LITHUANIAN UNIVERSITY OF HEALTH SCIENCES
Aušra
Ramanauskaitė
INVESTIGATION AND IMPROVEMENT
OF PERI-IMPLANTITIS CLINICAL
CHARACTERISTICS, DIAGNOSTICS
AND TREATMENT
Doctoral Dissertation Biomedical Sciences, Odontology (07B) Kaunas, 2019Dissertation has been prepared at the Department of Dental and Oral Pa-thology of Medical Academy of Lithuanian University of Health Sciences during the period of 2014–2018.
Scientific Supervisor
Prof. Dr. Gintaras Juodžbalys (Lithuanian University of Health Sciences, Medical Academy, Biomedical Sciences, Odontology – 07B).
Consultant
Prof. Dr. Frank Schwarz (Department of Oral Surgery and Implantology, Carolinum, Johann Wolfgang Goethe-University Frankfurt, Germany, Biomedical Sciences, Odontology – 07B).
Dissertation is defended at the Odontology Research Council of the Li-thuanian University of Health Sciences:
Chairperson
Prof. Dr. Vita Mačiulskienė (Lithuanian University of Health Sciences, Medical Academy, Biomedical Sciences, Odontology – 07B).
Members:
Prof. Dr. Jurgina Sakalauskienė (Lithuanian University of Health Scienc-es, Medical Academy, Biomedical SciencScienc-es, Odontology – 07B);
Prof. Dr. Alvydas Gleiznys (Lithuanian University of Health Sciences, Medical Academy, Biomedical Sciences, Odontology – 07B);
Assoc. Prof. Dr. Saulius Diliūnas (Kaunas University of Technology, Technological Sciences, Mechanical Engineering – 09T);
Prof. Dr. Rui Amaral Mendes (Case Western Reserve University, Bio-medical Sciences, Odontology – 07B).
Dissertation will be defended at the open session of the Odontology Re-search Council on the 22nd of February, 2019 at 12 a.m in the auditorium No. 203 of the Centre for the Advanced Pharmaceutical and Health Tech-nologies of the Lithuanian University of Health Sciences.
LIETUVOS SVEIKATOS MOKSLŲ UNIVERSITETAS
Aušra Ramanauskaitė
PERIIMPLANTITO
KLINIKINIŲ
POŽYMIŲ, DIAGNOSTIKOS IR
GYDYMO
PROTOKOLŲ TYRIMAS
IR TOBULINIMAS
Daktaro disertacija Biomedicinos mokslai,
odontologija (07B)
Disertacija rengta 2014–2018 metais Lietuvos sveikatos mokslų universiteto Medicinos akademijos Dantų ir burnos ligų klinikoje.
Mokslinis vadovas
Prof. dr. Gintaras Juodžbalys (Lietuvos sveikatos mokslų universitetas, Medicinos akademija, biomedicinos mokslai, odontologija – 07B).
Konsultantas
Prof. dr. med. dent. Frank Schwarz (Johano Volfgango fon Gėtės univer-sitetas, Burnos chirurgijos ir implantologijo klinika, Frankfurtas, Vokie-tija, biomedicinos mokslai, odontologija – 07B)
Disertacija ginama Lietuvos sveikatos mokslų universiteto odontologi-jos mokslo krypties taryboje:
Pirmininkė
Prof. dr. Vita Mačiulskienė (Lietuvos sveikatos mokslų universitetas, Medicinos akademija, biomedicinos mokslai, odontologija – 07B).
Nariai:
Prof. dr. Jurgina Sakalauskienė (Lietuvos sveikatos mokslų universitetas, Medicinos akademija, biomedicinos mokslai, odontologija – 07B).
Prof. dr. Alvydas Gleiznys (Lietuvos sveikatos mokslų universitetas, Medicinos akademija, biomedicinos mokslai, odontologija – 07B).
Doc. dr. Saulius Diliūnas (Kauno technologijos universitetas, techno-logijos mokslai, mechanikos inžinerija – 09T).
Prof. dr. Rui Amaral Mendes (Keiso Vestern Rezervo universitetas, bio-medicinos mokslai, odontologija – 07B).
Disertacija ginama viešame Odontologijos mokslo krypties tarybos po-sėdyje 2019 m. vasario 22 d. 12 val. Lietuvos sveikatos mokslų universiteto Naujausių farmacijos ir sveikatos technologijų centre, 203 auditorijoje.
Disertacijos gynimo vietos adresas: Sukilėlių pr. 13, LT-50166 Kaunas, Lietuva.
CONTENT
ABBREVIATIONS ... 7
INTRODUCTION ... 8
1. AIM AND OBJECTIVE OF THE STUDY ... 10
2. NOVELTY OF THE STUDY ... 11
3. LITERATURE REVIEW ... 12
3.1.Etiology of peri-implantitis ... 12
3.1.1. Microbiological profile of peri-implantitis ... 12
3.1.2. Periodontitis as a risk factor for peri-implantitis ... 13
3.1.3. Risk factors/indicators ... 14
3.1.4. Onset and progression of peri-implantitis ... 15
3.2. Definitions, clinical characteristic and peri-implantitis diagnostic parametersl profile of peri-implanti ... 15
3.2.1. Definitions of peri-implantitis ... 15
3.2.2. Clinical characteristics of peri-implantitis ... 21
3.2.3. Suggested diagnostic parameters ... 23
3.3. Peri-implantitis treatment approaches ... 25
3.3.1. Non-surgical therapy ... 25
3.3.2. Surgical therapy ... 31
3.3.2.1. Access flap surgery ... 31
3.3.2.2. Resective therapy ... 36
3.3.2.3. Reconstructive therapy ... 43
3.4. Factors inlfluencing peri-implantitis treatment outcomes ... 64
3.5. Summary of literature review ... 65
4. MATERIALS AND METHODS... 67
4.1. Part of clinical innovations ... 67
4.1.1. Guidelines for peri-implantitis diagnosis and prognosis ... 67
4.1.2. Evaluation of the effectiveness of different peri-implantitis treatment approaches ... 67
4.2. Clinical part ... 68
4.2.1. Type of the study ... 68
4.2.2. Study participants ... 68
4.2.3. Selection criteria for study participants and case definitions ... 70
4.2.3.1. Selection criteria for the patients included into the clinical investigation of peri-implant tissue health and disease and case definitions ... 70
4.2.3.2. Selection criteria for the patients included into the clinical investigation of surgical peri-implantitis treatment outcomes and case definitions ... 70
4.2.4. Power of the study ... 72
4.2.5. Ethics of the study ... 73
4.2.6. Instrumentations and interventions of the study ... 73
4.2.6.1. Treatment procedure of peri-implantitis ... 73
4.2.6.2. Assessment of clinical parameters ... 74
4.2.6.2.1. Investigation of peri-implant tissue health and disease ... 74
4.2.6.2.2. Investigation of the effectiveness of peri-implantitis
surgical therapy outcomes ... 74
4.2.7. Outcome measures ... 75
4.2.7.1. Investigation of peri-implant tissue health and disease ... 75
4.2.7.2. Investigation of the effectiveness of peri-implantitis surgical therapy outcomes ... 75
4.2.8. Statistical analysis ... 75
4.2.8.1. Evaluation of clinical parameters around healthy and diseased implants ... 75
4.2.8.2. Evaluation of treatment outcomes at non-grafted and grafted implant sites ... 76
5. RESULTS ... 77
5.1. Part of clinical inovations 5.1.1. Guidelines for peri-implantitis diagnosis and prognosis ... 77
5.1.2. Evaluation of the effectiveness of different peri-implantitis treatment approaches ... 78
5.2. Clincal part ... 94
5.2.1. Clinical parameters associated with peri-implant tissue health and disease ... 94
5.2.2. Clinical outcomes following surgical treatment of peri-implantitis non-grafted and grafted implant sites ... 99
6. DISCUSSION OF THE RESULTS ... 107
6.1. Part of clinical innovations ... 107
6.1.1. Guidelines for peri-implantitis diagnosis and prognosis ... 107
6.1.2. Evaluation of the effectiveness of different peri-implantitis treatment approaches ... 109
6.2. Clinical part ... 112
6.2.1. Clinical parameters associated with peri-implant tissue health and disease ... 112
6.2.2. Clinical outcomes following surgical treatment of peri-implantitis at non-grafted and grafted implant sites ... 114
7. CONCLUSIONS ... 117
8. CLINICAL AND SCIENTIFIC RECOMMENDATIONS ... 118
8.1. Guidelines for peri-implantitis diagnosis and prognosis ... 118
8.2. Evaluation of effectiveness of different peri-implantitis treatment approaches ... 118
8.3. Clinical parameters of peri-implant tissue health and disease ... 119
8.4. Impact of bone grafting procedures on peri-implantitis treatment outcomes ... 119
9. REFERENCES ... 121
10. PUBLICATIONS AND SCIENTIFIC CONFERENCES, WHERE THE RESULTS OF THE DISERTATION WERE PRESENTED ... 132
11. SUMMARY ... 180
12. CURRICULUM VITAE ... 218
13. ACKNOWLEDGMENTS ... 220
ABBREVIATIONS
AAP – American Academy of Periodontology a/b – systemic antibioticsABL – amount of bone loss BL implant – bone level implant BOP – bleeding on probing CI – confidence interval
CMM – complex management and maintenance protocol DF – degree of freedom
DFDBA – demineralized freeze-dried bone allograft EWP – European Workshop on Periodontology NR – not reported
p – significance level PD – probing pocket depth PBL – pathological bone loss RBL – rate of bone loss
RCT – randomized clinical trial
Q – heterogeneneity test (Cochran’s Q) SD – standard deviation
SMD – standardized mean difference
SLA – sand blasted and acid etched implants Supp – suppuration
STL implant – soft tissue level implant
TPS – titanium plasma sprayed implants OR – odds ratio
INTRODUCTION
Peri-implant diseases are initiated by the host response to a bacterial challenge and comprise of two clinical phenotypes, peri-implant mucositis and peri-implantitis [1, 2]. While the former is restricted to the peri-implant soft tissues, peri-implantitis is mainly characterized by the progressive loss of supportive bone [3, 4]. Consequently, it is thought that peri-implantitis follows peri-implant mucositis [5].
