Implantology

Abdulhadi Warreth Shane Boggs, Najia Ibieyou, Ruaa El-Helali and Soohyun Hwang Peri-Implant Diseases: An Overview

Abstract: The use of dental implants in replacing missing teeth is proven to be a valid treatment with a high success rate. To achieve the best treatment outcome in all implant systems, the implant has to be able to integrate with the surrounding tissue. However, dental implants are affected by peri-implant diseases and may fail as a result. As the number of implants placed continues to increase, the prevalence of peri-implant disease will also increase. This requires preventive measures to inhibit the development of the disease and stop its progression. Clinical Relevance: Understanding how to maintain healthy peri-implant tissue as well as diagnosis and treatment of disease are vital for every and dental student. Dent Update 2015; 42: 166–184

Dental implants provide an alternative up protocol and supportive therapy to is located close to implant surface is not and a predictable treatment option for maintain peri-implant tissue health is of attached to it. Horizontal fibres, originating replacement of missing teeth with a high paramount importance. This article provides from the periosteum and the alveolar crest success rate.1,2 However, dental treatment an overview of peri-implant diseases, their to the oral epithelium, were also found. using oral implants may fail as a result diagnosis and treatments which are vital for The and connective of biological complications such as peri- every dental care professional. tissue are collectively known as the biologic implant mucositis and peri-implantitis.1-5 width. This biologic width is comparable When such complications occur and are to those found around teeth. The apical not treated properly, this may lead to the extension of the peri-implant epithelium loss of the affected implant. Thus, following Implant-soft tissue interface may be varied according to the implant implant placement, an effective check- Several studies have reported placement technique; submerged and that the soft tissue that surrounds an non-submerged. A study in beagle dogs4 implant has similar features to the soft reported that the apical extension of the tissue that surrounds teeth (Figure 1 and peri-implant junctional epithelium was Table 1).2-5 Therefore, the peri-implant soft significantly smaller and the attachment Abdulhadi Warreth, BDentSc, MDentSc, tissue consists of a junctional epithelium level significantly higher around non- PhD, MFDS, Division of Restorative which is attached to the implant and/ submerged, one-stage implants than and , Dublin or abutment surface through a hemi- submerged implants with second-stage Dental University Hospital, Trinity desmosomal attachment and a basal trans-mucosal abutments.4 College, Dublin, Shane Boggs, Fourth lamina. However, the basal lamina is less Materials from which the Year Dental Science Student, Dublin evident around an implant than teeth. abutment was made affect the location Dental University Hospital, Trinity Apical to the junctional epithelium and and the quality of the attachment that College, Dublin, Najia Ibieyou, BDentSc, coronal to the crest of alveolar , occurs between the peri-implant mucosa MDentSc, PhD, Postgraduate Student, there is an area of connective tissue which and the abutment.6 For instance, when Institute of Molecular Medicine, Trinity includes a dense circular avascular zone abutments are made of gold or porcelain, College, Dublin, Ruaa El-Helali, Fifth Year of fibres that are surrounded by a loose no proper attachment is formed at the Dental Science Student, Dublin Dental vascular connective tissue.5 Collagen fibres abutment level, but soft tissue recession University Hospital, Trinity College, arising from the crest of alveolar bone are and bone resorption occurs, consequently Dublin, Soohyun Hwang, Fourth Year oriented parallel to the implant surface/ the abutment-implant junction is exposed Dental Science Student, Dublin Dental abutment towards the oral epithelium. and the mucosal barrier is located on the University Hospital, Trinity College, Unlike connective tissue that is attached implant body. On the other hand, when Dublin, Ireland. to the root surface, connective tissue that the abutments were made of commercial

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Parameters Teeth Implants

Gingival/mucosal sulcus depth Shallow (on average 0.69 mm). Dependent on implant type and prosthetic component length. In general, it is deeper than around the teeth.

Relationship of oral epithelium with the A well-keratinized oral epithelium joins the A well-keratinized oral epithelium joins the junctional epithelium . sulcular epithelium.

Location of crestal bone 1−2 mm apical to cemento-enamel junction. Dependent on implant design; ranges from 0.5−2.5 mm from implant shoulder or the first thread.

Biologic width Junctional epithelium approx. 0.97 mm long Junctional epithelium about 2 mm long Figure 5. with extensive loss and a connective tissue attachment of and connective tissue about l−1.5 mm. of interproximal tissue. 1.07 mm in crono-apical direction.

Connective tissue attachment Collagen fibres inserted into alveolar bone Collagen fibres arise from the crestal bone and . and run parallel to the implant surface.

Collagen content and fibroblast density The gingiva contains less collagen content The peri-implant mucosa contains more and more fibroblast density than the collagen and less fibroblast density than peri-implant mucosa. the gingiva.

The occlusal thickness perception Teeth-to-teeth contact is about 20 µm. Implants with opposing teeth is about 48 µm.

Supporting mechanisms As a result of the presence of periodontal No periodontal ligament but an intimate ligament and its viscoelastic properties, implant–alveolar bone contact present: when teeth are loaded, they move within when implants are loaded, they move the socket with lateral movements that laterally approximately 10−50 μm and 3−5 range from 56−108 μm and apical μm apically due to bone deformation. movements which range from 25 to 100 μm.

