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ORIGINAL ARTICLE
Year : 2019  |  Volume : 22  |  Issue : 5  |  Page : 652-660

Analyses of clinical and osteoimmunological parameters on keratinized mucosa around dental implants


Department of Periodontology, Faculty of Dentistry, Karadeniz Technical University, Trabzon, Turkey

Date of Acceptance10-Jan-2019
Date of Web Publication15-May-2019

Correspondence Address:
Dr. E Baltacioglu
Department of Periodontology, Karadeniz Technical University, Faculty of Dentistry, Trabzon - 61080
Turkey
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/njcp.njcp_522_18

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   Abstract 


Introduction: This study investigated the effects of keratinized mucosa width (KMW) on peri-implant tissues by evaluating peri-implant clinical and bone resorption parameters. Subjects and Methods: Seventy-one dental implants (DIs) were separated based on adequacy/inadequacy of KMW. DIs with inadequacy KMW were grouped as peri-implant plastic surgery (PIPS) (free gingival graft/free periosteal graft groups) and maintenance (M) groups. DIs with adequacy KMW were grouped as the controls. Peri-implant clinical parameters were measured at the baseline and 6th month. Levels of receptor activator of nuclear factor κB ligand (RANKL) and osteoprotegerin (OPG) in peri-implant sulcular fluid were determined after clinical measurements using enzyme-linked immunosorbent assay. Results: In baseline, gingival index, bleeding on probing, and plaque index (PI) were lower in controls compared to the PIPS and M groups, and KMW was higher. At 6th month, peri-implant pocket depth and PI were lower in the PIPS groups and controls compared to the M group, and KMW was higher. While RANKL and OPG values and RANKL/OPG ratio at baseline were not significantly different between groups, OPG concentration and RANKL/OPG ratio in the 6th month were higher in the PIPS group compared to the M group (P < 0.05). The RANKL/OPG ratio decreased at 6th month in the PIPS groups and controls (P < 0.05). Positive and negative correlations were observed between peri-implant clinical and osteoimmunological parameters. Conclusion: This study demonstrated that adequate KMW and PIPS techniques exhibited positive effects on clinical peri-implant parameters and osteoimmunological mediators.

Keywords: Bone biology, grafts, implantology, molecular biology


How to cite this article:
Sukuroglu E, Baltacioglu E. Analyses of clinical and osteoimmunological parameters on keratinized mucosa around dental implants. Niger J Clin Pract 2019;22:652-60

How to cite this URL:
Sukuroglu E, Baltacioglu E. Analyses of clinical and osteoimmunological parameters on keratinized mucosa around dental implants. Niger J Clin Pract [serial online] 2019 [cited 2019 May 27];22:652-60. Available from: http://www.njcponline.com/text.asp?2019/22/5/652/258277




   Introduction Top


Peri-implant plastic surgery (PIPS) approaches facilitate the development of healthy peri-implant structures while obtaining satisfactory functional and esthetic results in soft and hard tissues.[1],[2],[3] Procedures to augment keratinized mucosa (KM) and increase soft tissue volume are well described.[4],[5],[6] KM consists of dense, collagen-rich connective tissue that is lined by a keratinizing epithelium and directly attached to the bone periosteum.[7] Furthermore, the function of KM for teeth and implants is predominantly for sensation and protection because the oral mucosa forms a physical barrier to the oral environment.[8]

Whether the presence or a certain zone of KM is required around dental implants (DIs) to maintain peri-implant health is controversial.[3],[4],[5],[6],[7] Some studies report significantly higher plaque accumulation[9],[10],[11] and bleeding on probing,[9],[10],[11],[12] more mucosal inflammation and recession,[11],[13] greater probing depth,[12],[14] and a greater incidence of peri-implantitis[5],[8],[15],[16] in regions with “inadequate” KM width (KMW <2 mm). Other studies concluded the opposite when maintenance therapy was considered.[7],[8],[15] Interproximal bone level and implant loss were not detected in such cases, but these evaluations could not be assessed completely because of methodological limitations.[5],[7],[15] Therefore, although no significant association was found between KM existence/nonexistence and peri-implant health, the establishment or maintenance of an adequate KMW is likely necessary.[5],[7],[8],[9],[10],[11],[12],[15]