Recent data suggests that the onset of peri-implantitis occurs within the first few years of implant functioning [6] and in the absence of treatment, the disease progresses in a non-linear and accelerating pattern [6, 7].
The prevalence of biological complications, was reported to be high, ranging from 19 to 65% for peri-implant mucositis and from 1 to 47% for peri-implantitis [8]. The recent meta-analysis based on 29 investigations estimated the overall prevalence of peri-implantitis, that amounted to 18.5% at the patient level and 12.8% at the implant level [9].
Currently while there seems to be a common sense on the definition of per-implantitis [8], the respective case definitions vary considerably in the literature [8]. These are commonly based on clinical parameters to determi-ne peri-implant mucosal inflammation (e.g., reddetermi-ness, bleeding on probing – BOP, suppuration – Supp) along with a loss of the supporting tissues (e.g. increases in probing depths – PD, progressive radiographic bone loss) [10]. However, threshold levels for PD scores and radiographic bone levels may be misleading and not allow for a proper differentiation between peri-implant mucositis and peri-peri-implantitis [10]. Moreover, the definition of a physiological PD at implant sites is difficult, since the vertical mucosal thickness (i.e., measured from the mucosal margin to the crestal bone level) at healthy implant sites varied considerably (from 1.6 mm to 7.0 mm) [11].
Consequently, the 8th European Workshop on Periodontology agreed upon reasonable case definitions for peri-implant diseases [10]. However, at the time being, data on the clinical features of peri-implant mucositis and peri-implantitis which were assessed based on the aforementioned case def-initions are still scarce.
As peri-implantitis is becoming a more common condition, its treatment is crucial for maintaining functionality of the implant. According to the con-sensus report of the World Workshop on the Classification of Periodontal and Peri-implant Diseases and Conditions (2017) [12], anti-infective peri-implantitis treatment strategies are successful in decreasing soft tissue in-flammation and in suppressing disease progression. Despite numerous pro-tocols suggested for peri-implantitis management, treatment of the
gy is still considered unpredictable [13, 14] and appears to be influenced by a variety of different prognostic factors, such as the configuration of the pe-ri-implant bone defect [15], the physicochemical properties of the bone filler [16, 17], the surface characteristics of the affected implants [18, 19], and implant location [20]. To optimize management of the disease, better un-derstanding of possible prognostic factors of peri-implantitis therapy is nec-essary.
1. AIM AND OBJECTIVES OF THE
STUDY
The aim of the study:
The aim of the present study is to investigate and update clinical and di-agnostic parameters associated with peri-implant tissue pathology and to evaluate the effectiveness of different peri-implantitis treatment modalities and determine the impact of initial bone grafting procedures for the surgical treatment outcomes.
Objectives:
1. To review and summarize the currently suggested peri-implantitis diag-nostics parameters and based on the available evidence propose guide-lines for peri-implantitis diagnosis and prognosis.
2. To evaluate the effectiveness of different treatment approaches for the clinical and radiographic symptoms of peri-implantitis by conducting meta-analysis and suggest a novel peri-implantitis treatment protocol. 3. Clinically evaluate parameters associated with peri-implant tissue health
and disease by using our developed diagnostic guide.
4. Clinically investigate the impact of previous bone augmentation proce-dures on the clinical outcome of surgical combined therapy of peri-implantitis.
2.
NOVELTY OF THE STUDY
1. Currently, a uniform classification and diagnostic methodology for peri-implantitis is lacking. This leads to confusion in diagnosis, making it hard to determine the prevalence of the disease, which in turn makes it hard for clinicians to decide whether the implant can be treated or if it has failed and must be removed. Therefore, we aimed to propose ra-tionale for diagnosis and prognosis of peri-implantitis.
2. Presently, there are many treatment protocols suggested for peri-implantitis management, including non-surgical and surgical approaches. However, it is still hard to clarify which method is most effective at ar-resting further disease progression. As the number of patients receiving dental implants is continuously increasing, it is important to have a thor-ough understanding of the effectiveness of various treatment interven-tions to better manage peri-implantitis.
3. At present, there are only few clinical investigations evaluating clinical parameters associated with peri-implant tissue health and disease (e.g., peri-implant mucositis and peri-implantitis) based on the definition sug-gested by the 8th European Workshop on Periodontology. Therefore, it is meaningful to determine clinical parameters related to peri-implant tissue health and pathology based on the most widely used case definitions. 4. As the therapeutic outcomes of peri-implantitis are still considered
un-predictable, it is very important to evaluate the factors that influence the prognosis of the treatment outcomes. To the best of our knowledge, this is the first study to evaluate initial bone grafting on peri-implantitis sur-gical regenerative treatment outcomes.
3. LITERATURE REVIEW
3.1. Etiology of peri-implantitis 3.1.1. Microbiological profile of peri-implantitis
Currently, there is a strong evidence from animal and human experi-mental studies that supports the bacterial etiology of peri-implantitis [1, 12]. Based on the findings of a clinical investigation, 30% of microbiota in peri-implantitis cases were found to consist of Tannerella forsythensis (Tf), Porphyromonas gingivalis (Pg), T. socranskii, Staph. aureus, Staph. Anaero-bius, Strep. intermedius, and Strep. mitis [21]. Higher counts of dontopathogenic bacteria were found in individuals with a history of perio-dontitis (p<0.001) [21]. The comparison of microbial profiles at healthy and diseased peri-implant sites revealed concentrations of Pg (p<0.01) and Td (p<0.05) as well as the total bacterial load (p<0.05), all of which were sig-nificantly higher in the peri-implantitis group compared to healthy implants [22].
It should be noted that, in contrast to these findings, other previous com-parative studies failed to detect significant differences between healthy and diseased peri-implant sites (e.g., peri-implant mucositis and peri-implantitis) with regard to microbiological profiles [23, 24]. In particular, the presence of periodontopathogens, including Actinobacillus actinomycetemcomitans (Aa), Porphyromonas gingivalis (Pg), Prevotella intermedia (Pi), Tannerella forsythensis (Tf), and Treponema denticola (Td)) in subgingival peri-im-plant sites were equally present in healthy peri-imperi-im-plant tissues as well as those diagnosed with mucositis and peri-implantitis [23].
