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Characteristics and frequency distribution of bone defect configurations in peri‐implantitis lesions—A series of 193 cases

Abstract Background Knowledge on peri‐implantitis bone defect characteristics and predictors is still limited. Purpose To describe peri‐implantitis bone defect characteristics and identify possible predictors. Methods Various parameters at patient‐ (age, gender, smoking, and supra‐structure), implant‐ (surface, type, connection, platform, and misfit), and site level (region, alveolar ridge position, defect characteristics, neighboring structure) were recorded retrospectively. Results Among 193 implants, the most prevalent defects were class Ic (25.4%), and Id (23.8%); a previously non‐described category “class Id with only one bone wall” was frequently observed (11.9%). Mean intrabony defect depth and width ranged from 4.5 to 6.2 mm and from 2.7 to 2.9 mm, respectively; mean dehiscence extent ranged from 2.8 to 7.0 mm. A total of 37.8% of the defects presented horizontal bone loss and an intrabony component; in 52.7% of the implants, total defect extent was >6 mm. Jaw region, implant position within the alveolar ridge, and implant/abutment misfit showed significant associations either to defect configuration and/or defect extent. Conclusion (a) Most common peri‐implantitis defects exhibited a combination of intrabony component and a buccal/oral dehiscence, while purely circumferential defects were relatively seldom; (b) implants with defects with bone dehiscence were placed more frequently closer to the lateral aspect of the ridge harboring the dehiscence; (c) implants placed in the lower anterior region had the highest risk for more severe peri‐implant bone loss; and (d) peri‐implant bone defects with only a single bone wall appropriate for regenerative procedure were relatively frequent.


| INTRODUCTION
Peri-implantitis is a site-specific pathological condition characterized by inflammation of the peri-implant soft connective tissue and progressive loss of implant-supporting bone. 1,2 With a weighted mean prevalence of 22% and an increasing number of annually placed dental implants, peri-implantitis represents a growing problem. 3,4 In moderate and advanced peri-implantitis cases, non-surgical therapy often does not achieve complete disease resolution and surgical treatment is required. 5 Specifically, a class I defect is defined by a buccal dehiscence and/or the presence of an intrabony defect, and a class II defect is characterized by horizontal bone loss. Class I defects are further subclassified (i.e., class Ia to Ie) based on the presence/absence of supporting bone walls and/or of intrabony defects at the four implant aspects (buccalmesial-oral-distal). 9 In this study, most intrabony defects (55.3%) had a circumferential configuration (i.e., class Ie). 9 In another study, based on 46 implants in total and 37 implants with an intrabony component, 40.5% of the intrabony defects presented with class Ie. 10 More recently, based on cone-beam computed tomography (CBCT) analysis of peri-implantitis lesions in a larger patient cohort with 158 implants, a class III configuration was added to the classification scheme, to describe defects with both intrabony and horizontal bone loss (i.e., combination of classes I and II). 11 Interestingly, circumferential defects were much more rare (i.e., only in 8.4% of the defects with an intrabony component) 11 compared to what was reported in the previous studies. 9,10 This difference among the later study and the former ones may be due to either the small patient cohorts (i.e., ≤40 implants) in the former studies 9,10 or due to the assessment method in the latter study, 11 which appears to be more prone to bias, especially in cases with thin alveolar bone. It has recently been shown, that in cases with a thin buccal bone (i.e., ≤1 mm thickness), detection of the buccal bone level at dental implants is largely inaccurate in CBCT images. 12 In this context, peri-implant bone defect configuration is considered crucial, affecting treatment choice (i.e., resective, regenerative, or combined surgical approach) and the outcome of surgical treatment. 7,17,8,18 Specifically, class Ie defects have shown a better response comparing to class Ib and Ic, after a regenerative approach including grafting plus a collagen membrane; that is, after 6 and 12 months of healing, mean probing pocket depth reduction and clinical attachment level gain was up to 1 to 1.5 mm higher in class Ie compared to other defect classes, while the worst outcome was observed at implants with class Ib and Ic defects at the lateral aspect of the alveolar ridge harboring the bone dehiscence 7 ; similar findings were reported in other recent studies. 8,17 Considering the importance of defect configuration for the outcome of surgical peri-implantitis treatment, it is interesting to know the prevalence of the various defect configurations and of any factors possibly contributing to the one or other configuration. The aim of the present study was (a) to assess characteristics and frequency distribution of peri-implant bone defects (i.e., configuration and extent) in a large patient sample, based on intra-operative recordings, and (b) to investigate a possible association of peri-implant bone defect characteristics to patient-, implant-, and site-related variables.

