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  Table of Contents 
Year : 2019  |  Volume : 22  |  Issue : 10  |  Page : 1388-1395

Peri-implant bone defects: A 1-year follow-up comparative study of use of hyaluronic acid and xenografts

1 Kaya Dental Clinic, Izmir, Turkey
2 Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, Ondokuz Mayis University, Samsun, Turkey
3 Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, Ordu University, Samsun, Turkey

Date of Acceptance29-May-2019
Date of Web Publication14-Oct-2019

Correspondence Address:
Dr. O A Kaya
Kaya Dental Clinic, Izmir
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/njcp.njcp_502_18

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Objective: The aim of this study was to compare the efficacy of hyaluronic acid (HA) and xenografts on the repair of peri-implant dehiscence-type bone defects occur during implant placement. Patients and Methods: Forty-two dehiscence Class I type defects located on the buccal surface of the implants were included in this study. Defects were divided into two main groups as small sized (height of <3 mm) and medium sized (height between 3 and 5 mm). Both of the main groups were further divided into two subgroups as HA plus xenograft plus collagen membrane (HAXC) or xenograft plus collagen membrane (XC) applied groups. After grafting, repair of defect site was evaluated with the help of the cross-sectional images on cone-beam computed tomography at 6th and 12th months. Results: In both main groups, vertical bone height (VBH) was higher in defects repaired with HAXC (2.65 ± 1.12 mm) than in the XC (2.45 ± 1.10 mm) groups at the 6th month. However, the difference between two subgroups was not statistically significant (P > 0.05). Reduction in VBH was observed up to 6–12 months after prosthetic loading in all defect sites. This reduction was found statistically significant in medium-sized defects that grafted with XC (P < 0.05, paired t-test). However, in other subgroups, the difference between measurements at 6th and 12th months was not statistically significant (P > 0.05). Conclusions: According to the data obtained from this study, it can be concluded that HA did not have a significant positive effect on the repair of defects around dental implants.

Keywords: Alveolar ridge augmentation, dehiscence, dental implants, guided bone regeneration, hyaluronic acid, peri-implant defects

How to cite this article:
Kaya O A, Muglali M, Torul D, Kaya I. Peri-implant bone defects: A 1-year follow-up comparative study of use of hyaluronic acid and xenografts. Niger J Clin Pract 2019;22:1388-95

How to cite this URL:
Kaya O A, Muglali M, Torul D, Kaya I. Peri-implant bone defects: A 1-year follow-up comparative study of use of hyaluronic acid and xenografts. Niger J Clin Pract [serial online] 2019 [cited 2022 Oct 3];22:1388-95. Available from:

   Introduction Top

Dental implant therapy, long-term success has been proven in the literature, is the most preferred treatment option in the rehabilitation of complete or partial edentulism.[1],[2] However, in some instance, the implant therapy may become a challenge for clinician because of the reduced horizontal/vertical bone height (VBH) and the presence of local defects in alveolar crests that are occur as a result of periodontal diseases, tooth extraction, trauma, pathologic conditions, or age-related bone resorption.[3],[4] Dehiscence and fenestration type defects may occur during dental implant surgery, especially in horizontally deficient alveolar crests and alveolar crests with local defects. As a result of these defects, the rough surfaces of dental implants may become exposed and this negatively affects the survival of the implants. To increase long-term success, prevent esthetic and functional complications, the exposed surfaces of the implants, and bone defects need to be repaired.[5],[6]

In oral and maxillofacial surgery, fibrotic tissue healing is mostly an unenviable situation in the healing of bone defects. Guided bone regeneration (GBR) is generally preferred technique to overcome the shortcomings of fibrotic tissue healing, especially on bone defects around the dental implants.[7],[8] In 1989, first animal study about GBR technique was conducted by Dahlin et al.[9] for the repair of the defects around dental implants. The first clinical researches about simultaneous implant placement with alveolar bone augmentation by GBR technique were performed 1 year after this study.[10],[11] In many studies carried out till date, successful results about simultaneous implant placement with horizontal alveolar bone augmentation reported to have achieved.[12],[13]