Moreover, peri-implantitis was shown to be associated with a complex and heterogenous infection, including opportunistic pathogens, such as Pseudomonas aeruginosa and Staphylococcus aureus (S. aureus) [25], fun-gal organisms (e.g., Candida albicans, Candida biodinii, Penicillum spp., Rhadotorula laryngis) [25–27] and viruses (e.g., human cytomegalovirus, Epstein-Barr virus) [28].
Clinically, the peri-implant mucositis conversion to peri-implantitis in the absence of a proper plaque control was reported by Costa et al. [29]. In particular, 44% of individuals who had been diagnosed with mucositis without preventive maintenance developed peri-implantitis within a five-year period, while only 18% of patients undergoing regular post-operative control were diagnosed with peri-implantitis after five year [29]. These find-ings are supported by Ramanauskaite et al. [30], whose research indicates
that the lack of regular plaque control results in significantly higher fre-quencies of sites with mucosal bleeding, deepened peri-implant pockets, and alveolar bone loss and are associated with higher risk of implant loss [30]. Furthermore, patient noncompliance was a substantial risk factor, increasing the possibility of developing peri-implantitis (OR=0.13, p=0.01) [31].
3.1.2. Periodontitis as a risk factor for peri-implantitis
The microbiota associated with peri-implant diseases have been reported to be similar to the bacteria that cause periodontal diseases [32]. Hence, placing dental implants in patients with a history of periodontitis can be risky because the periodontal pathogens can colonize within days of healing [33]. This suggests that periodontal pathogens can translocate from periodontally involved teeth to the peri-implant sulcus in partially dentate patients [33, 34]. Therefore, the presence of residual periodontal pockets may represent niches of infection for adjacent implants. As a result, perio-dontitis patients may be exposed to a higher risk of peri-implantitis that may eventually lead to implant loss.
The systematic review and meta-analysis by Ramanauskaite et al. [35] aimed to evaluate whether susceptibility to chronic periodontitis has any influence on dental implant prognosis. The authors concluded that there is no difference, in terms of implant survival rate, between periodontitis and non-periodontitis patients [35]. However, patients with a history of perio-dontitis had higher incidence of having more implant marginal bone loss and developing peri-implantitis when compared with non-periodontitis pa-tients [35].
These findings align with the previously published systematic review, wherein periodontitis was found to be a risk factor for implant loss and re-lated with a higher risk of developing peri-implantitis [36]. Moreover, the recent World Workshop on the Classification of Periodontal and Peri-implant Diseases and Conditions (2017) confirmed strong evidence that a history of chronic periodontitis increases the risk of peri-implantitis [4].
However, in this context, it should be also noted that conflicting reports regarding the possible association between periodontitis and peri-implantitis exists. Thus, Marrone et al. [37] found neither current periodontitis nor his-tory of periodontitis to be statistically significant predictors for peri-implantitis. Also Rokn et al. [38] failed to demonstrate a higher risk for pe-ri-implantitis in patients with a history of periodontitis. These disagreements between the studies may be attributed to the differences in case definitions for periodontitis and /or peri-implantitis.
3.1.3. Risk factors/indicators
Although the bacterial challenge is considered to be the main etiological factor, peri-implantitis is a multifactorial pathology, and many factors, in-cluding implant related (e.g., shape, surface) and/or patient related (e.g., local and systemic factors) as well as clinician competence and different implant treatment protocols, may play a role in its etiology [39, 40]. The etiology of peri-implantitis and potential risk factors/indicators were exten-sively analyzed and reported during the World Workshop on the Classifica-tion of Periodontal and Peri-implant Diseases and CondiClassifica-tions (2017) [4, 12]. Based on the findings, there is a strong evidence that there is an increased risk of developing peri-implantitis in patients who have a history of chronic periodontitis, poor plaque control skills, and no regular maintenance care after implant therapy [4]. Data identifying smoking and diabetes as potential risk factors/indicators for peri-implantitis are inconclusive [4]. There is some evidence linking peri-implantitis to such factors as: post-restorative presence of submucosal cement and positioning of implants that make it difficult to perform oral hygiene and maintenance [4]. The evidence is equivocal regarding the effect of keratinized mucosa on the long-term health of the peri-implant tissues [12]. It appears, however, that keratinized muco-sa may have advantages regarding patient comfort and ease of plaque re-moval [12].
In this context implant-related factors should also be mentioned. When considering the implant design, tissue-level implants, in comparison to bone-level implants, were less frequently associated with the presence of suppuration and less plaque accumulation [31]. Concerning implant surface characteristics, it is known that implant surface properties may affect initial biofilm formation and have an impact on the implant survival rate [41]. However, whether the surface of the implants is of influence for long-term bone stability or peri-implantitis under clinical conditions in humans re-mains unclear, and the evidence seems to be contradictory [41]. In a Cochrane Collaboration review, it was concluded, that there were no signif-icant difference for failures, amount of marginal bone loss, and peri-im-plantitis between various implant systems [42]. Some recent studies report-ed lower bone loss around rough surface implants when adjacent to the im-plants with a smooth surface [43, 44], while other researchers observed less bone loss around implants with a smooth surface [45, 46]. In summary, there is not clear evidence that a particular implant design and/or implant surface would have an impact on peri-implantitis occurrence.
3.1.4. Onset- and progression of peri-implantitis
Previous retrospective clinical investigation attempted to evaluate the on-set and the progression of peri-implantiti [6, 7]. Particularly, one observa-tional study with a 9 year of follow-up indicated a non-linear, accelerating pattern of bone loss at the 105 affected implants [6]. Onset of peri-im-plantitis occurred early, as 52% and 66% of the implants presented with bone loss of >0.5 mm at year 2 and 3 respectively [6]. A total of 70% and 81% of subjects presented with ≥1 implants with bone loss of >0.5 mm at years 2 and 3 respectively [6]. The pattern of peri-implant bone loss has been described by Fransson et al [7]. Authors evaluated 182 patients with total off 419 implants that presented with progressive bone loss 47. For the-se implants, bone levels were associated using intra-oral radioghraphs ob-tained between the 1-year examination and a follow-up period of 5 to 23 years. The average bone loss was 1.7 mm and cumulative percentage of im-plants with bone loss ≥ 1 mm, ≥2 mm, or ≥3 mm were 68%, 32% and 10%, respectively [7]. In agreement with the previous study, a multilevel growth curve model revealed that the pattern of bone loss was non-linear, accelerat-ing and demonstrataccelerat-ing an increase variance over time. In addition, the mod-el also revealed that the pattern of peri-implantitis associated bone loss was similar within the same subject [7].
3.2. Definitions, clinical characteristics and diagnostic parameters of peri-implantitis
3.2.1. Definitions of peri-implantitis
Numerous definitions of peri-implantitis have been suggested by differ-ent authors (Table 3.2.1.1). In brief, Padial-Molina et al. [48] defined peri-implantitis as cases presenting PD >6 mm with bone loss ≥2 mm, detected radiographically. Froum et al. [49] suggested classification of peri-im-plantitis based on a comparison of bone loss, determined by the percent of bone loss related to the length of the implant. They classified the disease into early, moderate, and advanced types, having peri-implant measure-ments of ≥4 mm, ≥6 mm, or ≥ 8 mm and bone loss of >20%, 25–50%, and >50%, respectively [49]. Ata-Ali et al. [50]offered the classification of peri-implantitis based on the amount of bone loss (ABL) occurring beyond the biological bone remodelling together with signs of inflammation (BOP and/or Supp). Koldsland et al. [51] defined peri-implantitis as detectible bo-ne loss with inflammation and suggested different levels of peri-implantitis according to the ABL (≥2 mm and ≥3 mm) and pocket PD (≥4 mm and ≥6 mm).
Table 3.2.1.1. Currently suggested peri-implantitis clinical parameters and diagnostic guidelines. Author Year of publi-cation Baseline records Clinical parameters Radiographic evaluation Peri-implantitis/implant success
Pain PD BOP SUPP/
exudate Mobi-lity Other clinical indices 1 2 3 4 5 6 7 8 9 10 11 Koldsland et al. [51] 2010 Different levels of severity: > 4 mm; ≥ 6 mm + + Digital orthopantomograms and full-mouth status intraoral analog pic-tures used; different levels of peri-implantitis severity: bone loss ≥ 2 mm; and ≥ 3 mm
Peri-implantitis defined as detectible peri-implant bone loss with inflammation. Levels of severity: 1. bone loss ≥ 2 mm + BOP/SUPP at PD ≥ 4 or ≥ 6 mm; 2. bone loss ≥ 3 mm and BOP/SUPP at PD ≥ 4 mm or PD ≥ 6 mm Misch et al. [52] International Congress of Oral Implan-tologists (ICOI) Pisa Consensus Conference 2008 Bone-loss meas-urements should be related to the original marginal bone level at implant insertion. + +
May be of little diag-nostic value; routine probing depths are not suggested in the absence of other signs or symptoms.