| Patient-, implant-, and site-related parameters
Various parameters were extracted and calculated from the patients' dental records and radiographs. The following parameters were recorded: At the patient level: • Age at time-point of surgical treatment for peri-implantitis (in years)

What is known:
• Peri-implant bone defect configuration is considered crucial for treatment choice and outcome. However, knowledge on bone defect characteristics and predictors is still limited.
What this study adds: • Implants with peri-implantitis mostly exhibit a combination of intrabony and buccal/oral dehiscence defect rather than purely circumferential defect, in contrast to what previously reported.
• Implants placed closer to the lateral aspect of the alveolar ridge develop frequently bone dehiscences.
• Peri-implant bone defects presenting only a single bone wall appropriate for regenerative procedure are not uncommon.
• Gender • Smoking status at time-point of surgical treatment for periimplantitis (i.e., smoker; non-smoker) • Number of implants included herein per patient • Type of supra-structure (i.e., single implant; multiple implants; teeth and implants combined; cross-arch restoration) • Number of implants splinted in the supra-structure At the implant level: • Implant surface (i.e., modified; smooth) • Implant type (i.e., bone level; tissue level) • Connection type (i.e., internal; external) • Platform type (i.e., match; switch) • Presence of an implant/abutment misfit (i.e., presence or absence of a gap between the implant and abutment/crown) At the site level: • Peri-implant bone defect configuration assessed intra-operatively according to Schwarz et al. 9 Bone defect configurations were intraoperatively recorded as classes I, II, or combinations thereof. Class I defects were further subclassified into class Ia (i.e., presence of a buccal bone dehiscence), class Ib (i.e., buccal bone dehiscence in combination with mesial and distal intrabony defects), class Ic (i.e., buccal bone dehiscence in combination with a circumferential defect), class Id (i.e., buccal and oral bone dehiscences combined with mesial and distal intrabony defects), and class Ie (i.e., circumferential defect). If defects, which fulfilled in general the above-described characteristics for class Ic or Ie but presented with minor additional bone dehiscences buccal and/or oral, they were still classified as Ic or Ie. If defects could not be assigned to one Note: The following bone defect configurations are summarized among "Others": class Ic but one wall missing (n = 3), inverted class Ic (n = 4), intrabony defect at a single aspect (n = 2), class Ia with the bone defect/dehiscence at another aspect (n = 2), class Ia with a second bone dehiscence at another aspect (n = 1), and class Ia with an intrabony component at a single aspect (n = 1). n indicates number. This parameter was further classified according to its extent into the following categories: (a) slight (i.e., 2 to 3 mm), (b) moderate (i.e., >3 to ≤6 mm), (c) advanced (i.e., >6 to ≤9 mm), and (d) severe (i.e., >9 mm).  distance to the neighboring tooth or implant was <1.5 or <3 mm, respectively, or as (c) "neighboring tooth" or (d) "neighboring implant" if the tooth or implant was in a distance of 1.5 to 5 or 3 to 5 mm, respectively. A digital radiography software (Sidexis version XG 2.52, Sirona, Bensheim, Germany) was used for the measurements on periapical radiographs taken with the parallel technique. All radiographs in each center were measured by a single examiner (Vienna: C. W., Malmö: K. B.) and a calibration based on the known size of the digital sensor was performed. The above-mentioned classes were used instead of the actual distance to minimize the effect of a measurement error due to non-standardized radiographs.
• Position of the implant in the alveolar ridge assessed at the buccal and oral aspect Three categories applied for this parameter depending on the distance of the implant surface to the lateral aspect of the alveolar ridge; that is, as (a) "outside" if the implant surface was more buccally or orally than the lateral aspect of the alveolar ridge, as (b) "≤1 mm" if the implant surface was within 1 mm to the lateral aspect of the alveolar ridge, and as (c)" >1 mm" if the implant surface was >1 mm to lateral aspect of the alveolar ridge.

| STATISTICAL ANALYSIS
Descriptive statistics were used and means, SD, and frequency distribu-

| Peri-implant bone defect configuration
Peri-implant bone defects were most often class Ic (25.