In literature, bone grafts have shown to contribute to bone regeneration by their osteoinductive and osteoconductive potential, also prevent the collapse of the membrane into the defect site.[14] Autogenous bone is primarily preferred bone graft for alveolar bone reconstruction in oral implantology due to its osteoinductive potential. However, because of the disadvantages such as donor site morbidity, longer operation time, limited amount of bone obtained and unpredictable resorption pattern, other alternative bone graft substitutes are suggested to use in the repair of defects around the implants.[15],[16]

Hyaluronic acid (HA) is the main component of the extracellular matrix of the connective tissue and its morphological structure is considerably suitable to hold together other components of the connective tissue.[17] Researches have been shown that HA increases intracellular signal transmission, accelerates angiogenesis in the early stages of tissue regeneration, and guide the inflammatory process during wound healing.[18],[19] Thus, HA reported to contribute the healing of hard and soft tissues in a positive fashion. HA preparations are used in various medical fields such as dermatology, orthopedics, ophthalmology, and as well as in oral and maxillofacial surgery.[20],[21]

Previously, the healing of the buccal bone defects in immediately inserted implants has been investigated mostly using histological methods in animal studies, or by exposing the area with a second surgery in clinical studies. However, in the past few decades, the use of cone-beam computed tomography (CBCT) seemed to be very promising modality in terms of the evaluation of hard-tissue quantity around teeth and implants. This method has been used successfully in studies to evaluate the buccal wall dimension in the anterior maxilla and labial bone thickness around the maxillary anterior implants.[22],[23]

Nowadays, there still seems no consensus in terms of the biomaterial that creates the optimum results in the repair of the defects around the dental implants. Therefore, the aim of this study was to compare the effectiveness of HA, a newly developed biomaterial for bone healing, and xenografts in the repair of buccal dehiscence defects around dental implants.

   Patients and Methods Top

This prospective, single-center, randomized, controlled clinical study was performed in the Oral and Maxillofacial Surgery Department of Ondokuz Mayis University between 2014 and 2016. The study approved by the Institutional Review Board and clinical studies local ethics committee of Ondokuz Mayis University with the Declaration of Helsinki. Informed consent was obtained from all participants by explaining the procedure and possible risks and complications.

A total of 20 patients (11 males and 9 females, mean age 50 ± 15 years, age range between 24 and 85 years) who applied to our department for implant therapy, have horizontal insufficiency or local defect in alveolar crest after clinical and radiographic evaluation and meet the criteria of the American Society of Anaesthesiology (ASA) I and ASA II were enrolled in this study [Table 1]. Patients who have severe systemic disease (ASA III and ASA IV), used drugs that disrupt wound healing (e.g., immunosuppressive drugs), have had previous chemotherapy or radiotherapy in the head-and-neck region, smoke more than five cigarettes a day, have active periodontitis and cannot be regularly checked with CBCT (such as pregnancy) were excluded from this study. Before surgery, oral hygiene of all patients was evaluated and periodontal therapy was performed when necessary. Preoperative radiological and clinical examinations were done to evaluate bone volume at the proposed implant sites.
Table 1: Distribution of the implants among the patients

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Defect type was determined according to Tinti and Parma-Benfenati [24] classification, which described deficient alveolar ridges and defects around implants. Only Class I type dehiscence defects that occurred on the buccal bone wall of dental implants included in this study. Defects were divided into two main groups in the pursuance of vertical heights on the exposed buccal surfaces of the implants. Both of the main groups were further divided into two subgroups as HA plus xenograft plus collagen membrane (HAXC) or xenograft plus collagen membrane (XC) applied groups. Study and control groups were created according to the applied materials. While the study group was determined as the group that the defects repaired with HAXC, the control group was constituted of the defects repaired with XC only [Table 2].
Table 2: Defect groups

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Surgical procedure

All the surgeries were performed under local anesthesia using 4% articaine 1:100,000 adrenalin (Ultracain D-S Fort, Sanofi-Aventis, Deutschland GmbH, Germany) by the same surgeon. The mucoperiosteal flap was reflected after anesthesia with midcrestal and lateral vestibular releasing incisions. Straumann Standard Plus implants with SLA (sand-blasted acid etched) surface (Institut Straumann AG, Basel, Switzerland) were inserted using standard procedures following the manufacturer's guidelines. All implants were placed with adequate primary stability (≥35 Ncm). At the time of implant placement, the length from the most apical aspect of the defect to the coronal margin of the implant platform's rough surface were measured by calipers to measure the initial vertical height of the dehiscence on the buccal bone wall of the implants.