+ + Conventional
periapical radiographs; computer-assisted images and customized X-ray positioning devices may be superi-or. Success; Satisfactory; Compromised (peri-implantitis); Compromised.
Success No pain No history of
exudate
No mo-bility
<2 mm
Satisfactory No pain No history of
exudate No mo-bility 2–4 mm Compromised = slight to moderate peri-implantitis May be sensitive PD >7 May have exudate history No mo-bility >4 mm, <1/2 implant body
Failure Pain Exudate
Mobi-lity
> 1/2 length of implant
Table 3.2.1.1 continued 1 2 3 4 5 6 7 8 9 10 11 Lindhe and Meyle [2] Sixth European Workshop on Periodontology
2008 Baseline probing measure-ments and radiographs should be recorded at the time of suprastructure placement. At minimum, annual monitoring of the peri-implant probing depths and the presence of BOP and SUPP must be performed. + Probing at four surfaces is essential for diagnosis of peri-implantitis. + BOP indicates the presence of inflam-mation in the peri-implant mucosa. + Suppura-tion is a sign of peri-im-plantitis.
+ When clinical signs suggest the presence of peri-implantitis, the clinician is advised to take a radiograph.
Peri-implant mucositis: can be identified clinically by redness and swelling of the soft tissue, but bleeding on probing is currently recognized as the important feature.
Peri-implantitis: a mucosal lesion is often associated with suppuration and deepened pockets but always accompa-nied by loss of supporting marginal bone. Lang and Berghlundh [1] Seventh European Workshop on Periodontology
2011 Time of prosthesis installa-tion should be chosen to establish baseline radiographs and peri-implant probing. This will be the reference from which the development of peri-implant disease can be recognized and followed in subsequent examinations.
+ + + When changes in
clinical parameters indicate disease (BOP, increased PD), the clinician is encouraged to take a radiograph to evaluate possible bone loss (PD > 5 mm + BOP ->take a radio-graph)
Peri-implantitis: changes in the level of crestal bone, presence of bleeding on probing and/or suppuration; with or without concomitant deepening of peri-implant pockets. Puss is a common finding at peri-implantitis sites.
Table 3.2.1.1 continued 1 2 3 4 5 6 7 8 9 10 11 Froum et al. [49] 2012 Obtain a periapical radiograph immediately following placement of the definite prosthesis.
+ + + + Early peri-implantitis;
Moderate peri-implantitis; Advanced peri-implantitis. Early peri-implantitis PD
≥4 mm BOP +/– SUPP noted on two or more aspects of the implant
<25% of the implant length
Moderate PD
≥6 mm BOP +/– SUPP noted on two or more aspects of the implant
25–50% of the implant length
Advanced PD
≥8 mm BOP +/– SUPP noted on two or more aspects of the implant
>50% of the implant length Kadkho dazadeh et al. [53]
2012 Implant success index Not reported + PD ≤4 mm; PD >4 mm + Is neither representative of a specific condition nor a predictable factor for further tissue breakdown
+ Long cone, parallel peri-apical technique; ≤2 mm (≤ 20%) – initia-tion of hard-tissue break-down
2–4 mm (<40%) – hard-tissue breakdown >40% – severe bone loss
Implant success index:
I. Clinically healthy: PD ≤4 mm; BOP –. II. Soft-tissue inflammation PD ≤4 mm; BOP +.
III. Deep soft-tissue pockets PD >4 mm; BOP +.
IV. Initiation of hard-tissue breakdown. V. Hard-tissue breakdown plus soft-tissue recession.
VI. Notable hard-tissue breakdown. VII. Notable hard-tissue breakdown plus soft-tissue recession.
VIII. Severe bone loss. IX. Clinical failure – Mobility.
Table 3.2.1.1 continued 1 2 3 4 5 6 7 8 9 10 11 Sanz et al. [10] Eight European Workshop on Perio-dontology
2012 Baseline clinical and radio-logical data should be established once the re-modeling phase post-implant placement has occurred.
Long-cone parallel radiographs; in the absence of previous radiogra-phic records, a threshold vertical distance of 2 mm from the expected marginal bone level following remodeling post-implant placement is recommended, provided peri-implant inflammation is evident.
Peri-implantitis – inflammatory process around the implant that includes both soft-tissue in-flammation and progressive bone loss of supporting bone beyond biological bone remod-eling.
American Academy of Periodonto-logy [54]
2013 Establish clinical and radiographic baseline at final prosthesis insertion. There is no single diagnos-tic tool that can, with certainty, establish a diag-nosis of peri-implantitis. + + + + Bacterial cultur-ing, inflammato-ry markers, and genetics may be useful in the diagnosis.
Periapical radiographs should be perpendicular to the implant body. CBCT may be considered depend-ing on the location of progressive attachment loss.
Used the definition by Sanz et al. [21]
Padial- Molina et al. [48]
2014 Baseline records should be used as a reference from which the development of peri-implant disease can be recognized and followed in subsequent examinations.
+
Should be repeated over time but not considered an abso-lute and isolated diagnostic tool.
+ + + Conventional radiographs: intraoral and panoramic are reliable; comput-er assisted are more accurate. Take a radiograph if PD < 5 mm + BOP/SUPP detected.
PD ≤5 mm + BOP/supp / + bone loss ≤2 mm = mucositis. PD >6 mm + bone loss ≥2 mm = peri-implantitis.
Table 3.2.1.1 continued
1 2 3 4 5 6 7 8 9 10 11
Ata-Ali et al. [50]
2015 X-rays must be obtained at implant placement and prosthesis installation to allow comparisons with the periapical X-rays obtained at periodic patient controls.
Peri-implant probing is essential for estab-lishing a diagnosis of peri-implant disease.
+ + Parallelized intraoral X-rays should be used in all dental implants to determine possible marginal bone loss.
Stage I: BOP and/or SUPP and bone loss ≤3 mm beyond biological bone remodelling.
Stage II: BOP and/or SUPP and bone loss >3 mm but <5 mm beyond biological bone remodelling.
Stage III: BOP and/or SUPP and bone loss ≥5 mm beyond biological bone remodelling.
Stage IV: BOP and/or SUPP and bone loss ≥50% of the implant length beyond biological bone remodelling.
The most recent definitions suggested by the consensus report of the World Workshop on the Classification of Periodontal and Peri-implant Dis-eases and Conditions (2017) indicate that the diagnosis of peri-implantitis requires the presence of bleeding on probing (BOP) and/or suppuration on gentle probing, increased probing depth compared to previous examinations, and the presence of bone loss beyond crestal bone level changes resulting from initial bone remodeling [12]. In the absence of previous examination data, the combination of the following parameters should be used for peri-implantitis diagnosis: presence of BOP/suppuration and PD ≥6 mm together with the bone level ≥3 mm of the most coronal portion of the implant [12]. This differs from the previously proposed threshold vertical distance of 2 mm from the expected marginal bone level following remodeling post-implant placement, which was suggested by the 6th, 7th, and 8th European Workshops on Periodontology [1, 2, 10].
3.2.2. Clinical characteristics of peri-implantitis
Peri-implantitis is characterized by inflammation in the peri-implant mu-cosa and subsequent progressive loss of supportive bone [12]. Clinically, signs of redness, swelling, bleeding on probing and/or suppuration, mucosal hyperplasia, increased probing depth values and/or recession of the mucosal margin, and radiographic bone loss are commonly used in case definitions for peri-implantitis [4, 47, 55, 56].
A recent case-control study with 262 implants from 141 patients reported that sites exhibiting peri-implantitis showed significant levels of BOP (OR=2.32), mucosal recession (OR=7.21), PD (OR=2.43), and suppuration (OR=1.76) (case definition according to 8th EFP [10] and AAP [54]) [56]. Mean PD values amounted to 2.63 ±1.21 mm at healthy and 3.26±1.57 mm and 4.58±1.71 mm at peri-implant mucositis and peri-implantitis sites, re-spectively [56]. According to the results, PD was the only diagnostic param-eter showing significance comparing implant mucositis and peri-implantitis sites (OR=1.76) [56].