| Extent and characteristics of peri-implant bone defects
Defect extent and characteristics of the most prevalent peri-implant bone defect configurations (i.e., peri-implant bone defect configurations with a frequency >10 implants) are summarized in The total defect extent ranged from 5.9 ± 2.5 to 7.7 ± 3.0 and more than half of the implants (i.e., 52.7%) presented with advanced bone T A B L E 4 Implant characteristics of the most prevalent peri-implant bone defect configurations (i.e., peri-implant bone defect configurations with a frequency >10 implants)   Due to the low number of cases the premolar and molar region was pooled as "posterior" for the regression analysis. b No case with "multiple teeth + implants." c "Nothing" is defined as no neighboring structure within 5 mm; <1.5 mm is the cut-off value for a tooth being too close and <3 mm is the cut-off value for an implant being too close. loss (i.e., with a total defect extent >6 mm). Class Ic and Ie presented the highest percentage of severe bone loss (i.e., >9 mm total defect extent; in 25% and 20% of the implants, respectively), while the total defect extent of class II defects remained ≤6 mm in about 70% of the implants ( Figure 2). Furthermore, implants installed in the lower anterior followed by the upper anterior presented the highest percentage of advanced and severe peri-implant bone loss (i.e., about 60% each of the implants with advanced or severe bone loss were installed in the anterior region; Appendix 2a).

| Implant characteristics
Implant characteristics of the most prevalent peri-implant bone defect configurations are summarized in Table 4. Overall, the implants pres- that is, tissue level implants and implants with a misfit presented more often a slight peri-implant bone loss (i.e., 2 to 3 mm).

| Neighboring structure mesial and distal of the diseased implant
The data regarding the neighboring structure at the mesial and distal aspect of the implants in relation to defect configuration and the total defect extent is presented in Table 5 and Appendix 2c, respectively.
Overall, ≥49% of the implants had either mesially or distally no neigh-  were placed more often too close to the neighboring structure. Table 6 displays the associations between the potential predictors and total defect extent. In the univariate regression analyses age, jaw region, implant type, implant/abutment misfit, and supra-structure showed significant results. More specifically, a higher age, implants placed in the lower anterior, bone level type implants, lack of a misfit, and implants of a cross-arch restoration showed an increased risk for presenting with more severe peri-implant bone defects (i.e., an increased total defect extent). After combining these significant predictors together with gender (P = .079) in a multivariate regression analysis, only jaw region and implant/abutment misfit remained statistically significant.