In the study group HA (Hyaloss matrix, Anika Therapeutics Inc., Bedfordshire, England) and xenograft (Bio-gen, Bioteck Inc., Torino, Italy), in the control group, only xenograft (Bio-gen, Bioteck Inc., Torino, Italy) were applied over the implant's exposed surfaces. HA was first hydrated with sterile saline solution (1 cc) and gel form of HA obtained. Then, HA mixed with xenograft particles (in a proportion of 1 HA: 3xenograft) before the application to the defect area in the study group. A resorbable collagen membrane (OsteoBiol Evolution, Tecnoss Inc., Torino, Italy) was used to cover graft particles in both study and control groups [Figure 1]. After closure of the wound, a piece of gauze was applied to the wound for hemostasis. Patients were prescribed antibiotics, analgesic, and mouth rinse twice daily for a week. Patients were instructed in adequate hygiene maintenance and a soft diet was recommended for 8 weeks. Patients were not allowed to use removable prostheses in the early healing period after bone grafting surgeries.
Figure 1: Intraoperative photograph showing (a) measurement of the defect, (b) grafting with xenograft plus collagen membrane + hyaluronic acid, (c) collagen membrane application

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Postoperative follow-up and data collection

Sutures were taken in the 10th day following the surgery and periodic follow-up visits were performed at 1st, 3rd, 6th, and 12th months for clinical evaluation. At the 6th month, gingiva formers were placed by performing small horizontal incisions from the alveolar crest to prevent any alterations on the grafted buccal surface. Subsequently, secondary implant stability was measured using Ostell device (Osstell AB, Gothenburg, Sweden). Implant stability quotient (ISQ) values of all implants were higher than 70 ISQ values at the 6th month and these values were adequate for prosthetic loading.

The sectional CBCT scans (Galileos Comfort Plus, Sirona Dental Systems, Bensheim, Germany) were used to evaluate the defect site improvement at 6th and 12th months postoperatively. The CBCT scans were performed following settings: dimension 50 mm × 77 mm, voxel size 76 × 75 × 76, grayscale - 14 bits, focal spot −0.5 mm, 98 kVp, 25 mAs, voxel size 0.25 mm, FOV 15 mm × 15 mm, scanning time 14 s, exposure time 2–6 s; rotation 204°.

Before measurements, the position of each implant was set to be parallel to the sagittal plane with the long axis of the implant. All radiological measurements were performed on cross-sectional images of 1 mm thickness from the buccal bone wall of the dental implants to evaluate the presence of any residual vertical bone defects.

  • A line: A line was drawn from the most apical part to the most coronal part of the implant and the length limit of the implant that should be within the bone was determined
  • B line: B line was drawn perpendicular to the long axis of the implant and the A line, from the most coronal point of the implant at the buccal surface
  • C line: The most coronal point of the alveolar bone (alveolar crest) at the buccal surface of the implant was marked and C line was drawn perpendicular to the long axis of the implant passing through this point.

The length between parallel lines B and C was measured in millimeters and the remaining defect heights were recorded. When the defect was completely filled, the residual defect height was recorded as 0 mm since the line B and C overlapped [Figure 2].
Figure 2: Measurement of residual defect height on cone beam computed tomography images

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The VBH values obtained from the CBCT at the end of the 6th month and at the end of the 12th month were determined according to the following formulas.

Initial defect height – 6th-month residual defect height = 6th-month VBH (mm).

Initial defect height – 12th-month residual defect height = 12th-month VBH (mm).

Furthermore, defect healing at 6 and 12 months was grouped according to residual defect height as;

  • Complete healing 0 mm
  • Partial healing < initial defect height
  • No healing ≥ initial defect height.

In order to ensure standardization and prevent possible errors, the measurements on CBCT scans were performed by two independent researchers twice with 10-day intervals [Figure 3].
Figure 3: Postoperative 6th and 12th months cone-beam computed tomography images showing (a) complete healing in hyaluronic acid plus xenograft plus collagen membrane group, (b) Complete healing in xenograft plus collagen membrane group, (c) partial healing in hyaluronic acid plus xenograft plus collagen membrane group, (d) partial healing in xenograft plus collagen membrane group

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Statistical analysis

The data were analyzed using the IBM SPSS V23 (Chicago, USA) package program. All data were characterized using descriptive statistics (n, mean, standard deviation [SD], median, minimum, maximum, and ranges). Normal distribution of the data was examined using the Shapiro–Wilk test. Independent sample t-test and paired sample t-test were used in the comparison to the means of normally distributed data. Results were presented as mean ± SD and were assessed with 0.05 level of significance.