Another investigation noted that the frequency of implants demonstrating PD ≥6 mm increased with increasing severity of peri-implantitis [55]. In particular, when evaluating 588 patients with 2,277 implants after a function time of 9 years, a PD >6 mm was recorded at 59% of all implants presenting with moderate/severe peri-implantitis (case definition: BOP + bone loss >2 mm) [55]. In contrast, at healthy implant sites (no BOP) diagnosed with peri-implant mucositis (BOP but with no bone loss >0.5 mm), 3% and 16% of implants showed PD ≥6 mm, respectively [55].
In cross-sectional analysis, Schwarz et al. [57] evaluated 238 patients ex-hibiting 512 implants and reported the peak of BOP of 67% at peri-implantitis sites (case definition: BOP + changes in radiographic bone level compared to baseline). Diseased implants were associated with higher fre-quencies of 4–6 mm PD than implants with healthy peri-implant mucosa and PD values ≥7 mm, which were only observed in one implant diagnosed with peri-implantitis [57].
A recent case-control study with 262 implants from 141 patients reported that sites exhibiting peri-implantitis showed significant levels of BOP (OR=2.32), mucosal recession (OR=7.21), PD (OR=2.43), and suppuration (OR=1.76) (case definition according to 8th EFP [10] and AAP [54]) [56]. Mean PD values amounted to 2.63±1.21 mm at healthy and 3.26±1.57 mm and 4.58±1.71 mm at peri-implant mucositis and peri-implantitis sites, re-spectively [56]. According to the results, PD was the only diagnostic param-eter showing significance comparing implant mucositis and peri-implantitis sites (OR=1.76) [56].
In cross-sectional analysis, Schwarz et al. [57] evaluated 238 patients ex-hibiting 512 implants and reported the peak of BOP of 67% at peri-implantitis sites (case definition: BOP + changes in radiographic bone level compared to baseline). Diseased implants were associated with higher fre-quencies of 4–6 mm PD than implants with healthy peri-implant mucosa and PD values ≥7 mm, which were only observed in one implant diagnosed with peri-implantitis [57].
In this context, it must be realized that the definition of a physiological PD at implant sites is difficult, as the vertical mucosal thickness (i.e., meas-ured from the mucosal margin to the crestal bone level) at healthy implant sites varies considerably (from 1.6 mm to 7.0 mm) [11].
Several consensus statements reported that suppuration as a common finding at sites diagnosed with peri-implantitis [1, 2]. Based on the findings of the recent study, the presence of suppuration significantly increases diag-nosis of peri-implantitis (OR=6.81, p<0.001) [56]. Another study that exam-ined implants with progressive bone loss and implants with stabile marginal bone levels found suppuration at 19% of the implants with progressive and 5% of the implants with stabile marginal bone levels [58].
The classification of bone defects occurring in peri-implantitis cases was suggested [59]. Following open flap surgery, peri-implant bone defects re-vealed two different classes: intrabony defects (Class I) and horizontal bone loss (Class II) (Fig. 3.2.2.1) [59]. According to the type of intrabony defects, Class I was subdivided into circumferential intrabony defects (Class Ie) and defects featuring a dehiscence (Classes Ia through Id). Most frequently de-tected bone loss configuration (55.3% of the cases) refers to Class Ie, which
was followed by Ib (15.8%), Ic (13.3%), Id (10.2%), and Ia (5.4%). It should be pointed out that, in majority of cases (79%), naturally occurring peri-implantitis lesions featured a combined supra (Class II) and intra-bony (Class I) defect configuration [59].
These data were also confirmed in a cross-sectional analysis, where the majority of intra-operatively assessed peri-implant bone defects revealed an uniform bone loss at all four implant aspects with a high frequency of Class Ie defects (15/46, 33%) [60].
Fig. 3.2.2.1. Combined surgical therapy of peri-implantitis at respective defect sites
(a) Class II: supra-alveolar exposure of implant surface. (b) Class Ia: dehiscence-type component on the buccal aspect of the alveolar crest. (c) Class Ib: circumference defect in mesial and distal areas with dehiscence-type component on the buccal aspect of the alveolar
crest. (d) Class Ic: circumference defect in mesial, distal and oral areas with dehiscence-type component on the buccal aspect of the alveolar crest. (e) Class Id: circumference defect in mesial and distal areas with dehiscence-type component on the buccal and oral aspect of the alveolar crest. (f) Class Ie: circumference defect in mesial, distal, buccal and
oral areas without dehiscence-type component [59].
3.2.3. Suggested peri-implantitis diagnostic parameters
Currently in the literature suggested parameters for peri-implantitis diag-nosis are reviewed and summarized in the publication by Ramanauskaite and Juodzbalys [47]. Below is a short summary of the possible peri-im-plantitis diagnostic parameters (Table 3.2.1.1).
a b c
d e f
Pain
Pain from the implant body does not occur unless the implant is mobile and surrounded by inflamed tissues or has a rigid fixation but impinges on a nerve. Presence of pain during implant function places the implant into the failure category [52].
Probing depth
The time of prosthesis placement should be chosen to assess baseline probing depth values [10]. Probing around the implants should be repeated over the time and in the presence of increased values compared to the base-line, clinicians should be encouraged to take a radiograph to evaluate possi-ble bone loss [1, 10, 48]. In the case of the absence of the baseline PD val-ues, presently suggested cut-off threshold values range between 4 [49] to 6 mm [12].
Bone loss
Conventional periapical radiographs were recommended for the diagnos-tic purposes [10, 48, 49, 52, 54]. Bone-loss thresholds to diagnose peri-implantitis suggested by the authors differ: Padial-Molina et al. [48] sug-gested that bone loss >2 mm indicated peri-implantitis, while Misch et al. [52] suggested the threshold of >4 mm. The implant success index by Kadhazahed et al. [61] reported that ≤2 mm (≤20%) of bone loss indicated the initiation of tissue breakdown, 2–4 mm (<40%) indicated hard-tissue breakdown, and >40% indicated severe bone loss. Ata-Ali et al. [50] suggested using different stages of peri-implantitis based on the amount of marginal bone loss beyond biological bone remodelling (Stage I: ≤3 mm; Stage II: >3 mm but <5 mm; Stage III: ≥5 mm; Stage IV: ≥50% of the im-plant length).
Peri-implantitis classification by Froum et al. [49] is based on a compari-son of bone loss determined by changes in the percentage of bone loss relat-ed to the length of the implant: bone loss of <25% of the implant length in-dicates early peri-implantitis, 25–50% of the implant length inin-dicates mod-erate implantitis, and >50% of the implant length indicates severe peri-implantitis. Koldsland et al. [51] classified peri-implantitis into different le-vels of severity according to the bone loss: ≥2 mm and ≥3 mm, accordingly. The 6th, 7th and 8th EWPs [1, 2, 10] suggested a diagnosis of peri-im-plantitis when changes in the level of crestal bone occur compared to base-line data. In the absence of previous radiographic records, a threshold verti-cal distance of 2 mm from the expected marginal bone level following re-modeling post-implant placement is recommended provided peri-implant inflammation is evident [10]. Based on the new recommendation presented
at the World Workshop on the Classification of Periodontal and Peri-implant Diseases and Conditions (2017), the threshold level for bone loss in the absence of previous radiograph has been suggested to be 3 mm [12].
3.3. Peri-implantitis treatment approaches
The main etiology of peri-implant diseases refers to plaque accumulation [40, 62]. According to the cause-related concept of therapy, plaque removal is a key strategy for the management of peri-implantitis [5]. The methods suggested for peri-impalntitis management can be divided into two ap-proaches: non-surgical and surgical.
3.3.1. Non-surgical therapy
The basis for peri-implantitis non-surgical therapy is infection control through debridement of the implant surface, with the aims of debriding the adhered biofilm and reducing the bacterial load below the threshold level for causing disease [63]. Various methods for mechanical cleansing, including piezoelectric ultrasonic scaler or subgingival air polishing of the implant surface were suggested [64–66] (Table 3.3.1.1). However, in comparison to the hand instruments, these alternative approaches did not provide differ-ences in term of treatment results [64–67].
