change when used continuously

CO 2 lasers Won’t cause excessive titanium accumulation improve new bone formation by effective decontamination, cause temperature change when used continuously Antibiotics Local Useful adjunctive therapy for mechanical debridement, especially when it is combined with controlled release system Systemic May increase the antimicrobial level in the peri-implant crevicular fluid Soft Tissues around Implants 9

137 moved circumferentially around the implant surface in 810-nm diode laser. The CO 2 laser as well as the equal fashion in order to decontaminate the implant Nd:YAG laser have been used to a limited extent in den- 128 surface. tistry. The CO 2 laser has lower penetration depth in soft 138 One of the main drawbacks of the air-polishing tissues than the Nd:YAG lasers. In contrast, CO 2 lasers technique is that it increases implant surface roughness, at an energy density of 100 J/cm 2 can destroy microbial which in turn increases bacterial adhesion. The standard colonies including S. sanguinis and P. gingivalis without powdered air-abrasive system (sodium-carbonate) damage to the tooth root surface. 139 Furthermore, in proved unsuitable for implant instrumentation because another study, Deppe and colleagues found that CO 2 of the high abrasiveness revealed by SEM examination, laser-assisted therapy of ailing implants did not cause whereas low-abrasive amino-acid glycine powder is rec- excessive titanium accumulation in tissues, thus making ommended for debriding implant surfaces as it does no it a suitable and safe method for implant decontamina- 129 140 damage to hard or soft tissues. Petersilka and col- tion. Although CO 2 is relatively stable for titanium leagues compared a low abrasive air-polishing powder decontamination, its combination with Nd:YAG lasers with hand instruments and found that the powder can produce the undesirable result of extensive melting resulted in a significantly greater reduction in mean in irradiated areas and damage to the microstructure of CFU (log 1.7 1 0.98 and log 0.61 1 0.79, respectively; the implant as confirmed by SEM examination. 135 p < .05) from pockets of 3 to 5 mm depth. 126 Another Promising results have also been observed with the study showed that air-abrasive powders produced a Er:YAG laser in the treatment of peri-implantitis, and 0.8 to 0.5 mm reduction in periodontal depth and a it is the most popular choice at present. Kreisler and reduction in bacteria ( Pseudomonas aeruginosa , Staphy- colleagues demonstrated that the Er:YAG laser has a lococcus aureus and Peptostreptococcus anaerobius ) at 1 high bactericidal potential regarding common implant month. 130 Drago and colleagues constructed a new for- surfaces, even at low energy densities. 141 A study by mulation consisting of erythritol and chlorhexidine Matsuyama and colleagues showed that an Er:YAG powders, and its in vitro antimicrobial and antibiofilm laser at 30 mJ/pulse and 30 Hz with water spray was effects on bacteria ( S. aureus , Bacteroides fragilis , and capable of effectively removing plaque and calculus Candida albicans ) were stronger than the standard without injuring the implant surfaces. 142 Schwarz and glycine powder used in air-polishing devices. 124 Apart colleagues observed that the Er:YAG laser resulted in from abrasiveness, another potential disadvantage of air a statistically significant higher reduction of BOP powder abrasive systems is the remnants. A study by than mechanical debridement with plastic curettes Tastepe and colleagues showed that although the powder and antiseptic therapy. 143 Takasaki and colleagues was effective in biofilm removal, powder particle rem- demonstrated that degranulation and implant surface nants were observed on and impacted on the titanium debridement were obtained effectively and safely by the surface. 123 In the HA and HA + TCP group, a calcium Er:YAG laser and that a favorable formation of new content varying between 2% and 5% was observed. bone was observed on the laser-treated implant surface histologically. 144 Lasers Kreisler and colleagues performed an extensive Since their first application in dentistry in 1989, 131 lasers study of numerous lasers including Nd:YAG, Ho:YAG, have gained popularity in different aspects of dentistry Er:YAG, CO 2, and diode lasers for implant decontami- and have been utilized in peri-implant decontamina- nation. 138 It was found that Nd:YAG and Ho:YAG were tion. There are a variety of options for decontamination not suitable for implant surface decontamination of implant surfaces including semiconductor diode because of partial melting, cracking, and crater forma- lasers, the solid state laser Nd:YAG, Er:YAG lasers, and tion on implant surfaces irrespective of the power 132–134 gas lasers such as CO 2 lasers. output. The Er:YAG and CO 2 lasers were recommended It was found in an in vitro study that the 980-nm for use at low power settings so as to avoid surface diode laser caused little or no damage to implant sur- damage. However, the diode laser did not cause surface faces 135 while still being useful for bacterial reduction of changes. Thus, despite their being popular choices, P. gingivalis -contaminated implants. 136 This result has care must be taken when implants are decontaminated since been verified in clinical testing with a similar with either CO 2 or Er:YAG lasers to avoid temperature 10 Clinical Implant Dentistry and Related Research, Volume *, Number *, 2015 increases above the critical threshold (10°C) after 10 synthetically fabricated hydroxyapatite performed worse seconds of continuous irradiation. 145,146 than xenografts. 152 Although the data comparing materials for the treatment of peri-implantitis SURGICAL TECHNIQUES remain very limited, it has been observed in numerous Typically, surgical techniques and reconstructive proce- studies that a xenograft in combination with a dure are more effective but limited to moderate to severe resorbable membrane increases clinical attachment peri-implantitis. Below is a list of various techniques level. 