   Results Top

A total of 45 implants were inserted and 3 of them which have low image quality that prevents to make measurements clearly, were excluded from the study. Total of 20 patients, 42 implants and 21 small, 21 medium-sized defects were evaluated for bone level changes. Soft-tissue healing was uneventful in all operated sites and membrane exposure did not observe in any of the cases. According to intra-class coefficient analysis, the correlation coefficient was 89% for 6th-month measurements and 99% for the 12th-month measurements. It was seen that the correlation between the repeated measures were coherent and reproducible (correlation coefficient >80%). From this point of view, a group of measurements were included in the study and assessments were made on these data.

The mean ISQ values before prosthetic loading at the 6th month were 77.69 ± 4.64 in small-sized defect group and 76.81 ± 3.79 in medium-sized defect group. HA applied defect groups showed higher ISQ values than the groups xenograft applied alone. However, the difference was not statistically significant (P > 0.05 paired sample t-test) [Table 3].
Table 3: RFA measurements among the groups

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The mean values and standard deviations of marginal bone measurements that recorded at baseline and the dimensional changes that occurred at 6th and 12th months after the operation are shown in [Table 4]. Dehiscence type defect height measurements after implant placement showed that the mean vertical defect was 1.92 ± 0.4 mm in small-sized defect groups and 4.09 ± 0.58 mm in medium-sized defect groups. The highest VBH (3.5 ± 0.65 mm) was observed in medium-sized defect group that applied HAXC at the 6th month and the lowest one (1.54 ± 0.39) observed in small-sized defect group that applied XC at the 12th month. In both small- and medium-sized defect groups, the VBH was higher in the groups that applied HAXC than the XC applied groups. However, the differences were not found statistically significant (P > 0.05 independent sample t-test).
Table 4: Defect height measurements at baseline and vertical bone heights at 6th and 12th months

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From the 6th to 12th months postoperatively, after prosthetic loading, the decrease was detected in VBH in all groups. However, this decrease was minimum and not statistically significant in HAXC applied groups (from 1.72 ± 0.69 to 1.69 ± 0.71 mm in small-sized defect group; and from 3.5 ± 0.65 to 3.29 ± 0.60 mm in medium-sized defect group) (P > 0.05 paired sample t-test). In XC applied groups, while the decrease was not found statistically significant in small-sized defect groups (from 1.54 ± 0.39 to 1.38 ± 0.50 mm) (P > 0.05 paired sample t-test), it was statistically significant in medium-sized defect groups (from 3.46 ± 0.6 to 2.60 ± 1.10 mm) (P < 0.05 paired sample t-test) [Table 5]. Healing status of the grafted implant sites is shown in [Figure 4].
Table 5: The comparison of hyaluronic acid plus xenograft plus collagen membrane and xenograft plus collagen membrane groups

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Figure 4: Graph showing the healing status among the groups

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   Discussion Top

Bone defects around dental implants are observed frequently when implants are placed in areas with dehiscence, fenestration, residual intraosseous type defects, and defects associated with extraction sockets. In all of these situations, repair of the defect is imperative to improve the long-term survival of the implants.[25] In an attempt to stimulate osteogenesis and reconstruct bone defects that occur associated with different types of injuries, diseases, and congenital malformations, various types of bone grafts or biomaterials have been used in dentistry to date.[26]