Widespread use of implants has led to an increasing trend of technical and biological complications commonly grouped as peri-implant diseases.[17],[18],[19] These diseases may affect the peri-implant mucosa only (peri-implant mucositis) or also involve the supporting bone (peri-implantitis).[20] While peri-implant mucositis represents the host response of the peri-implant tissues to the bacterial challenge that is not fundamentally different from gingivitis representing the host response to the bacterial challenge in the gingiva, peri-implantitis may differ from periodontitis both in the extent and composition of cells in the lesion as well as the progression rate. Furthermore, it has to be realized that peri-implantitis may be initiated and/or maintained by iatrogenic factors (e.g., excess cement remnants, inadequate restoration-abutments seating, overcountouring of restorations, implant mal-positioning, and technical complications).[17],[18],[19] Inflammatory osteoclastogenesis represents the central pathological pattern of peri-implantitis. This process is mediated by proinflammatory mediators, but it is ultimately performed by the regulators of osteoclastogenesis.[21] Receptor activator of nuclear factor κB ligand (RANKL) is a key mediator of physiological osteoclastogenesis and pathological bone loss.[22],[23] Osteoprotegerin (OPG) is a natural inhibitor of RANKL, and it acts as a decoy and blocks the binding of RANKL to receptor activator of nuclear factor κB (RANK), preventing osteoclastogenesis.[24] Therefore, inflammatory bone destruction is regulated by the molecular interplay between RANKL, RANK, and OPG.[25] An examination of the levels of resorption biomarkers that are associated with osteoclastogenesis may help identify the link between the necessity of KMW and peri-implantitis/peri-implant mucositis in adequate/inadequate KMW cases. Therefore, this study hypothesized that bone resorption biomarkers would increase in inadequate KMW, and the RANKL/OPG ratio could be used as a diagnostic tool for the early diagnosis of related peri-implantitis. Furthermore, application of the PIPS methods to increase KMW may exert a positive effect on peri-implant health.

This longitudinal study evaluated the effects of KMW on peri-implant tissue health using clinical and osteoimmunological parameters and compared the results of PIPS treatment strategies [free gingival graft (FGG)/free periosteal graft (FPG)] for peri-implant sites with inadequate KMW.


   Subjects and Methods Top


Clinical studies

Study groups

Seventy-one DIs in 29 patients (15 males, 14 females, aged 36–65 years) undergoing two-stage implantation at Karadeniz Technical University, Faculty of Dentistry, Department of Periodontology were recruited from January 2011 to January 2014. The individuals in the study were nonsmokers or light smokers (<5 cigarettes/day). They had no systemic disease that could influence the outcome of implant or PIPS. Moreover, they had proper periodontal care and good oral hygiene [plaque index (PI) <1].[26]

The participants were informed about the study, and their written consent was obtained. Patients who achieved appropriate oral hygiene standards following phase I treatment were included in the study group. DIs were classified into four groups according to adequacy/inadequacy (KMW ≥2 mm/KMW <2 mm) of peri-implant KMW. DIs with a KMW <2 mm were classified to the FGG, FPG, and maintenance (M) groups, and DIs with a KMW ≥2 mm were the control group [Table 1].
Table 1: Study design and distribution of the characteristics of the groups

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Clinical parameters and peri-implant sulcular fluid (PISF) samples were measured at the 1st (baseline) and 6th month following stage-2 surgery in the surgical groups (FGG group + FPG group; PIPS groups) and the nonsurgical groups (M group + control group; non-PIPS groups). The same calibrated periodontist (E.S.) performed all clinical and radiographic examinations. Clinical peri-implant parameters were measured in duplicate. All the PIPS procedures were performed by another periodontist (E.B.) who had a 10-year PIPS experience.

Clinical measurements

Peri-implant pocket depth (PPD) and gingival recession (GR) (measured using a Michigan “0” probe with Williams markings) (Hu-friedy, Chicago, IL), gingival index (GI), bleeding on probing (BOP), and PI were determined in all groups.[27],[28] To measure the KMW, mucogingival junction was assessed by the “rolling technique” and the distance between the free gingival margin and the mucogingival junction was measured at the midbuccal aspect.[29]

Patients in PIPS group were asked to complete a questionnaire form of pain with a visual-analog scale (VAS, 0–10 cm) for 10 days following surgery. The cut points on the pain VAS were no pain (0–4 mm), mild pain (5–44 mm), moderate pain (45–74 mm), and severe pain (75–100 mm).