Adjunctive therapies, such as local antibiotics, laser application, antibac-terial irrigations and photodynamic therapy were shown to improve the effi-cacy of non-surgical therapy, the obtained clinical outcomes appeared to be limited to a period of six to 12 months and were particularly compromised at advanced defect sites [68–71].
Non-surgical therapy is stated to be ineffective for peri-implantitis man-agement [5, 72, 73]. This could be mainly attributed to the limited access to the implant surface, which makes it difficult to effectively clean the contam-inated implant surface using non-surgical treatment methods. Therefore, surgical interventions are often required [71].
Table 3.3.1.1. Non-surgical treatments Author/ study design Follow-up period (months) Number of patients/ implants Systemic
antibiotics Treatment Clinical treatment outcomes Radiographic treatment outcomes
1 2 3 4 5 6 7 Karring et al 2005 [64] Pilot study 6 11/22 No Group 1: ultrasonic device (Vector system) Group 2: mechanical debridement with carbon fiber curettes
BOP changes (%) mean±SD Group 1: baseline 63.6; after 6 months 36.4
Group 2: baseline 72.7; after 6 months 81.8 BOP was reduced
in group 1, when compared with
baseline, while it was increased in group 2 (p>0.1). PD changes (mm) mean±SD
Group 1: baseline 5.8±1.1; after 6 months 5.8±1.2 Group 2: baseline 6.2±1.6;after 6 months 6.3±2.2 In both treatment groups, PD did not
change between baseline and 6 months.
Bone-level changes:
Group 1 at baseline 6.8±1.7 mm; after 6 months 7.1±1.9 mm; difference -0.3±1 mm
Group 2: at baseline 7.4±2.1 mm; at 6 months 7.7±2.6 mm; difference -0.3±0.8 mm Intrabony component changes:
Group 1: baseline 4.1±2.2 mm; after 6 months 4.5±2.2 mm; difference -0.4±0.8 mm Group 2: at baseline 4±1.5 mm; after 6 months 4.1±1.5 mm; difference -0.1±0.4 mm No statistically significant
differences between baseline and the 6- month control
neither within each treatment group nor between treatments Schwarz et al 2005 [68] Pilot study 6 20/20 Group 1: 10 Group 2: 10 No Group 1: Er:YAG laser (ERL) Group 2: mechanical debridement using plastic curettes and antiseptic therapy with chlorhexidine digluconate (0.2%)
BOP changes (%) mean±SD
BOP reduction: group 1 at baseline 83; after 6 months 31 (p<0.01)
Group 2: baseline 80; after 6 months 58 (p<0.01). Statistically significantly greater reduction in group 1(p<0.01)
PD changes (mm) mean±SD
Group 1: baseline 5.4±1.2; after 6 months 4.6±1.1 (p<0.01)
Group 2: baseline 5.5±1.5; after 6 months 4.9±1.4 (p<0.01)
No statistically significant differences between the 2 groups (p>0.01)
NR
Table 3.3.1.1 continued 1 2 3 4 5 6 7 Renvert et al 2006 [69] RCT 12 30/30 Group 1: 14 Group 2: 16 No Subgingival antimicrobial treatment using:
Group 1: minocycline micro-spheres
Group 2: chlorhexidine gel
BOP changes (%) mean±SD
Group 1: baseline 88±12, after 12 months 71±22 Group 2: baseline 86±14; after 12 months 78±13 Significantly greater BOP reduction in group 1 (p<0.01) PD changes (mm) mean±SD
Group 1: baseline 1: 3.9±0.7;at 12 months 3.6±0.6 Group 2: baseline 3.9±0.3; at 12 months 3.9±0.4 No significant differences between the groups (p>0.01) NR Renvert et al 2008 [70] RCT 12 32/32: Group 1: 17 Group 2: 15
Group 1: mechanical deb-ridement with local minocy-cline microspheres Group 2: chlorhexidine gel treatments were performed on 3 occasions: baseline and days 30 and 90
BOP changes (%) mean±SD
Group 1: baseline 86.5±20.1; after 12 months 48.1±207 Group 2: baseline 89.2±17.2; after 12 months 63.5±19.2 Significantly greater reduction in group 1 (p<0.01) PD changes (mm) mean±SD
Group 1: 3.85±1.04; at 12 months 3.55±0.98 Group 2: baseline 3.87±1.16; at 12 months 3.72±1.02 No difference between the groups (p>0.01)
Bone level changes:
Group 1: baseline 0.77±0.85 mm; after 12 months 0.7±0.84 mm Group 2: baseline: 0.41±0.7 mm; after 12 months 0.46±0.76 mm No statistical differences in radiographic bone levels were found. Renvert et al 2009 [65] RCT 6 31/31 Group 1: 17 Group 2: 14
No Group 1: mechanical deb-ridement with titanium hand-instruments
Group 2: mechanical deb-ridement with an ultrasonic device
BOP changes (%) mean±SD Mean bleeding at implant: Group 1: baseline 1.7±0.9; after 6 months 1.4±1.0 Group 2: baseline 1.7±0.6; after 6 months 1.2±0.7 PD changes (mm) mean±SD Group 1: 4.0±0.8;at 6 months 4.0±0.8 Group 2: baseline 4.3±0.6; at 6 months 3.9±0.8
NR
Table 3.3.1.1 continued 1 2 3 4 5 6 7 Sahm et al 2011 [66] RCT 6 32/32 Group 1: 16 Group 2: 16
No Group 1: amino acid glycine powder (AAD)
Group 2: mechanical deb-ridement using (MDA) car-bon curettes and antiseptic therapy with chlorhexidine digluconate
BOP changes (%) mean±SD
Group 1: baseline 94.6±15.8; after 6 months 51.1±24.7; difference 43.5±27.7
Group 2: baseline 95.3±9.6% after 6 months 84.3±15.5; difference 11.0±15.7
Significantly higher (p<0.05) reduction in group 1 PD changes (mm) mean±SD
Group 1: baseline 3.8±0.8;at 6 months 3.2±0.9; difference 0.6±0.6
Group 2: baseline 4.0±0.8 ; at 6 months 3.9±0.8; difference 0.5±0.6
No significant difference in PD reductions between the groups (p>0.05)
NR Renvert et al 2011 [74] RCT 6 42/42: Group 1: 21 Group 2: 21
No Group 1: Er:YAG laser Group 2: air-abrasive device
BOP changes (%) mean±SD
BOP decreased in both the groups (p<0.01) compared to baseline, but there was no difference between the groups (p=0.22).
PD changes (mm) mean±SD
PD reduction in group 1: 0.8 ± 0.5; group 2: 0.9±0.8; (p=0.55)
Bone-level decrease was diagnosed in 39% of im-plants in group 1 and 41.5% of imim-plants in group 2. No bone changes occurred in 2.1% of the implants in group 1 and 2.4% of the implants in group 2. Increases in bone level ranging from 2.1 up to 3 mm occurred in 6.3% of the implants in group 1, none in group 2; 0.1–1mm increase in 52% of implants in group 1, 56% in group 2.
No difference between the groups (p=0.42)
Table 3.3.1.1 continued 1 2 3 4 5 6 7 Schär et al (2013 [75] RCT 6 40/40: Group 1: 20 Group 2: 20
No All implants underwent mechani-cal debridement with titanium curettes followed by a glycine-based powder air polishing. Group 1 (test): Implants received adjunctive PDT.
Group 2: Minocycline micro-spheres were locally delivered into the peri-implant pockets.