Table 1. Summary of the differences and similarities between natural teeth and dental implants.

pure titanium or highly sintered aluminum tissue may be caused by the inflammatory associated with bone resorption.9 On the based ceramic (Al2O3), proper mucosal response of this tissue to that other hand, peri-implantitis is considered attachment was found on the abutment colonize the implant surface and form when peri-implant soft tissue surface.6 These findings may be due to a biofilm.7,8 It occurs when the balance is associated with bone resorption.10-12 differences in adhesive properties or to the between the bacterial load and host The Seventh European Workshop on corrosion resistance of the materials. defence is shifted in favour of the bacteria. Periodontology (2011)13 specified an It seems that the implant-soft The response of the peri-implant tissue objective diagnostic criterion for peri- tissue interface makes a protective seal to such bacterial insult may be limited implant diseases as follows: between the oral environment and the to the soft tissues, or it may also extend Mucositis, when there is bone, which plays a vital role in the success to affect peri-implant crestal bone and on gentle probing and peri-implantitis, when of the implants. It is important to mention lead subsequently to its resorption. This the bleeding is associated with crestal bone that the peri-implant tissue is more likely to inflammatory response occurs in a similar resorption with or without an increase in PPD resemble a scar tissue with less vascularity manner to that which is seen in periodontal and suppuration (Figure 2). and more collagen fibres in comparison tissue and periodontal disease. In peri-implant mucositis, with the soft tissue around teeth.5 The diseases that affect the peri- the inflammatory response resembles implant tissue are collectively known as the response in gingivae when exposed peri-implant diseases. They are classified as to pathogenic bacteria which leads to Peri-implant diseases peri-implant mucositis or peri-implantitis. . Thus, peri-implant mucositis is Biological complications that Mucositis represents an inflammation not essentially different from gingivitis. are reported to affect the peri-implant of the peri-implant mucosa, but is not For instance, after three months of

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plaque accumulation in beagle dogs, the Several risk indicators are which shows that bacteria are the histological examination of the gingiva identified to be associated with the main cause of the peri-implant disease and the peri-implant mucosa revealed that presence of peri-implant diseases. These but its severity is influenced by other both tissues, which were obtained from factors include poor , history environmental factors as well as the gingivitis and mucositis sites, contained of periodontitis, smoking, type 1 diabetes, individual’s genetic make-up.24 A study inflammatory cell infiltrates (ICIs), but genetic traits and excessive alcohol carried out on adult monkeys by Eke et al26 the peri-implant mucositis had more ICIs consumption18-22 (Table 2). indicated that the microbiota associated than that found in gingivitis.14 In peri- with progression of experimentally induced implantitis, the response to bacterial peri-implantitis and periodontitis, which insult may differ from periodontitis, both Microbiota associated with occurred simultaneously in partially in the extent and the composition of peri-implant diseases edentulous mouths, are similar. However, cells in addition to the progression rate.14 The sub-mucosal part of the while peri-implantitis sites contain a greater Furthermore, histopathological features abutment is colonized by the microbiota number of Spirochetes, the periodontitis of peri-implantitis and periodontitis in which closely resemble those found on the sites harbour more Actinomyces.26 humans are not closely identical and some neighbouring teeth in partially edentulous variations may be present.15 A review of patients. It was proposed that teeth are the several studies,16 which were carried out on source of the bacterial biofilm on implant Prevalence of peri-implant human biopsy material, indicated that the surfaces in the same individual.16,23,24 The diseases ICIs were found to be more pronounced literature indicates that the microbiota The precise prevalence rate and located more apically in peri-implantitis associated with are of peri-implant diseases is difficult to than in periodontitis. Neutrophils and also found on surfaces of implants that have estimate due to many factors, such as a macrophages were present in more failed due to peri-implantitis.24,25 lack of a standardized definition of each numbers in peri-implantitis lesions than in The microbiota that are most disease entity, different limits for bone periodontitis.15 In animal studies, plaque commonly found to colonize the surfaces loss, which indicate the presence of the formation is observed following ligature of failed implants include: Gram-negative disease, and the variability in the other placement, which results in the loss of anaerobic bacteria, such as Fusobacteria, clinical parameters used in diagnosis of supporting tissues and large ICIs around Spirochetes, Bacteroides forsythus and the disease.27,28 However, peri-implant both implants and teeth.17 However, after Aggregatibacter actinomycetemcomitans mucositis was reported to occur in about ligature removal, the ICTs extended to the and ‘black-pigmented bacteria’ like 80% of subjects and in 50% of implant sites, bone crest in peri-implant tissues, whereas a , Prevotella nigrescens whereas peri-implantitis occurs in about band of connective tissue capsule separated and .24,25 28% to 56% of patients and in 12% to 43% the ICIs from bone in the periodontia.15 There is increasing evidence of implant sites.29 In a recently published systematic review and meta-analysis study, Atieh et al30 reported that the frequency of peri-implant mucositis in the patients and on the implants was at 63.4% and 30.7%, a b respectively. The figures for peri-implantitis were about 19% for the patients and 9.6% for the implant sites. These figures indicate that mucositis is more common than peri-implantitis when patients or implant sites were considered. There is a general

Figure 1. A schematic representation of a comparison between: (a) periodontal and (b) peri-implant Figure 2. Probing using a plastic probe to avoid tissues. damaging the implant surface.