Sample collection

For each DI, PISF samples were obtained at three sites (midmesial, midbuccal, and middistal). Collections were performed in 2 min with standardized paper strips (Periopaper, Oraflow Inc., Amityville, NY, USA) and the volume was measured using a precalibrated electronic device (Periotron 8000, Oraflow Inc.).[30],[31] PISF-containing periopaper strips from each DI were pooled in glass tubes, to which was added 500 ml phosphate buffered saline (pH 6.5). Samples were eluted for 30 min at room temperature prior to removal of the strips and storage of the eluent in −80°C until analysis.

PIPS and maintenance procedures

FGG procedures were performed according to the technique described by Newman and colleagues [Figure 1].[32] Connective tissue with periosteum was obtained using a periosteal elevator from palatal tissue during FPG application.[3],[33] The whole peri-implant surgery was conducted by one of the authors (E.B.). Standardized professional oral hygiene procedures, including supra- and subgingival scaling and polishing, were performed subsequently.
Figure 1: Free gingival graft (FGG) application to the right posterior maxillary area at the first month following stage 2 surgery: (a) clinical view prior to FGG operation, (b) immediately after FGG operation, (c) 1 month after FGG operation, (d) 6 months after FGG operation, and (e) FGG

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Laboratory studies

RANKL and OPG assay

RANKL and OPG levels in the PISF samples were determined using commercially available human-specific enzyme-linked immunosorbent assays (ELISAs), in accordance with the manufacturer's instructions (Total sRANKL ELISA kit [BioVendor, Brno, CZECH REPUBLIC] and Osteoprotegerin ELISA kit [RayBio, Inc., Norcross, USA]).

RANKL and OPG levels in PISF were measured in the total amount of PISF that was collected in 2 min.[31] PISF RANKL and OPG concentrations were calculated by dividing the total RANKL and OPG by the volume of PISF.

Statistical analysis

The normality of the data's distribution was evaluated using the Shapiro–Wilk test. Comparisons among the groups regarding clinical and laboratory findings were evaluated using the Kruskal–Wallis, and Mann–Whitney U with the Bonferroni correction when needed. The differences in clinical parameters and GCF RANKL and OPG levels within the groups were measured using the Wilcoxon signed-rank test. Correlations between clinical parameters, RANKL and OPG levels, and RANKL/OPG ratios were investigated using Spearman's correlation coefficient. Reliability of the clinical investigator was tested by intraclass correlation coefficient (ICC), and all ICC values were found greater than or equal to 0.94. A value of P < 0.05 was accepted to be statistically significant. All statistical analyses were performed with a software program (SPSS v 17.0 for Windows, SPSS Inc., Chicago, USA).


   Results Top


Clinical findings

[Table 2] shows the mean values of the peri-implant clinical parameters. KMW findings and other clinical parameters are specified independently below.
Table 2: Intra and intergroup comparisons of clinical parameters at baseline and 6th month

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Intergroup comparisons

At baseline, clinical parameters showed no significant differences in the inadequate KMW groups (P > 0.05). GI, BOP, and PI values were significantly higher in the PIPS groups than in the controls (P < 0.05). GI and BOP were lower in controls compared to the M group (P < 0.05). The lowest clinical parameters and the highest KMW at baseline were observed in the control group.

At the 6th month, clinical parameters were not significantly different between the two PIPS groups (P > 0.05). KMW and clinical parameters in the PIPS groups showed no significant differences compared to the control groups (P > 0.05). Clinical parameters, except GR, were significantly lower in the FGG group and controls than in the M group (P < 0.05). PPD and PI were lower in the FPG group than in the M group (P < 0.05). KMW was higher in the PIPS groups and controls than in the M group (P < 0.05). At the 6th month, the lowest clinical parameters and the highest KMW were observed in the FGG group.

Intragroup comparisons

KMW in the PIPS groups increased in 6th month compared to baseline, but the other parameters generally decreased (P < 0.05). PPD in the control group decreased at the 6th month (P < 0.05), but there were no significant differences in other parameters (P > 0.05). In the M group, PPD increased and KMW decreased at the 6th month (P < 0.05), but there were no significant differences in other parameters (P > 0.05).

