Journal of Dental Implant Research 2022; 41(3): 37-41  https://doi.org/10.54527/jdir.2022.41.3.37
Evaluation of long-term changes in bone graft height after maxillary sinus floor augmentation: a comparison between xenografts and synthetic material for bone grafts
Seung-Woo Lee , Tae-Seok Jang , Gyu-Jo Shim , Joo-Young Ohe
Department of Oral and Maxillofacial Surgery, School of Dentistry, Kyung Hee University, Seoul, Korea
Correspondence to: Joo-Young Ohe, https://orcid.org/0000-0002-4411-7871
Department of Oral and Maxillofacial Surgery, School of Dentistry, Kyung Hee University, 26 Kyungheedae-ro, Dongdaemun-gu, Seoul 02447, Korea. Tel: +82-2-958-9440, Fax: +82-2-966-4572, E-mail: ojyoung81@khu.ac.kr
Received: June 7, 2022; Revised: June 24, 2022; Accepted: June 27, 2022; Published online: September 30, 2022.
© The Korean Academy of Implant Dentistry. All rights reserved.

This is an open access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract
Purpose: The purpose of this study was to assess the height change of graft bones in a long-term follow-up after maxillary sinus floor augmentation procedures and compare the difference between xenografts and synthetic material.
Materials and Methods: The subjects comprised 28 patients (62 implants) who underwent sinus floor augmentation using the lateral window technique and staged implantation. Panoramic radiographs of the 28 patients were collected immediately after implantation and at follow-up.
Results: Changes in the grafted bone height showed a statistically significant decreasing tendency with time in both groups. However, there was no significant difference between the groups.
Conclusions: Both xenogeneic bones and synthetic bone substitute materials were resorbed with time but maintained their shape and properties after 10 years. Therefore, both materials are suitable for sinus augmentation and biphasic calcium phosphate, a synthetic bone substitute, has shown predictable stability in sinus augmentation during long-term follow-ups.
Keywords: Maxillary sinus floor augmentation, Bone substitutes, Dental implants
INTRODUCTION

The demand for dental implants has been increasing. And it is difficult to place implants in the edentulous posterior maxilla area due to poor bone density and maxillary sinus pneumatization. The missing state of upper molars can increase sinus pneumatization by resorbing bone through osteoclast activity in Schneider’s membrane within a few months1-3). The maxillary sinus floor tends to expand inferiorly, which makes the alveolar bone deficiency4). To improve bone volume supporting dental implants, maxillary sinus augmentation was introduced in 19805), which became widely accepted as a common reliable method6-8).

Graft materials for the sinus augmentation should make rapid new bone formation with volume stability. The long-term stability of the grafted volume can be an important factor for implant success9). Autogenous bone is the gold standard for bone graft, but it has some disadvantages like side effects in the donor sites and resorption of grafted bone10). Allograft and xenograft materials also have issues such as potential immune problems and infection11). Biphasic calcium phosphate (BCP), a synthetic material, is another popular graft material. It has been accepted as a bioactive and effective scaffold for new bone formation12). The popular combination of BCP, a mixture of hydroxyapatite (HA) and b-tricalcium phosphate (b-TCP) has been widely used13). Oss-pol (Donsung Biopol, Gyeonggi-do, Korea), one of the numerous graft materials for SFE, is a biphasic material composed of hydroxyapatite (HA) and b-tricalcium phosphate. Both anorganic bovine bone (ABB) and BCP produced similar amounts of new bone formation, with a similar histologic appearance, which means that both materials are suitable for sinus augmentation and the placement of dental implants14).

Because the resorption of grafted bone might compromise the stability of implants into the grafted maxilla, the change of the augmented bone would be one of the important factors for successful implant treatment.

The aim of this study was to confirm the long-term stability and to evaluate the difference between xenograft and synthetic material when being used for sinus augmentation. Our study hypothesizes that the volume stability of hydroxyapatite and b-TCP in sinus augmentation would be stable.

MATERIALS AND METHODS

From December 2006 to July 2011, sinus augmentation and staged implant placement were performed at the Department of Oral & Maxillofacial Surgery, Kyung Hee University Dental Hospital. To analyze the long-term grafted bone height changes, patients only who had panoramic radiographs taken at least 10 years after surgery were included in this study, and the cases were retrospectively analyzed. A total of 28 patients were included as study subjects, 62 implants were placed after maxillary sinus bone grafting. Patients who had a history of smoking habits, and systemic diseases such as uncontrolled diabetic mellitus, or autoimmune disease were excluded. Appropriate institutional review boards approved the study protocol (document ver. KH-DT22006).

1. Surgical procedure

Preoperative residual bone height was lower than 5 mm. Sinus floor augmentation was carried out under local anesthesia in a staged surgical approach. The maxillary sinus was grafted utilizing a lateral window technique as described by Kent & Block6). In brief, through a crestal incision and muco-periosteal flap elevation, the maxillary wall was exposed. A buccal window osteotomy was performed and the sinus membrane was elevated from the maxillary walls.

2. Bone graft materials

Bone graft materials were used in combination, and two groups, containing xenogeneic bones and synthetic bone substitute materials were studied. The group containing xenogeneic bones (31 implants) like Bio-Oss (Geistlich Pharma AG, Wolhusen, Switzerland) were mixed with autogenous bones obtained from the mandibular symphysis or maxillary tuberosity, or allogeneic bones such as Orthoblast (IsoTis, Lausanne, Switzerland) and grafted. In the group with synthetic bones (31 implants), Oss-pol (Donsung Biopol, Gyeonggi-do, Korea), which is a biphasic material composed of hydroxyapatite (HA) and β-tricalcium phosphate was packed with platelet-rich fibrin (PRF) into the maxillary sinus.