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of minor marginal inflammation, the Local Factors General Factors probe penetrates deeper around implants 39 Oral hygiene History of periodontitis than around teeth. It was also reported that the PPD was consistently greater Foreign body Genetics at implants with peri-implantitis than at implants with mild mucositis or healthy Periodontal health Acquired factors, ie diabetes mucosa.38 However, in an animal study, 40 Soft tissue conditions Environmental factors such as smoking, Etter et al reported that probing of the healthy peri-implant mucosal tissues alcohol consumption and stress caused a separation of the junctional Peri-implant pocket depth epithelium from the implant surface but not the connective tissue. The probe tip Roughness of transmucosal parts was located at the most coronal level of the supra-crestal connective tissue as FigureImplant 5. prosthesisPeriodontal connectiondisease with extensive loss of interproximal tissue. determined histologically. The epithelial adaptation was found to return to its Table 2. Local and general factors associated with the development of peri-implantitis.2 original position within five days after the peri-implant soft tissue probing.40 This may indicate the delicate nature and fragility of the peri-implant tissue compared with the consensus that during 5−10 years after should be considered when clinical and periodontal tissue. implant placement, about 20% of patients radiographic examinations are made. It is important to emphasize and 10% of implants were estimated that other factors, such as diameter of the 27,28 to be affected by peri-implantitis. It probe tip and angulation of the probe, as has been assumed that 9−14 years after Peri-implant probing well as presence of restoration, could affect implant placement peri-implantitis is a The is used in the measurement accuracy of the PPD and common clinical finding and smoking and examination of the pre-implant tissue in a CAL. The accuracy could also be affected by periodontal disease are risk factors in the similar manner to that used for periodontal the angulation and position of the implant. 31 development of the disease. examination (Figure 2). It is commonly used The PPD may also vary according to the for evaluating the gingival health status technique by which the implant is placed, and the connective tissue attachment level Diagnosis of peri-implant to implant systems and position of implant around teeth as well as around implants. shoulder in relation to crestal bone level. diseases: mucositis and peri- Thus, in order to avoid tissue trauma, the implantitis Several clinical studies reported use of a gentle probing force of 0.2 to 0.25N a deeper PPD in implants with radiographic Clinical parameters that are used is considered suitable for determination peri-implant bone loss when compared to 32,33 in the diagnosis of periodontal diseases are of PPD and CAL. However, according implants without such bone loss.33,37 It is 34 also used for diagnosis of the peri-implant to Gerber et al a force of 0.15 N might important to indicate here that the clinical diseases. These parameters are: represent the threshold that is to be used measurement in these studies was carried  The quality of peri-implant mucosa; during implant probing to avoid a false out without the removal of the prosthesis,  Plaque accumulation; positive BoP. It appears that probing around which may affect the measurements. A  (BoP); implants has a higher sensitivity compared weak correlation between PPD before the  Probing pocket depth (PPD); with probing around teeth. removal of implant-retained prosthesis  Clinical attachment level (CAL); and There is strong evidence which and the amount of bone loss evaluated  Width of peri-implant keratinized mucosa. indicates that the probe tip position during was reported.41 On the Peri-implant mucosa should be within the is affected by other hand, a high correlation was reported carefully examined for detection of redness, periodontal and peri-implant tissue health when the prosthesis was removed, as 2 hyperplasia or recession. Monitoring for conditions. For instance, in inflamed better access to probing was achieved.41 presence or absence of suppuration, which conditions the probe tip was found to Furthermore, removal of the restoration indicates the association of peri-implant penetrate the junctional epithelium may also be required for and disease with deep lesion and progressive and reach the connective tissue (closer decontamination, when sub-mucosal access bone loss, should also be considered. to bone), whereas in healthy tissue the is inadequate as a result of the presence of Implant mobility, which may indicate a probe will stop short of the base of the the restoration or due to design or position 35-39 complete implant failure or fracture, should junctional epithelium. In healthy sites of the implant.24 Thus, to obtain consistent also be included in the clinical examination. around implants and teeth, the distance PPD and CAL measurements and to achieve Radiograph evaluation is also important in between the probe tip and the alveolar a proper treatment outcome, removal of the the diagnoses. However, these evaluating bone was found to range from 0.5 to restoration is of vital importance in certain measures are not without drawbacks that 1.5mm. Furthermore, even in the presence clinical situations. March 2015 DentalUpdate 171 Implantology