BOP changes (%) mean±SD Decrease in BOP positive sites:
Group 1: baseline 4.03±1.66, after 6 months 1.51±1.41 (p<0.05)
Group 2: baseline 4.41±1.47; after 6 months 2.10±1.55 (p<0.05)
No statistically significant difference (p>0.05) between groups
PD changes (mm) mean±SD
Group 1: baseline 4.19 ± 0.55; after 6 months 3.83 ± 0.58 mm
Group 2: baseline 4.39 ± 0.77; after 6 months 3.90 ± 0.78
Statistically significant reduction from the baseline (p<0.05) in both groups
No statistically
significant difference between the groups (p>0.05) NR Deppe et al 2013[76] Pilot study 6 16 patients, 18 im-plants: Group 1: 10 implants Group 2: 8 implants
No Photodynamic therapy without surgical intervention
Group 1: moderate bone loss (< 5 mm)
Group 2: implants with severe defects (5–8 mm)
BOP changes (%) mean±SD
Comparable sulcus bleeding index in the 2 groups; no difference between the baseline and 6 months PD changes (mm) mean±SD
Group 1: baseline 3.3±0.8; after 6 months 2.9±0.5 (t value = –2.4)
Group 2: baseline 5.8±0.8; after 6 months 6.5±0.9 (t value = 2.05)
Distance from implant shoulder to bone: Group 1: baseline 3.9±0.8 mm; after 6 months 3.6±0.8 mm (t value = -1.125)
Group 2: baseline 8.7±0.7 mm; after 6 months 6.8±0.8 mm (t value = –6.27)
Table 3.3.1.1 continued 1 2 3 4 5 6 7 Bassetti et al 2014 [71] RCT 12 40/40: Group 1: 20 Group 2: 20
No All implants were mechanically debrided with titanium curettes and with a glycine-based powder air-polishing system.
Group 1 (test): Implants received adjunctive photodynamic therapy (PDT).
Group 2 (control): Minocycline microspheres were locally delivered into the peri-implant pockets of control implants.
BOP changes (%) mean±SD Decrease in BOP positive sites:
Group 1: baseline 4.03±1.66; after 12 months 1.74±1.37 (p<0.05) Group 2: baseline 4.41±1.47; after 12 months 1.55±1.26 (p<0.05) PD changes (mm) mean±SD
Group 1: baseline 4.39 ± 0.77; after 12 months 3.83 ± 0.85 Group 2: baseline 4.19 ± 0.55; after 9 months 3.89 ± 0.68
A statistically significant decrease in PD from baseline was observed in group 1 after 12 months and group 2 after 9 months (p<0.05).
NR John et al 2015 [67] RCT 12 25/25: Group 1: 12 Group 2: 13
No Group 1: amino acid glycine powder (AAD) Group 2: mechanical debridement using carbon curettes and antiseptic therapy with
chlorhexidine digluconate
BOP changes (%) mean±SD
Group 1: baseline 99.0±4.1; after 12 months 57.8±30.7; difference 41.2±29.5 Group 2: baseline 94.7±13.7; after 12 months 78.1±30; differ-ence 16.6±33.4 Group 1 revealed a signifi-cantly
higher BOP reduc-tion (p<0.05) when com-pared with group 2. PD changes (mm) mean±SD
Group 1: baseline 3.7±1; after 12 months 3.2±1; difference 0.5±0.9 Group 2: baseline 3.9 ±1.1; after 12 months 3.5±1.2; difference 0.4±0.8 p>0.05
NR
3.3.2. Surgical therapay
Numerous surgical approaches, including access flap surgery as well as resective and/or reconstructive approaches were shown to improve peri-implantitis treatment outcomes [5]. The major objective of surgical therapy is to provide access for removal of the biofilm and calcified deposits from the implant surface to enable healing and reduce the risk of further disease progression [77]. Reconstructive techniques also seek to restore the tissues that have been lost [13].
3.3.2.1. Access flap surgery
Access flap surgery (also called open flap debridement) is a basic sur-gical procedure that focuses on the decontamination of the implant surface and aims to maintain all of the soft tissues around the affected implant[63]. Clinical studies demonstrated that this surgical approach resulted in im-proved peri-implant tissue health (reduced probing depths (PD) and bleed-ing on probbleed-ing (BOP)) [78–82], and in the majority of cases was associated with stable marginal bone levels [78, 81, 82] (Table 3.3.2.1.1). However, access flap surgery of peri-implantitis was followed by a significant postop-erative soft tissue recession on the buccal aspect (1.0±0.9 mm) [78]. Given that, this surgical technique should be indicated in aesthetically non-demanding areas, since the possible exposure of the implant surface may lead to undesirable treatment outcomes.
Decontamination of implant surface and systemic antibiotics
The effectiveness of two different implant surface decontamination pro-tocols following access flap surgery was evaluated in a randomized cont-rolled clinical study (RCT) [80]. In one group, decontamination was per-formed using a 980-nm diode laser, and the other group underwent a con-ventional decontamination approach (mechanical cleaning and rubbing with cotton pellets soaked in sterile saline). After 6-months, no significant differ-ences were detected between the two investigated groups [80]. Moreover, a 12-month RCT revealed that the adjunctive use of systemic antibiotics sub-sequent to access flap surgery of peri-implantitis did not improve clinical, radiographic or microbiological treatment outcomes when compared with the control group [81].
Additional application of biologically active materials
Recently, a RCT evaluated the clinical and microbiological effects of ac-cess flap surgery of peri-implantitis alone or in combination with the
cation of enamel matrix derivate (EMD) [82]. Based on the findings, the adjunctive use of EMD did not result in improved clinical treatment out-comes (i.e., PD and BOP reduction) after 12 months, but was linked with increased prevalence of Gram +/– aerobic bacteria and increased marginal bone level [82]. In particular, an increase in marginal bone levels occurred in 75% (9/12) of the implants in the group treated with EMD compared to 46% (6/13) in the control group [82].
Treatment success
Depending on the applied composite success criteria treatment success was achieved in 5% (1/20) [77] to 35.3% (11/31) [81] of the patients at the 1-year follow-up. In the 5-year period treatment success was obtained in 63% (15/24) of the patients enrolled in a regular supportive therapy [79] (Table 3.3.2.3.2).
Table 3.3.2.1.1. Access flap surgery Author/ study design Follow-up period Number of patients/ implants Treatment Submerged/ non-submerged healing Systemic
antibiotics Clinical outcomes
Radiographic outcomes 1 2 3 4 5 6 7 8 Heitz-Mayfield et al. 2012, 2016 [78, 79] Prospective cohort study 1 to 5 years
24 /36 Access flap + mechanical debridement with titanium coated Gracey curettes or car-bon fibre curettes + irrigation with sterile saline and rubbing of the implant surface with cotton pellets soaked in sterile saline Non-submerged Amoxicillin (500 mg) + metronidazole (400 mg), 3 times/day, 7 days Implant level
Mean PD changes (mean±SD)(mm) baseline: 5.3±1.8 mm
12 months: 2.9±0.8 mm 3 years: 2.8±0.8 mm 5 years: 3.2±1.0 mm
Significant reduction compared to the baseline (p<0.001)
Number of sites with BOP (mean±SD) baseline 2.5±1
12 months : 1±1.2 5 years: NR
Significant reduction compared to the baseline (p<0.01)
Number of implants with suppuration (mean±SD)(%)
baseline: 21±58% 12 months: ±5.6% 3 years: 2±6.7% 5 years: 5 ±21%
Significant reduction compared to the baseline (p<0.001)
Facial recession (mean±SD) (mm) baseline: no recession,
12 months: 1.0±0.9 mm 5 years: 1.8±1.6 mm
Significant increase comparted to the baseline (p<0.001) Three implants in 3 patients had 0.6-1.0 mm bone loss. Three implants in 3 patients showed bone gain, while the rest of the im-plants had sta-bile marginal bone levels.
Table 3.3.2.1.1 continued 1 2 3 4 5 6 7 8 Papadopoul os et al. 2015 [80] RCT 6 months 16/16 Test: 8/8 Control: 8/8 Test
Access flaps + mechanical deb-ridement with plastic curettes + use of cotton swabs soaked in saline solution + use of a diode laser (low-power 980 nm) Control
Access flaps + mechanical deb-ridement with plastic curettes + use of cotton pellets soaked in saline solution Non-submerged No Implant level PD changes (mean±SD)(mm) Baseline: control: 5.52 mm test: 5.92 6 months: control: 4.31 test: 4.44 mm
Significant reduction compared to the baseline (p<0.05) Not significant difference between the groups (p>0.05) BOP changes
baseline: control: 93.8% test: 81.2%
6 months: control: 31.3% test: 23.8%
Significant reduction compared to the baseline (p<0.05) No significant difference between the groups (p>0.05) Clinical attachment level changes (CAL)(mm) baseline: control: 4.94 mm
test: 5.25 mm
6 months: control: 4.11 mm test: 4.46 mm
Statistically significant differences between baseline and 6 months (p>0.05)
NR
Table 3.3.2.1.1 continued 1 2 3 4 5 6 7 8 Isehed et al. 2016 [82] RCT 1 year 29/29 Test: 15/15 Control: 14/14 Test
Access flap + debride-ment with ultrasonic device and titanium hand instruments + cotton pellets soaked in sodium chloride Control
Access flap + deb-ridement with ultrasonic device and titanium hand instru-ments + cotton pellets soaked in sodium chloride + Emdogain (0.3 ml) Non- sub-merged No Implant level PD mean differences (mm): test: 2.8 mm control: 3.0 mm
No significant difference between the groups (p=0.270) BOP changes
BOP decreased from approximately 90% to 30%, but relapsed to nearly 70% at 12-months.