Laboratory findings

[Table 3] shows the mean values of the peri-implant laboratory parameters.
Table 3: Intra and intergroup comparisons of laboratory parameters at baseline and 6th month

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Intergroup comparisons

RANKL and OPG values and RANKL/OPG ratios showed no significant differences between the PIPS groups at baseline and 6th month (P > 0.05). Baseline and the 6th month laboratory parameters in the FGG group were not significantly different from the controls (P > 0.05), but the 6th month RANKL concentration was lower in the FPG group than in the controls (P < 0.05). All baseline laboratory parameters were not statistically different in the PIPS groups and controls compared to the M group except PISF volume, but the RANKL/OPG ratio was lower in the PIPS groups than in the M group in the 6th month (P < 0.05).

Intragroup comparisons

While the RANKL/2 value and RANKL/OPG ratio in the PIPS groups decreased, OPG concentration at the 6th month increased compared to baseline (P < 0.05). Moreover, while the RANKL/OPG ratio decreased also in the controls at 6th month, no (statistically significant) change of osteoimmunological parameters was observed at baseline and 6th month.

The mean ± SD of PISF volumes in the groups are given in [Table 3]. In the PIPS groups, PISF volume showed no statistically significant differences at the baseline and 6th month (P > 0.05). Moreover, PISF volume was lower in control group compared to the PIPS groups at the baseline, whereas the M group had higher PISF volume values at the 6th month compared to other groups (P < 0.05).

Correlations

Correlations between clinical parameters and PISF volume and RANKL and OPG levels and RANKL/OPG ratios in PISF were analyzed together for all groups. Correlations between clinical parameters and laboratory parameters exhibited positive and negative directions, but more correlations were observed at 6th month for PPD, laboratory, and other clinical parameters [Table 4].
Table 4: Correlations between the clinical periodontal parameters, and PISF RANKL, OPG levels, and RANKL/OPG ratios in all groups

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The mean ± SD of visual analogue scale (VAS) showing the pain intensity for 10 days in the PIPS groups is given in [Table 5]. Regarding the VAS for PIPS groups, there were no statistically significant differences between both groups (P > 0.05).
Table 5: Mean VAS for 10 days comparison in PIPS groups until the 10th day following the surgery

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   Discussion Top


Despite the absence of strong associations between the adequate/inadequate of KM and peri-implant health, recent findings suggested that the presence of at least 1–2-mm-wide KM is beneficial for the long-term prognosis of DIs.[7],[15] Moreover, few data on the overall success and longevity of PIPS techniques from well-controlled, long-term studies have been published.[3] To our knowledge, this report is the first study to compare the superiorities of KMW requirements and the two PIPS techniques using bone resorption biomarkers, which are potential diagnostic tools for peri-implantitis.

Increased pocket depth, plaque accumulation, and mucosal inflammation cause peri-implantitis in the presence of inadequate KM.[3],[7],[8],[16],[34] Peri-implant mucositis is defined as a reversible inflammatory change in peri-implant soft tissues without bone loss, and if not treated, it could lead to peri-implantitise.[35] In this study, baseline and 6th month peri-implant clinical and osteoimmunological findings indicated some differences depending on the adequacy (≥2 mm) or inadequacy (<2 mm) of KMW. According to our baseline findings which demonstrate the figures prior to the PIPS, with reference to BOP, GI, and PI values, the inflammatory indices of FPG, FGG, and M groups (inadequate KMW groups) were significantly higher than the controls (adequate KMW), which indicates the significance of KMW for peri-implant health.[16],[35] At 6th month, after a 3-mm increase in KMW in the FPG and FGG groups following PIPS, the PIPS groups also had adequate KMW. That is, when the FGG, FPG, and control groups (KMW adequate ones) are compared with the M group (KMW inadequate ones), maintenance treatment on its own may not be sufficient for peri-implant tissue, and that the increase in bacterial plaques increases peri-implant damage over a longer term with a cumulative effect.[7]

The host response of the peri-implant mucosa tended to be less pronounced than the gingiva with the increasing duration of plaque accumulation.[10] Therefore, poor oral hygiene is a risk factor for peri-implantitis.[7] The baseline and 6th month results of this study support the results of previous studies that showed an increase in PPD, BOP, PI, and mucosal inflammation in inadequate KMW.[7],[8],[10],[11],[12],[14],[36]