It may be concluded that results reported by Bouri and co-workers,47 An intra-oral radiograph may PPD is an important indicator of bone who found a higher mean of gingival and underestimate the bone level and defect loss at implant sites if proper access is plaque scores, as well as radiographic bone depth around implants when compared to provided41 and an increasing PPD with loss around implants with a decreased direct bone measurements during surgical time is usually an indicator of crestal bone keratinized mucosa (<2 mm), than implants exposures. It has also been estimated loss. Monitoring PPD is important and its with more keratinized mucosa. Inversely, that about 30% reduction in calcified increase when associated with BoP is an according to Chung and co-workers,48 the structures is essential before it can be seen indication of a risk for peri-implant disease absence of adequate keratinized mucosa radiographically.50 progression. Thus, probing should be was not found to be associated with higher The evaluation of the peri- carried out after attachment of restorative plaque accumulation and mucositis.48 It implant bone level around an implant is component to the implant body and has also been reported that inadequate also influenced by the angulation of the this probing measurement is taken as a peri-implant keratinized mucosa was not central X-ray beam to the long axis of the baseline record from which the peri-implant found to affect the implant hygiene or peri- implant body. Thus, a precise parallelism tissue status is monitored. It should be implant soft tissue health status adversely. between implant body axes and film plane pointed out that the literature indicates Nevertheless, the susceptibility to gingival is important to obtain valid results.51 The that the reproducibility and sensitivity of recession and the peri-implant crestal central beam is then directed at a right PPD measurements, in general, is low.42 bone loss may increase.49 Even though angle to the film. In this case, implant Therefore, all of these deficiencies in no conclusive recommendation can be threads can clearly be seen with no probing should be considered when peri- made, healthy peri-implant mucosa can overlapping. Figure 4 shows a radiograph of implant tissue probing is carried out and still be seen in the presence and absence an affected implant. interpreted. of keratinized peri-implant mucosa. There During the probing procedure, is, however, a general consensus that the bleeding areas are also observed and presence and preservation of peri-implant recorded (Figure 3). It indicates mucosal keratinized mucosa is important for the inflammation.12,43 However, in the evaluation health of the mucosa32 and for long-lasting of periodontal disease, BoP does not have maintenance and management of tissue.32,49 a good predictable value. Nevertheless, the absence of BoP is considered a reliable indicator of stable and healthy periodontal Radiographic evaluation tissue.44,45 When BoP is considered around After implant placement a the implants, it seems to have a better radiograph is needed. This radiograph is diagnostic accuracy than around the teeth.12 usually used to confirm the position of the It has been reported that BoP occurred in implant and may also be used in comparing Figure 3. Bleeding on probing with suppuration. about 91% of peri-implantitis sites.38 Thus, it the peri-implant bone level with this bone is a valuable diagnostic parameter. However, level in the future. However, after placement smoking may affect peri-implant mucosa as of the implant, a 3-month healing period it has a suppressive effect on its BoP, which should be given and peri-implant bone may lead to an improper diagnosis. level recorded radiographically, as the osseointegration of peri-implant bone is probably now achieved. This radiograph Keratinized mucosa is used as a baseline to monitor the It has been suggested that the bone level.24 The radiograph should also presence of keratinized mucosa around be standardized in order to minimize implants may be beneficial in maintaining distortion and to obtain a comparable view the mucosal health as it facilitates plaque which is important to reach an accurate control and enhances its removal. The interpretation. importance of keratinized mucosa around Patient clinical assessment is dental implants was evaluated by Boynueğri required first and a radiograph is carried 46 and co-workers in 15 edentulous out only if it is a necessity and is used to patients with implant-retained complete confirm the clinical finding and for an overdentures. The results of this study estimation of the peri-implant bone level indicated that less plaque accumulation and to detect any existing pathology. and less mucosal inflammation were Nevertheless, a repeat exposure of the associated with the presence of a minimum patient to unnecessary radiation is not of 2 mm band of keratinized mucosa when ethically sound and adherence to what is Figure 4. Radiographic representation of compared with implants with no keratinized known as the ALARA (As Low As Reasonably peri-implantitis lesion for the same patient as in mucosa. This is in agreement with the Achievable) principal is essential. Figures 2 and 3. 172 DentalUpdate March 2015 Implantology

Radiographically, the health status of the treated sites requires treatment of peri-implant mucositis distortion of buccal and lingual bone regular check-ups, and enhancement of consists of mechanical debridement, oral margins may lead to an overestimation of the patient’s oral hygiene, to keep plaque hygiene education and regular check-ups. peri-implant bone heights.51 The degree accumulation on the implant body and/or The outcome of such treatment could of overestimation is also affected by the abutment surface as low as it is achievable. be enhanced when an antimicrobial bucco-lingual position of the implant Furthermore, clinical examination and peri- mouthrinse is used as an adjunctive.10 body, as well as the width of the alveolar implant disease therapy require instruments Mechanical debridement, bone ridge.51 Thus, the wider the ridge, that are designed and made from materials as well as mechanical debridement the less accurate bone level readings will which are unlikely to damage the implant supplemented with , be. It has been concluded that the width surface during the examination and resulted in a reduction of plaque, of the alveolar ridge and the amount treatment. The instruments used for inflammation and PPD, as well as a gain of bone loss may negatively affect the clinical examination and implant surface in CAL, and were effective in suppressing accuracy and precision of the intra-oral debridement are displayed in Figure 6. or eradicating the pathogenic bacteria radiograph evaluation.52 A number of methods which is often associated with peri- We should bear in mind that have been suggested for cleaning and implant inflammation.61 It appears that radiography is 2-dimensional imaging decontamination of implant surfaces.54-59 such a treatment option is effective and of a 3-dimensional object. Furthermore, These methods may be categorized into could lead to the reduction in peri-implant radiographic assessments of marginal three classes as follows: mucosal inflammation. Furthermore, bone loss are highly specific and are 1. Mechanical techniques such as the use a positive effect was reported when limited to the mesial and distal aspects of titanium-coated Gracey curettes, carbon antimicrobial mouthrinses were used of the implants.37 Therefore, changes fibre curettes, plastic-coated ultrasonic as an adjunctive to the mechanical in bone level on the labial and lingual scalers, or air-powder abrasives; intervention.18,57,62 Thus, it is correct to say aspect cannot be radiographically 2. Use of chemicals such as chlorhexidine, that treatment of mucositis is identical to detected as the implant material will citric acid, , , that used in treatment of gingivitis. absorb the radiation and, consequently, or stannous fluoride; and the bone level will not be seen. In a 3. -based treatments. Treatment of peri-implantitis clinical study carried out by Serino et However, no single surface Similar to the objectives of 37 60 al, only 66% of the implants presented cleaning technique seems to be superior. the mucositis treatment, the goal of peri- with circumferential bone loss (Figure implantitis treatment is to stop further 5). While 34% had a tendency to have peri-implant tissue destruction and to more bone loss buccally, radiographs Treatment of peri-implant were poor in detecting such loss. In diseases another study examining 40 implants The principal step in any undergoing surgical treatment for peri- treatment option for peri-implant diseases implantitis, only 55% of the implants had consists of debridement of the tissue circumferential bone loss.53 defect and decontamination of the affected It is worth mentioning that a implant surface. Largely, the treatment may 3-dimensional image may be obtained be divided into two categories: by use of conventional or cone-beam 1. Those targeting peri-implant mucositis; and computed tomography, which provide 2. Those used in treatment of peri- a more accurate representation, but its implantitis (Table 3). availability and expense may preclude its While the treatment of use in diagnosis of peri-implant disease. mucositis is non-surgical, the treatment Figure 5. Circumferential bone defect around It may be concluded that of peri-implantitis may be surgical or non- implant. diagnosis of peri-implant diseases surgical, depending on several factors such requires the use of probing techniques as the severity of the disease, aesthetic c to identify the presence or absence of requirement and the presence/absence of pocketing, bleeding, as well as CAL, all neighbouring teeth. b of which may indicate the presence of peri-implant disease. Radiographs are a also required to detect and estimate Treatment of peri-implant mucositis peri-implant bone level. Diagnostic The aim of the treatment is information should be obtained for all to decrease and disturb the peri-implant Figure 6. The instruments used for clinical implant patients once placement and microbial community in order to stop examination and treatment: a plastic probe used healing of the implant is complete, to further tissue destruction and to change to avoid scratching and damaging the implant surface (a); titanium implant curettes (Titan®) allow for longitudinal monitoring of the microbial composition to those used for implant surface debridement (b and c). peri-implant conditions. Monitoring the associated with healthy tissue. In general, March 2015 DentalUpdate 173 Implantology