Did not differ from baseline to 12-months between the groups.
Suppuration changes Presence of suppuration: baseline: test group: 9/15 (60%)
control group: 6/14 (43%) After 1 y: test: 1/15 (7%) control: 1/14 (7%)
Mean marginal bone level changes (mm):
test: increase 0.9 Increased bone levels oc-curred in 9/12 (75%) of the implants Control: decreased 0.1 Increased bone levels oc-curred in 6/13 (46%) of the implants Hallström et al. 2017 [81] RCT 1 year 31/31 Test: 15/15 Control: 16/ 16
Access flap + mechan-ical debridement with curettes and cotton pellets soaked in saline
Non- sub-merged
Test group: post-operative systemic antibiotics – Zitrimax (Sandoz AS, Copenhagen, Denmark) 250 mg × 2 at the day of surgery, and 250 mg × 1 per day for 4 days.
Control group: no systemic anti-biotics
Implant level
Mean PD reduction (mean±SD) (mm) test: 1.7±1.1 mm, p<0.001
control: 1.6±1.5 mm, p<0.001).
Significant reduction compared to the baseline (p<0.001) No significant difference between the groups (p= 0.5) BOP changes (mean±SD)(%)
baseline: test: 100% control: 100% After 1 year: test: 12.4±9.2 % control: 13.3±11.1%
No significant difference between the groups (p=0.1)
Radiographic bone level (mean±SD)(mm): baseline: test: 4.6±1.6 mm control: 4.9±1.7, mm; (p=0.6)
After1 year: test: 4.0±1.6 mm, control: 4.5±1.5 mm The mean gain of alveolar bone: 0.4 mm
No significant difference between the groups (p=0.4)
3.3.2.2. Resective therapy
Resective peri-implantitis therapy is primarily aimed at reducing the probing depth around an infected implant and improving access for home care [77]. This surgical approach involves the reduction or elimination of pathological peri-implant pockets and apical positioning of the mucope-riosteal flap with or without bone recountouring. The systematic review by Ramanauskaite et al. [83] found resective peri-implantitis therapy to be ef-fective in reducing soft tissue inflammation and decreasing probing depths. In addition, to reduce the exposed implant surfaces’ roughness and thereby decrease bacterial biofilm formation, implant surface modification (i.e., implantoplasty) can be performed at the time of the surgery [84–86]. In a study by Romeo et al. [84, 85], implantoplasty was performed in nine out of 19 patients treated with a resective surgical procedure. At the 3-year follow-up, adjunctively performed modification of the implant surface positively influenced implant survival rates, significantly reduced PDs, suppuration, sulcus bleeding, and was associated with stable marginal bone levels in comparison to the control sites, where bone loss amounted to 1.45–1.54 mm [84, 85] (Table 3.3.2.2.1). Nonetheless, sites treated with implantoplasty revealed significantly more soft tissue recession (test group: 2.3 mm, control group: 1.64 mm) and consequently marked exposure of the fixture surface [85]. This finding suggests that resective peri-implantitis treatment in con-junction with implant surface modification should be restricted to non-aesthetic areas.
Decontamination of implant surface and systemic antibiotics
Numerous methods have been proposed for the decontamination of im-plant surfaces during the resective treatment of peri-imim-plantitis (Table 3.3.2.2.1). Mechanical debridement of implant surfaces was followed by the application of antibacterial/chemical agents, such as chlorhexidine gluco-nate [18, 87–89], hydrogen peroxide [90], sterile saline [18, 87, 89], phos-phoric acid [91] or antibiotic gel [84, 85].
Several RCTs evaluated the influence of decontamination strategy on the resective peri-implantitis therapy outcomes. Based on their findings, alt-hough the additional use of chlorhedixine gluconate (0.12% CHX) + cetyl-pyridinium chloride (0.05% CPC) substantially reduced the anaerobic bac-terial load on the implant surface compared to the mechanical debridement and the use of sterile saline [87], the adjunctively applied antiseptic (0.12% CHX + 0.05% CPC or 2.0% CHX) had no significant effect on the clinical treatment outcomes [87, 88]. These findings are in line with the results of
Table 3.3.2.2.1. Resective therapy Author/ study design Follow-up period Number of patients/ implants Treatment Submerged/ non-submerged healing Systemic
antibiotics Clinical outcomes Radiographic outcomes
1 2 3 4 5 6 7 8 Romeo et al. 2005, 2007 [84, 85] RCT 3 years 17/35 Test: 10/19 Control: 7/16 Test
Access flap + bone re-contouring + decontamination with metronidazole gel and solution of tetracycline hydro-chloride (3 min.) +
implantoplasty + apical flap placement
Control
Access flap + bone re-contouring + decontamination with metronidazole gel and solution of tetracycline hydro-chloride (3 min.) +apical flap placement
Non-submerged Before treat-ment all patients received antimicrobial therapy (Amoxicillin 50mg/kg/day for 8 days) Implant level PD changes (mean±SD)(mm) Baseline: test: 5.70±1.69 mm control: 6.52±1.62 mm
After 24 months: control: 5.5±1.47 mm
After 36 months: test: 3.21±0.56 mm
Higher PD values in control group (Student’s t-value of -+5.5) Bleeding index (mBI) changes (mean±SD)
Baseline: test: 2.83±0.47 control: 2.86±0.35
After 24 months: control: 2.33±0.74 After 36 months: test: 0.61±0.67 (Student’s t-value of +9.61) Mucosal recession(mean±SD)(mm) Baseline: test: 0.5±0.91 mm control: 0.23±0.84 mm
After 24 months: control: 1.64±1.29 mm
After 36 months: test: 1.96±1.42 mm
(Student’s t-value of +9.61) Recession index in control group significantly lower (Student’s t-value of -2.14)
Test: peri-implant bone resorption mesial and distal baseline: 3.82 mm and 3.94 mm. After 3 years: 3.81 mm and 3.94 mm.
The mean variation of marginal bone level values mesial and distal were 0 and 0.001 mm, respectively (p > 0.05). Control: peri-implant bone resorption mesial and distal baseline: 3.45 mm and 3.49 mm. After 3 years: 5.35 mm and 5.42 mm.
The mean variation of marginal bone level values mesial and distal were 1.44 and 1.54 mm, respectively (p < 0.05).
Table 3.3.2.2.1 continued 1 2 3 4 5 6 7 8 De Waal et al. 2014 [87] RCT 1 year 30/79 Test: 15/31 Control: 15/48 Test
Access flap + bone re-contouring+ decontami-nation with 0.12% CHX+0.05% cetylpyridinium chloride (CPC) + apical flap placement Control
Access flap + bone re-contouring+ decontami-nation with placebo-solution without CHX and CPC + apical flap placement Non-submerged No Implant level PD changes (mean±SD) (mm) baseline: control: 5.5±1.4 mm test: 6.6±1.6 mm
After 1 year: control: 3.7 ±0.8 mm test: 4.3±2.1 mm
No significant difference between the groups (p = 0.563) % of implants with BOP (mean±SD)(%)
baseline: control: 95.8±46% test: 96.8±30%
After 1 year: control: 94.7±36% test: 96.8±30%
No significant difference between the groups (p = 0.965) % of implants with suppuration (mean±SD)
Baseline: control: 31.3±15% test: 64.5±20%
After 1 year: control: 15.8±6% test: 29.0±9%
No significant difference between the groups (p = 0.977)
Mean marginal bone loss (mean±SD)(mm):
baseline: control: 3.6±1.9 mm test: 4.3±2.1 mm
After1 year: control 3.9±2.0 test: 5.0±2.5
No significant difference between the groups (p = 0.949)