There are no studies that examined PISF bone resorption parameters in adequate/inadequate KMW, but PISF osteoimmunological markers in the pathological mechanism of peri-implantitis-induced bone resorption were studied in the recent years.[34],[37],[38],[39] In these studies, OPG and RANKL were significantly higher in peri-implantitis sites compared with healthy implant sites.[34],[37],[38],[39] Recent findings suggest an important role for the OPG/RANKL system in bone destruction in peri-implantitis, as previously observed for periodontitis.[34],[37],[38]

At baseline, there was no significant difference between the groups in terms of osteoimmunological parameters. Moreover, it was observed that at 6th month, the adequate KMW groups, compared to the inadequate ones, had inadequate RANKL/OPG and RANKL and higher OPG levels. At 6th month, the least RANKL was observed in the PIPS groups (especially in FPG group), and RANKL value of the FPG group was significantly lower than the M group. On the other hand, while the 6th month OPG concentration values of KMW adequate groups were significantly higher than the M group, OPG/2 min value between the groups was not found to be significantly different. Moreover, compared to PIPS groups, RANKL/OPG ratio was significantly lower in the M group. When the 6th month osteoimmunological parameters were compared according to baseline, RANKL and RANKL/OPG ration values decreased considerably while OPG values increased in general. When the findings are taken together, in parallel with the increase in clinical parameters in 6th month, increase in bone rezorbition parameters (RANKL and RANKL/OPG) at inadequate KM, compared to KMW surgery/non-surgery, demonstrated that inadequate KMW exerted negative effects on peri-implant health compared to adequate KMW, and peri-implant disease may develop.

FGG is among the earliest techniques to increase peri-implant KMW, but long-term clinical data are limited.[4],[5],[7],[36] That the lowest clinical parameters and highest KMW were observed in the FGG group in the 6th month shows the relative superiority of the FGG group. However, improvements in the FPG group were more apparent, although the differences between the groups in bone resorption parameters were not statistically significant. The periosteum is highly vascular and contains fibroblasts, osteoblasts and their progenitor cells, and stem cells.[3],[40] However, our previous study that assessed the clinical results of FPG and FGG in a case series observed that PPD was eliminated in inadequate KMW early peri-implantitis cases after FPG and KMW increased.[3] The results of the studies mentioned above and the PIPS results of the present study demonstrate that FPG exhibits immunological superiority and regenerative potential.[3],[33],[40] FGGs may be preferable because of the less invasive palatal wound, which results in less donor site morbidity and improved aesthetic results.[41] Although FGG appears to be a more advantageous technique in the ease of application and exhibits superiorities in clinical parameters, FPG may be preferred in inadequate KMW peri-implantitis cases because of its regenerative potential. Further studies that examine regenerative markers in FPG are required.

The results of the present study demonstrated positive relationships of PPD and GR with RANKL and a negative relationship with OPG at baseline and 6th month, which revealed a relationship between clinical parameters and bone resorption biomarkers in adequate/inadequate KMW that was similar to periodontitis and peri-implant tissue damage.[25],[34],[42] This study determined that PISF volume was positively correlated with clinical parameters and negatively and positively correlated with laboratory parameters. PISF volume increased significantly in the presence of inflammatory conditions. Conclusively, the degree of peri-implant inflammation in adequate/inadequate KMW is associated with bone resorption parameters.


   Conclusion Top


The results of this study show that bone resorption biomarkers also increased with clinical parameters in inadequate KMW as a diagnostic tool, and the degree of peri-implant inflammation is associated with bone resorption parameters. Additionally, two PIPS approaches exhibit similar clinical and immunological superiorities, and FGG is an ideal and effective treatment approach for ease of application. Conclusively, although maintenance treatment has some limited positive effects on peri-implant tissue health, PIPS application in inadequate KMW is an effective and reliable treatment approach for obtaining and maintaining a healthy peri-implant tissue. Long-term studies that contain more implants and more standardized methods will shed new light on the necessity of KMW and PIPS.

Financial support and sponsorship

This study was supported by a grant from the Scientific Research Commission of Karadeniz Technical University (grant number: 2010-127-007-2).

This study was presented as poster presentation to Europerio 8.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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