Clinical Parameters Clinical Diagnosis Treatment Protocols

PPD (Shallow) Healthy peri-implant tissue No treatment is needed, just regular check- No plaque ups and enhancement of oral hygiene No BoP

PPD (Shallow) Mucositis A. Mechanical debridement and polishing Plaque is present using a rubber cup and non–abrasive paste BoP is present and regular check-ups and enhancement of oral hygiene

PPD ≤5 mm Mucositis B. Treatment includes treatment A with antiseptic cleaning Figure 5. Periodontal disease with extensive loss PPD >5 mm associated with Peri-implantitis C. Same as treatment B in addition to the of interproximal tissue. bone loss of up to 2 mm use of local or systemic antibiotic

PPD >5 mm associated with bone Severe peri-implantitis D. Same as treatment C combined with loss >2 mm surgery (access flap, resective method or regenerative technique)

Table 3. Different treatment options proposed for treatment of peri-implant diseases.32

establish healthy peri-implant soft and is shallow,32 but not enough when the as an adjuvant to mechanical debridement hard tissues. Secondary goals, in certain PPDs are deep and with exposed implant is needed in deep PPD. However, surgical situations, are to obtain bone fill of the threads.63 However, the use of mechanical intervention may also be required. defective bone and re-osseointegration of debridement alone was not found to It was demonstrated2,65 that exposed implant surfaces. Several treatment achieve considerable re-osseointegration,57 the adjunctive use of a topical antibiotic, options have been suggested for treatment which is an important treatment outcome. minocycline microspheres, to mechanical of peri-implantitis.52-58,62-70 These options are It would seem rational to debridement tends to have greater based on several factors, such as degree combine the mechanical debridement with benefits than those achieved through and extent of the disease and morphology chemical antiseptic agents.64-66 In a human the use of an antiseptic, ie chlorhexidine of bone defect. They can be divided into study66 of oral implants with an initial to and mechanical debridement together. two main categories as follows: moderate peri-implantitis, the use of carbon In the study conducted by Renvert and 1. The non-surgical approach: mechanical curettes combined with chlorhexidine co-workers,65 where 32 subjects had debridement or laser applications, either antiseptic was compared with the use of peri-implant lesions with a PPD ≥4 mm alone or combined with antiseptic or air-abrasive devices alone. Both treatment with BoP and/or exudate, the adjunctive antibiotic agents; measures led to comparable but limited use of chlorhexidine resulted in limited 2. The surgical approach: open flap access reductions in PPD and in CAL gains at 6 reduction of BoP, but the adjunctive use of with or without resective or regenerative months.66 However, the result of the study minocycline led to improvements in both techniques. indicated that the first treatment regimen BoP and PPDs. The observed improvements was less effective in decreasing BoP than in bleeding scores and PPDs obtained by the second one. It was found that, in peri- the adjunctive use of minocycline were Non-surgical approach implant lesions with a PPD ≥ 5 mm, the maintained during a period of 12 months. This approach involves combination of mechanical debridement In another study conducted by Renvert et mechanical debridement of the peri- and antiseptic therapy may provide an al,67 using the same treatment protocols as implant tissues and the affected implant improvement in clinical parameters. used in the previous study, the treatment surface without raising a flap. In general, However, residual defects remain after was repeated three times: baseline, one this method is not always effective, the therapy, which may require additional and three months. Follow-up examinations particularly when the peri-implantitis treatment. According to Renvert et al65 the were carried out at 10 days and at 1, 3, 6, is associated with a deep PPD.10,24 addition of antiseptic therapy to mechanical 9 and 12 months. The results of this study Furthermore, the outcome of non-surgical debridement does not provide adjunctive indicated that the use of minocycline treatment of peri-implantitis was not benefits in shallow peri-implant lesions microspheres as an adjunctive is beneficial predictable and mechanical debridement (mean PPD <4 mm). Therefore, it may be in the treatment, but the treatment alone may be efficient when the PPD concluded that the use of antiseptic agents may have to be repeated. This raises the 174 DentalUpdate March 2015 Implantology