HA is a type of polysaccharide that produced by the plasma membrane of fibroblasts, and plays an important role in tissue regeneration and healing.[18] Recently, the use of HA in the field of oral and maxillofacial surgery has increased steadily. Nolan et al.[27] reported in their clinical study that the viscoelastic structure of HA has a positive effect on the healing of oral lesions such as aphthous ulcer. Gocmen et al.[28] have applied HA gel to the postextraction sockets after the third molar surgery. They reported according to the result of their study that HA has an anti-inflammatory effect and accelerates wound healing. Furthermore, studies have shown that HA acts as a primer for tissue scaffolding, enhances angiogenesis, is a good carrier for bone cells and growth factors, and also it accelerates the differentiation of cells by increasing signal transduction between mesenchymal cells and growth factors.[20],[29] It is reported that the effect of HA on bone healing is evident, especially in the early stage of healing.[29],[30] In the present study, because of the ethical issues, we have evaluated the grafted sites only by measuring the VBHs on CBCT scans. Thus, we have not clearly detected whether new bone formation occurs associated with HA stimulation in the early period. On the other hand, we observed a lower amount of decrease in VBH in the defect sites which grafted with HA and xenograft together, after prosthetic loading. This decrease was significantly lower in the middle-sized defect group grafted with HAXC. We think that the possible reason of this result may originate from the better organization of the graft particles with HA or more evident positive effect of HA in terms of defect filling with the increase in the size of the defect.

In the literature, successful results of clinical studies that use the HA gel alone or together with grafts and growth factors in periodontal bone defects or extraction sockets have been reported.[31],[32] However, Vanden Bogaerde et al.,[33] who used HA alone in bone defects, reported that the HA did not provide sufficient mechanical support in the single-walled bone defects. In our study, all defects were constituted of one walled dehiscence-type defects, and we used HA together with graft material to provide sufficient mechanical support in HAXC groups. During the operation period of this study, we observed that the viscous structure of the HA kept the graft particles together effectively, and the grafts manipulated very easily when used together with the HA.

Resorbable or nonresorbable membrane barriers are used to repair defects around implants with GBR.[34],[35] However, when nonresorptive membranes are used, it is necessary to remove these membranes by a second operation. Furthermore, studies on the repair of implant circumferential defects revealed that the use of nonresorbable membranes was associated with a higher risk of exposures and secondary infections compared to the resorptive membranes.[36],[37] Juodzbalys et al.[6] reported that they used collagen membranes and xenografts in the repair of dehiscence defects and no implant membrane exposures were seen. Similarly, in our study, a resorbable collagen membrane was preferred. We did not observe membrane exposure and associated secondary infection in any of the patients.

There seems no consensus on whether dehiscence or fenestration defects need repair with GBR in the literature.[38] In some studies, it has been reported that dehiscence or fenestration defects need to be repaired to provide adequate osseointegration of the implants and to improve long-term implant success.[7],[35] However, in some studies, it is suggested that repair of small dehiscence defects does not affect the long-term success of implants.[3],[5],[14] In this study, no gingival recession, gingival inflammation, or reflection of the gray color of the implant to gingiva was observed in any implant site. According to our results, it can be said that repair of defects around implants with GBR technique may be useful in preventing aesthetic complications that may occur even in small defects. In addition, we believe that it is useful to augment large dehiscence defects, especially higher than 3 mm, for long-term implant function and success.

Studies that dehiscence-type defects were included and repaired with GBR principles have high survival rates in the literature.[5] Juodzbalys et al.[6] reported that the implant survival rate was 100% after 5 years of defect repair and implant placement in their study. Similarly, Chiapasco et al.[3] reported that no failure observed after 3-year follow-up. In this study, there was no implant failure after 1-year follow-up in both groups in patients who underwent defect repair with GBR, and the survival rate of implants was 100%. Since our study is a short-term follow-up study, we think that the survival rate may change with time and need to be reevaluated in the long term.

There are some methodological limitations of our study depending on the CBCT device. The first of these is the possible formation of metal artifacts during the acquisition of images by CBCT of titanium implants. The other is to evaluate bone healing by comparing clinical measurements with radiographic measurements. However, it has been proven that linear measurements of dentofacial structures in CBCT devices reflect actual measurements in the clinic.[39] In the literature, when the voxel edge size of CBCT devices is smaller than 0.3 mm, it is reported that the image quality for the peri-metric bone measurements increase, artifacts decrease and the buccal bone can be better visualized.[40] The voxel size of the Galileos Comfort Plus CBCT device used in our study is <0.3 mm. In our study, one implant due to artifacts related to patient movement during imaging and two implants due to metal artifacts, were excluded from the study. Measurements of the remaining 42 implants that included in the present study were performed successfully.

   Conclusions Top

Our study suggested that HA did not have a significant positive effect on the repair of defects around dental implants. However, the use of xenograft with HA may be a viable option for the repair of the bone defects around the implants when compared to the use of xenograft alone in terms of easy handling and decrease in operation time.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

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

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