| DISCUSSION
The present study based on intra-operatively assessed characteristics of 193 peri-implantitis defects in 100 patients undergoing surgical treatment, showed that (a) most common peri-implantitis defects In a more recent study 11 including a larger number of implants (i.e., 158 implants in 47 patients), purely circumferential defects (i.e., class Ie) were observed in only about 8% of the defects with an intrabony component, while the majority of the defects exhibited an intrabony component and a bone dehiscence, similarly to the present study. While some of those "non-classifiable" defects had a quite unique configuration and could not be grouped in a reasonable way as a "new" class, one specific defect type was present more often (i.e., 23-times or in 11.9% of all cases). These defects were related to class Id but were lacking one additional bone wall either mesially or distally ( Figure 1E-G); therefore, a new class is suggested: "class Id with only 1 wall" (i.e., Id-m and Id-d, when the mesial or distal bone wall is present, respectively). It appears thus important, for treatment planning or within the context of clinical studies, to have the possibility of a peri-implant bone defect configuration presenting only a single bone wall appropriate for regenerative procedure in mind.
As outlined in the introduction, studies have indicated that periimplant bone defect configuration and extent influence the outcome of reconstructive therapy of peri-implantitis., 7,17,8,18 although this has not been a consistent observation. 19 This may indicate that other factors, such as the difficulty to achieve effective debridement of the contaminated implant surface in deep circumferential defects can be challenging and thereby potentially limiting the outcome. Furthermore, it has been demonstrated that peri-implantitis lesions with limited to moderate bone loss (i.e., 2 to 4 mm prior to treatment) achieve a better clinical outcome 2 years after surgical therapy compared to implants with more severe bone loss (i.e., ≥5 mm). 18  Indeed, in the present study, Ie defects were more likely associated with posterior implants compared to anterior ones; implants harboring class Ie defects also had almost in 100% of the cases a distance >1 mm to the lateral aspect of the alveolar ridge, while implants with defects with bone dehiscence appeared placed more often closer to or beyond the lateral aspect of the alveolar ridge harboring the dehiscence. Truly, the residual alveolar ridge is wider more posteriorly comparing to more anteriorly, and this usually allows for a more central implant placement-in relation to the bucco-oral width of the ridgeand for sufficient bone wall thickness buccally and orally to the implant after installation. It is reasonable to assume that implants placed in wider/wide ridges are more likely to develop defects with more bone walls at the event of peri-implantitis, compared with implants placed in narrower/narrow ridges. This notion is supported by the results of a recent study, showing that implants harboring "4-wall defects" had a wider bucco-oral width distally and mesially to the implant, compared with implants with "2and 3-wall" defects. 8 Furthermore, it is also reasonable to assume that implants placed in "narrower/narrow" ridges will present with fewer bone walls at a "later" stage of disease, where the disease has resulted in complete resorption of the bone wall, than at an "earlier" stage of disease.
Indeed, horizontal bone loss height and intrabony defect depth herein, ranged from 2.3 ± 1.8 to 5.9 ± 2.5 mm and from 4.5 ± 2.4 to 6.2 ± 2.4 mm, respectively, in the various defect classes, which indicates a rather advanced disease stage at the timepoint of treatment in this specific population. In comparison, the average horizontal bone loss height and intrabony defect depth in the Schwarz et al 9 was 1.9 ± 1.3 and 2.9 ± 1.5 mm, respectively.
It is of interest whether specific patient-, implant-, and/or siterelated parameters predispose to a specific peri-implant bone defect configuration and/or a more advanced lesion. Indeed, in a previous study, 11 a significant association between the defect configuration and patient age and between the amount of vertical bone loss and smoking status, type of supra-structure, and proximity to the neighboring structures has been described. Specifically, peri-implant bone defects with intrabony components and a bone dehiscence but without horizontal bone loss were observed more often with higher age, while heavy smoking, fixed restorations, and implant proximity were significantly associated with a larger total defect extent. 11 Herein, the only predictor that appeared somehow consistently having a relevant effect on both defect configuration and extent was jaw region. Thus, implants placed in the lower anterior region had the highest risk to show a class Ic defect and the highest risk for more severe periimplant bone loss, for example, 14.5-and 3.5-times higher, respectively compared to the upper posterior. Although the width of keratinized mucosa was not registered in this study, the finding that implants in the lower anterior developed a more complex defect configuration and more severe disease may be, at least partly, also related to the frequent lack of adequate width or total lack of keratinized mucosa -i.e. in addition to the impact of the narrow alveolar ridge, discussed above. It has indeed been shown previously 11 that only a limited number of implants (i.e., <15%) with peri-implantitis lesions in the lower anterior presented ≥2 mm of keratinized mucosa. Lack of keratinized mucosa has been discussed as risk factor for peri-implant biological complications, because it is associated with plaque accumulation, and it appears more relevant for patients with a low compliance. [13][14][15][16] Surprisingly, presence of an implant/abutment misfit was associated herein with a reduced total defect extent. It can only be hypothesized that although the presence of a misfit may initiate a biological complication and result in some extent of peri-implant marginal bone loss, once a certain distance between the prosthetic gap and the marginal bone has been established, the misfit per se does not necessarily further drive disease progression, and other factors are probably more important. Indeed, a relatively recent review 24 concluded that the notion that prosthetic misfit leads to a higher rate of biological complications cannot be confirmed due to currently scarce information on this topic.
In perspective, this is a retrospective study with inherent limitations, which in turn may have compromised parts of the analysis. For example, despite that this study included 193 implants-the largest sample reported upon until now on this topic-some of the groups presented relatively small numbers; for example, implants with a machined surface or tissue level type implants were <15% of the total sample. Thus, lack of significance of tissue level implants to present a reduced risk for more severe peri-implant bone defects may, at least partly, be due to the low sample size of this type of implants. Furthermore, the peri-apical radiographs used herein for measuring the distance to the neighboring structures have not been taken under standardized conditions. Thus, classes of distances between the implant and the neighboring structures were used instead of the actual distance to minimize the effect of a measurement error due to non-standardized radiographs. Lastly, the majority of included implants has been placed elsewhere and there was no information on aspects related to the surgical procedure, for example, implant installation in connection with bone augmentation, type of augmentation material, immediate implant installation, implant misplacement, overheating during implant site preparation, overcompression of the (thick) cortical crestal bone, and so forth, which have been suggested to possibly affect the incidence and/or progression of peri-implantitis. 25 Therefore, no assessment of an association of these factors with defect configuration and extent was possible herein.
In conclusion, based on the current analysis, implants with periimplantitis exhibited a combination of intrabony and buccal/oral dehiscence defects rather than purely circumferential defects, in contrast to what reported previously. Furthermore, implants placed closer to the lateral aspect of the alveolar ridge developed frequently bone dehiscences, and implants placed in the lower anterior region had the highest risk for more severe peri-implant bone loss. Finally, the possibility of having a peri-implant bone defect configuration presenting only a single bone wall appropriate for regenerative procedure should be considered.