question as to whether peri-implantitis with Surgical approach soaked in sterile saline. Adjunctive systemic deep PPD can be adequately treated non- Surgical treatment of peri- antibiotics (amoxicillin and metronidazole) surgically by a combination of mechanical implantitis lesions can be performed after were also prescribed. Clinical parameters debridement and a local antibiotic, and the acute has resolved and proper such as BoP, PPD and suppuration were 2,32,70 whether the positive effect of this treatment oral hygiene has been established. The evaluated at 3, 6 and 12 months and the can be maintained for a longer period of primary objective of surgical treatment in treatment outcomes were analysed during time. Hence, well-controlled randomized peri-implantitis is to get direct access to these intervals. Forty seven percent of the clinical studies are required. the affected site and the implant surface, affected implants had complete resolution are used currently in which facilitates decontamination of the of inflammation (BoP negative) and stable dentistry and their use has extended to implant surface and eliminates granulation crestal bone levels or bone gain, which was the treatment of peri-implant diseases. tissue. The selected surgical protocol is also seen in 92% of implants. It was concluded For instance, Thierbach and Eger69 divided dictated by the degree and morphology of that the conducted treatment protocol was 28 patients with peri-implantitis into two the peri-implant bony defect. The amount effective and it was possible to maintain the categories: those with peri-implantitis and quality of the remaining peri-implant three month positive treatment outcomes with pus formation (Figure 3) and those soft tissue may play a role in surgical for at least one year post-operatively if a 2 without. Both groups were treated using the protocol selection. The surgical approach strict oral hygiene protocol was followed. same protocol initially after microbiologic can be categorized as follows: The use of an access flap diagnosis. All patients were treated at  Access surgery (an open flap technique); for debridement of the implant surface baseline with full-mouth scaling and root  Resective surgery with or without implant combined with chlorhexidine irrigation was planing. Two months later, full-mouth scaling surface modification (implanto-plasty); compared with non-surgical scaling before and root debridement and antimicrobial  Regenerative approach (use of grafting photodynamic therapy was implemented photodynamic therapy were applied. The materials with or without membrane). for microbial reduction in ligature-induced study indicated that the presence of pus peri-implantitis in dogs.71 This investigation influences the clinical outcome of the reported that several bacterial species, that Access surgery (an open flap technique): This treatment of peri-implantitis. According to are believed to be associated with peri- approach consists of raising a flap, removal this investigation, non-surgical treatment of implantitis, were significantly reduced by of granulation tissue and debridement/ peri-implantitis may be effective when the both treatments. However, photodynamic decontamination of implant surfaces.55,56,59 peri-implantitis lesion has no pus formation therapy is a non-invasive approach which This method provides a direct vision but not when pus is present. Nevertheless, may be an advantage over surgical access.71 and access to the affected peri-implant when the lesion is associated with pus It may be concluded that the tissue and to the unexposed implant formation, it can be successfully treated open flap technique permits direct access surface. The effect of this treatment was with a supplementary access flap surgery into the affected site, which may enable evaluated clinically, microbiologically and following an additional observation time of the clinician to evaluate the bony defect radiographically at 6 months, 1 year and 5 3 months. and to debride the implant surface and years after surgical exposure and implant It should be emphasized here also eliminate the granulation tissues surface decontamination using curettes that, although the use of lasers for implant effectively. In addition, this approach may and sterile saline.55 Systemic antibiotics surface de-contamination is a promising be necessary when the PPD is deep or when were also given according to a susceptibility treatment method, their use may be the angulation of the implant body is in an test of target bacteria. Six implants of the associated with implant surface changes inconvenient position that may preclude 26 studied demonstrated bone gain while that may negatively affect the treatment effective treatment. seven implants were lost and four continued result. Furthermore, laser irradiation to lose more bone. Nine implants revealed may raise the temperature beyond the unchanged peri-implant bone levels. This Resective surgery (with or without implant degree which the peri-implant tissue study indicated that the treatment protocol surface modification): Resective surgery can tolerate and leads to its damage.58,66 used may be useful in controlling peri- is used in treatment of periodontal Likewise, not all laser types are suitable implantitis lesions but with a low predictable diseases to correct soft and hard tissue as implant surface decontaminators. For value. However, the number of implants used defects around natural teeth. It is based instance, YAG and Ho:YAG were not found in the study may preclude from drawing a on periodontal pocket elimination, to be appropriate as implant surface valid conclusion and further well-controlled such as apical repositioning flap and decontaminators, irrespective of the power studies are important. Heitz-Mayfield et gingivectomy or pocket reduction to make output.58,66 Additionally, the application of al59 studied moderate to advanced peri- the periodontal tissue more accessible laser results in an increase in implant surface implantitis lesions in 36 implants in 24 for cleaning, thus facilitating the patient’s roughness that may encourage more plaque partially dentate patients. They were treated oral hygiene. Resective surgery may also accumulation and complicates its removal.68 with open flap surgery and implant surface involve an osseous resection/re-contouring Thus, the proper laser type, irradiation angle decontamination using titanium-coated which means the removal of defective/ and energy intensity and application time Gracey curettes or carbon fibre curettes and correction of supporting bone. This that is suitable for each implant surface rubbing of the implant surface with gauze resective treatment option is extended for should be recognized and used.58 March 2015 DentalUpdate 177 Implantology