3. Radiographic evaluation

Five panoramic radiographs were taken from right after the implantation to the last follow-up period. Panoramic radiographs were obtained using an Ortho stage (AUTO III N CM; Asahi) or Promax (Planmeca, Helsinki, Finland). In the images, the vertical length was measured using calipers (Piview STAR, Infinitt Healthcare, Seoul, Korea). A single observer measured the length 3 times.

The grafted bone height was measured from the supreme height of grafted maxillary sinus to the implant apex (Fig. 1). To calculate the magnification ratio, the real length of the implant fixture and the measured height of the implant were used in the panoramic radiographs.

Figure 1. Measuring of grafted bone height. (A) Right after the implantation (T0). (B) Last follow-up (T4). IL: implant length, BL: bone level, GBH: grafted bone height, GBH=BL-IL.

The height of graft material was measured at 5-time points.

·T0: right after the implantation (baseline).

·T1: after the prosthetic loading (7 to 12 months later).

·T2: a year later after surgery (13 to 36 months later).

·T3: 3 years after surgery (37 to 60 months later).

·T4: last visit after the 4th measurement (10 years later).

4. Statistics

We compared the bone graft height over 5-time points. A statistical program (IBM Corp. SPSS 26.0. Armonk, NY, USA) was used for the statistical analysis. The resorption amount of graft material with time was evaluated through repeated-measures ANOVA (P<0.05) and comparisons between graft materials were assessed through independent sample t-tests (P<0.05).

RESULT

1. Changes in grafted bone height in the xenogeneic bone group with time

There were 31 fixtures with radiographs acquired at least 10 years after implant placement. In patients with xenogeneic bones, the mean grafted bone height right after placement was 2.88±1.73 mm, 2.36±1.90 mm after 7 to 12 months, 1.59±1.88 mm after 13 to 36 months, 0.87±1.86 mm after 37 to 60 months, and 0.35±2.09 mm over 10 years.

2. Changes in grafted bone height in the synthetic bone group with time

There were 31 fixtures with radiographs acquired at least 10 years after implant placement. The mean grafted bone height right after placement was 3.84±2.31 mm, 2.95±2.29 mm after 7 to 12 months, 2.08±2.60 mm after 13 to 36 months, 1.59±2.62 mm after 37 to 60 months, and 1.15±2.55 mm over 10 years.

3. Results with statistical analysis

Changes in grafted bone height showed a statistically significant decreasing tendency with time in both groups (P=0.001*) (Fig. 2). However, no significant difference was observed between groups (P>0.05) (Table 1).

Table 1 . Statistical analysis of both groups with time

TimeXenogeneic boneSynthetic boneP-value
T02.883.840.14
T12.362.950.57
T21.592.080.70
T30.871.590.38
T40.351.150.93


Figure 2. Changes in height showed a statistically significant decreas-ing tendency over time in both groups (P<0.05).
DISCUSSION

Sinus graft has been widely used. This retrospective analysis aimed to evaluate bone graft amount change over 10 years after sinus floor augmentation. When the quantity and quality of bone around implants are sufficient, the stability of sinus graft material can be achieved which is an important factor for successful implant placement9). The stability of materials in the maxillary sinus and the change of the grafted bone height over time have been important issues. Wanschitz et al.15) reported a 13.9% bone loss of graft materials after sinus augmentation. Hatano et al.16) assessed changes of a 2:1 mixture of autogenous bone and bovine xenograft for up to 10 years. It showed a statistically significant decrease in graft height until 2∼3 years after augmentation, but the bone resorption was minimal after that. Cho and Kim17) reported that the graft bone height decreased significantly in the first 1 year and then it remained stable when either autogenous bone or alloplastic bone was used. Jensen et al.18) reported on various resorption tendencies with different kinds of graft material. Several studies also have shown that the height of bone graft can be remained steady (Haas et al.19), Nystrom et al.20) and Hallman et al.21)). On the other hand, Nystrom et al.22), Listrom and Symington23) observed that the implant loading force caused graft height to be maintained at a steady level.

Taken together, this study supports most other studies but there was a significant decrease compared with directly after implantation, after the prosthetic loading, after 1 year, after 3 years, and after at least 10 years. This result suggested that graft materials were resorbed over 10 years but there were also remaining bones around implants that offered stability. However, there was no significant difference in resorption between the two graft materials.

Since we investigated patients who have radiographs taken after at least 10 years, there are limitations that we selected 2D panoramic images and excluded cases of implant failure and abnormal bone material resorption. Although bioresorption and remodeling is different procedures, this study could not differentiate between the two due to the limitations of not being able to evaluate the bone volume, density, and cortico-cancellous complex accurately. Also, in this retrospective study, diverse bone graft materials like autogenous bones, allogeneic bones, and PRF were mixed and used. Further prospective studies with 3D images like computed tomography and controlled variables will be needed to observe changes in the maxillary sinus and to compare the effect of the bone graft materials more accurately.

CONCLUSIONS

Graft materials were resorbed with time, but even after 10 years, the graft maintained the height consistently. Therefore, both materials are suitable for sinus augmentation. Additionally, there was no significant difference in height change between xenogeneic bones and synthetic bone substitute materials. Hydroxyapatite and b-TCP could also provide predictable stability in sinus augmentation during long-term follow-ups.

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