152,153,156–158 used for the treatment of peri-implantitis. ADDITIONAL CAUSES OF PERI-IMPLANT Apically Positioned Flaps Apically positioned flap surgery is aimed at decontami- Although the aim of this review article was to examine nating the implant surface and exposing the affected differences between soft tissues found in natural teeth part of the implant to the oral cavity for better self- and dental implants as well as their related health and managed oral hygiene, 147 often accompanied by osteo- maintenance programs, it is also vital to state that many plasty. 148 This technique is very similar to apically additional factors and etiologies are constantly being positioned flaps for natural teeth and enables reduced investigated for their possible roles in peri-implantitis. pocket debts, facilitating patient hygiene. This technique For example, recent reports have suggested that cement- has clear drawbacks and is only recommended for retained crowns have been more prone to peri- nonaesthetic regions, however. 149 implantitis when compared with their screw-retained counterparts. 159–161 Some reports suggest that when sur- Access Flap Surgery gical flaps were raised to treat peri-implant bone loss, Access flap surgery is a surgical way to decontaminate over 70% of cases presented excessive cement in cement- the implant surface while maintaining the soft tissues retained crowns. 162 As a result from over-contour of around the affected implant. The aim of this surgery is cement, oral bacteria accumulation and a greater to maintain the soft tissue around the implant neck, and inflammatory response leading to eventual bone loss it is recommended when bone loss is minimal. Follow- pose a greater risk for peri-implantitis. 163 For these ing the access flap, the technique may be combined with reasons, it has become more mainstream to use screw- various other methods such as curettes, air-abrasive retained implants when possible or to modify cementing devices, ultrasonic devices, and lasers to enhance clean- techniques to avoid excess cement in peri-implant soft ing efficacy. 150 tissues. 164 Another area of research which has gained A regenerative technique is mainly utilized to tremendous awareness over the last decade is the effect support the tissue dimensions to avoid mucosa reces- of micro-gaps between implant components and their sion. After decontamination of the implant surface, a effect on bacterial microleakages. 165,166 Some investiga- graft may be placed around the implant, filling the peri- tors have reported that these gaps have been reported as implant defect. The graft commonly used is either large as 70 um implant-abutment interface, and implant autologous bone 151 or bone substitutes, 152 and combined design may affect the potential risk for invasion of oral with or without a resorbable or nonresorbable mem- into the fixture-abutment interface brane. 151,153 Furthermore, the use of a connective microgap under dynamic loading conditions. 165,167–170 tissue graft with a bone graft may be advantageous Further research to improve the implant to abutment aesthetically. 154 connection will further decrease the likelihood of soft The long-term goal of a regenerative procedure and hard tissue inflammation around implants. should be the re-adhesion of the peri-implant soft tissue and further enhancement of bone regeneration around SUMMARY AND CONCLUSIONS the implant surface. The change in probing depth has Osseointegration is a special kind of bone healing also been compared for various bone grafting materials. process, and the intact peri-implant seal plays an impor- Aghazadeh and colleagues demonstrated that xenografts tant role in protecting the alveolar bone from bacterial are better than autogenous grafts in reducing the invasion in the oral cavity. However, because of the probing depth, 155 and others have demonstrated that structural differences between implants and natural Soft Tissues around Implants 11 teeth, there are drawbacks in peri-implant soft tissue 2. Albrektsson T, Branemark PI, Hansson HA, Lindstrom J. healing compared with natural teeth such as deeper Osseointegrated titanium implants. Requirements for probing depth, weaker connective tissue attachment, ensuring a long-lasting, direct bone-to-implant anchorage faster inflammatory expansion, and reduced vascular in man. Acta Orthop Scand 1981; 52:155–170. 3. Becker W, Goldstein M. Immediate implant placement: supply, making the implant more vulnerable to bacterial treatment planning and surgical steps for successful accumulations and other external stimulations. Thus, it outcome. Periodontol 2000 2008; 47:79–89. is clear that implant surfaces necessitate more attention 4. De Bruyn H, Vandeweghe S, Ruyffelaert C, Cosyn J, to the maintenance of peri-implant soft tissue health. It Sennerby L. Radiographic evaluation of modern oral is also vital that patient self-management is rigorously implants with emphasis on crestal bone level and relevance employed, and this should be stressed at each dental to peri-implant health. Periodontol 2000 2013; 62:256–270. consultation. Dentists have a variety of means to 5. Degasperi W, Andersson P, Verrocchi D, Sennerby L. One- promote soft tissue health around implants, such as year clinical and radiographic results with a novel hydro- philic titanium dental implant. 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Quality assessment of paring the different options available to dentists to gen- reporting of animal studies on pathogenesis and treatment erate long-term predictable results. Future research of peri-implant mucositis and peri-implantitis. A system- should better define the most predictable methods for atic review using the ARRIVE guidelines. J Clin Periodontol decontamination of implant surfaces and characterize 2012; 39(Suppl 12):63–72. the effects of surface material and surface topography on 9. Albrektsson T, Buser D, Sennerby L. Crestal bone loss and the various implant systems. An ever-increasing number oral implants. Clin Implant Dent Relat Res 2012; 14:783– of implant companies offer various soft tissue connec- 791. tions either to the abutments in bone-level implants or 10. Albrektsson T, Dahlin C, Jemt T, Sennerby L, Turri A, to the implant collar in tissue level implants. Although Wennerberg A. 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