use in treatment of peri-implantitis lesions. was found to be more effective than the formation on exposed surfaces of titanium In the oral implant, it is carried out in the resective method alone. Consequently, it is implants in animal79 and human studies.80 treatment of peri-implant disease in order not unreasonable to conclude that resective The membrane used can to reduce PPD. It may involve correction surgery coupled with implanto-plasty could be made of resorbable material, such of the peri-implant soft tissue when the have a positive influence on the survival as collagen membrane, for example bone loss is mainly of the horizontal type. rates of rough-surface implants affected by (Bio-Gide®), or non- resorbable, such as Resective surgery combined with apical peri-implantitis, as well as on clinical peri- expanded polytetrafluoroethylene (ePTFE). repositioning flap may be performed implant parameters such as BoP, PPD and By the use of resorbable membrane the in the treatment of peri-implantitis that suppuration.73 second surgical intervention needed results in a two- or one-walled bony defect It is important to remember to remove the membrane is avoided. or horizontal bone resorption. However, that the resective approach is indicated However, resorbable membranes may be the resective approach should be carried when the regenerative treatment is not associated with more signs of post-surgical out cautiously as the amount of removed the treatment of choice.32 For instance, in inflammation than non-resorbable ones.81 peri-implant tissues may compromise the horizontal bone loss where the regenerative Studies comparing the use of resorbable aesthetic and/or mechanical results of the approach may not be a rational option. and non-resorbable membranes indicated implant and the neighbouring teeth. However, this surgical approach may be that both types had a comparable clinical In a clinical study of 31 subjects used in a non-aesthetic zone as tissue effectiveness.81,82 However, complications with clinical signs of peri-implantitis, 42% of recession is most likely to follow. such as membrane exposure is a real the implants still had the disease after two problem which can have a detrimental years of treatment with bone re-contouring impact on the treatment outcome.83,84 The and pocket elimination and plaque control Regenerative approach (use of grafting exposed membranes should be removed before and following the surgery.72 Seventy materials with or without membrane): immediately because, if it is left in situ, the four percent of the implants with an In general, the regenerative approach amount of bone gain will be negatively initial bone loss of 2–4 mm as measured consists of flap elevation, mechanical root affected. radiographically showed no sign of peri- debridement and placement of a graft In treatment of peri-implantitis, implantitis during the 2-year period in material, either alone or combined with a the use of membrane is usually combined comparison with 40% of the implants which membrane. The membrane protects the with graft materials. The objective here had a greater bone loss (≥ 5 mm). These graft material and provides a confined is to regenerate new bone, reduce PPD, findings reflected the effects of the severity space for formation of the desired tissues. gain of CAL and re-osseointegration of the of initial peri-implant bone loss on the When the membrane is used without decontaminated implant surface.85 The treatment outcome and on the stability of a graft material, the surgical method is use of grafting material with or without the achieved improvement. known as guided tissue regeneration (GTR). a membrane has been used extensively A combination of resective Guided tissue regeneration (GTR) was in the treatment of peri-implantitis, with surgery and modification of the initially used for treatment of periodontal a short-term follow-up with a promising implant surface (implanto-plasty) has disease to hinder epithelial and connective outcome. As the exposure of the membrane been proposed in treatment of peri- tissue migration into the surgical area but is a problem that adversely affects the implantitis.73,74 The implanto-plasty allowing cells from periodontal ligament treatment outcomes, the use of graft technique involves the use of rotary (PL) and bone to repopulate the root material alone appears to be an effective 75-78 instruments to smooth the exposed surface after its debridement, therefore alternative to the use of membrane and implant surfaces in order to reduce new cementum, PL and alveolar bone are the combination of graft materials and the formation of plaque on the implant surface regenerated. The GTR concept is based on membrane is not always an ideal treatment and to facilitate its removal.73 The use of the hypothesis that the cell type which option.2 Nevertheless, Hürzeler et al 86,87 proper burs with coolant is of paramount has the potential to colonize the exposed reported no significant difference in bone importance for efficient cutting to reduce root surface at the periodontal healing fill between the use of membrane alone clinical time and to avoid excess heat site will dictate the nature of the resultant and when the membrane was used with a 75 generation that can damage the peri- attachment or repair. Thus, if epithelial graft material. However, according to these implant tissue.74 Romeo and colleagues73 cells reach the surgical site and repopulate two studies, the combination of membrane studied peri-implantitis lesions in 19 the exposed root surface, a long junctional and graft materials led to a greater amount patients with 38 implants. The treatment epithelium will form. However, if the of re-osseointegration than debridement involved systemic antibiotics (Amoxicillin perivascular cells of the alveolar bone, as alone (with an air-powder abrasive), for 8 days) with full-mouth disinfection. well as cells from PL, repopulate the surgical or when debridement combined with Nine patients were treated with resective site, new bone, cementum and PL will be membrane or graft materials. It is important 76-78 surgery only and ten with resective surgery created. When the main goal of the to note that the findings of Hürzeler et and implanto-plasty. Marginal bone levels surgical process is to regenerate new bone, al86,87 were based on animal studies (seven were measured radiographically at 1, 2 the procedure is known as guided bone beagle dogs) in which the peri-implantitis and 3 years after surgery. The resective regeneration (GBR). This technique has was induced by ligature applications for 3 method combined with implanto-plasty been further applied to encourage bone months.86,87 178 DentalUpdate March 2015 Implantology

In another study in dogs,88 no scheduled. In addition, a decision on how Conclusion statistically significant differences in bone to handle the case can be made and which Management of mucositis fill in the treatment of ligature-induced treatment modality should be considered involves mechanical debridement and peri-implantitis were found when the use and carried out. Moreover, the following polishing of the restoration-abutment of membrane, bone graft, or a combination points may be suggested as a general surface in addition to oral hygiene of the two methods, were compared. The approach: education and follow-up. The effect three treatment options performed better  Peri-implantitis lesions with shallow PPDs of mechanical debridement could and gained more bone fill than debridement may be treated non-surgically with further be improved when it is combined alone. Accordingly, it was concluded that the follow-up and oral hygiene enhancement; with application of antiseptic agents. three treatment techniques can improve the  Deep PPDs may be treated surgically Management of peri-implantitis with bone fill in defects caused by experimentally with an access flap which aids further several surgical approaches have been 88 induced peri-implantitis in dogs. examination. This evaluation may dictate described. Unfortunately, there is no The clinical study by Schwartz the resective approach or regenerative general agreement on the best method of 89 et al demonstrated that treatment of method, depending on many factors, such treatment. Thus, due to lack of sufficient moderate peri-implantitis with either nano- as the severity of the disease, degree and evidence, a recommendation to implement crystalline hydroxyapatite (Ostim®) or Bio- type of bony defect, aesthetic requirements a specific protocol in the treatment Oss®, in combination with the use of collagen and neighbouring teeth. membrane, provided clinically significant Following any treatment improvements in clinical parameters, such protocol, a follow-up period is essential as PPD and CAL gains following 6 months in order to monitor oral hygiene and help of non-submerged healing. The two year stop and/or discover in time any further a results of the same clinical study90 once deterioration. more demonstrated that both treatment modalities were effective in providing clinically significant reductions of PPD and Other causes of peri-implant gains in CAL. However, the combination use crestal bone loss of Bio-Oss® and collagen membrane seemed As peri-implantitis is associated to correlate with greater improvements in with the peri-implant crestal bone loss, those clinical parameters and hence were other factors that may cause such bone associated with greater predictability and loss should be considered. Distinction enhanced healing outcome. between crestal bone loss as a result of the b It may be concluded that the peri-implantitis or that due to other causes routine use of the membrane should be is an important starting point in stopping judgementally implemented83 and the and treating such bone loss. It has been use of the membrane with graft material reported that an average of one millimetre may not always be required, as there is no of marginal bone loss is commonly seen strong evidence to support its advantage.91 after the first year of function.92,93 This may However, the use of graft material without be followed by an annual loss of less than a membrane may be considered when the 0.1 mm thereafter.94 However, the exact graft material can be retained within the cause of this bone loss is still debatable. Figure 7. Peri-implant mucosal enlargement bony defect, such as in a circumferential Currently available literature indicates associated with peri-implantitis. Before removal of bone defect, ie a 4-wall bony defect that the reformation of a ‘biologic width’ the bar (a) and after removal of the bar (b). Note (Figures 7 and 8). The use of the membrane around dental implants, presence of a deposition of on the implant surface. may be employed when the bony defect rough/smooth interface, and a micro-gap morphology does not retain the graft at implant-abutment interface and occlusal material, ie a 2-wall bony defect. However, overload are the most likely causes of early long- term, well-controlled randomized peri-implant crestal bone loss. Nevertheless, clinical studies are required.85 A summary of other contributing factors, such as surgical different treatment options for peri-implant trauma, may also have a role to play in disease, which is suggested by Lang and the process of early implant bone loss.92,93 colleagues,32 is displayed in Table 3. It is important to mention that occlusal In general, it may be proposed overload does not cause peri-implant that each peri-implantitis case should be disease, but can accelerate its effect when evaluated clinically and radiographically the disease is already present.19 The factors in a similar manner, as in the treatment of that may contribute to, or cause, peri- Figure 8. The circumferential (4-walled) defect of periodontal disease. Oral hygiene should be implant crestal bone loss are displayed in the patient in Figures 5 and 7 treated with graft material (Bio-Oss®). observed and regular check-ups should be Table 4. March 2015 DentalUpdate 179 Implantology

1993; 64: 1176−1183. 1. Bone remodelling after implant placement and an annual loss of <0.1 mm. 12. Luterbacher S, Mayfield L, Brägger U, Lang 2. Reformation of a ‘biologic width’. NP. Diagnostic characteristics of clinical 3. Presence of a rough/smooth interface. and microbiological tests for monitoring 4. Presence of a micro-gap at implant-abutment interface. periodontal and peri-implant mucosal tissue 5. Surgical trauma. conditions during supportive periodontal 6. Occlusal overload. therapy (SPT). Clin Oral Implants Res 2000; 11: 7. A ‘stress shielding’ phenomenon. 521−529. 8. Incomplete removal of luting cement. 13. Lang NP, Berglundh T. Peri-implant diseases: where are we now? Consensus of the Seventh Table 4. Other factors that may contribute to or cause crestal bone loss. European Workshop on Periodontology. J Clin Periodont 2011; 38(Suppl 11): 178−181. 14. Ericsson I, Berglundh T, Marinello C, Liljenberg B, Lindhe J. 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184 DentalUpdate March 2015