Vertical augmentation of the alveolar ridge is necessary in cases with extensive resorption of the alveolar ridge to perform esthetic prosthetic rehabilitation and implant insertion. A range of treatments, including guided bone regeneration (GBR), onlay block grafting, and distraction osteogenesis, have been studied for augmentation of the deficient alveolar ridge.1–3 GBR and onlay block grafting are predictable procedures that provide ridge augmentation.4–6 On the other hand, the associated surgical approach might lead to wound dehiscence, postsurgical swelling, and edema, often requiring a secondary surgical site to harvest the autogenous bone graft.7–9 Therefore, current surgical trends are toward minimally invasive techniques that minimize trauma, postoperative discomfort, and morbidity. Such techniques have been reported for periodontal regeneration and alveolar ridge augmentation procedures.10–12 A subperiosteal tunneling technique, which was performed with a small incision and minimal tissue dissection, has been reported using particulate hydroxyapatite and a particulate human mineralized bone allograft to enhance the thin alveolar ridges.13–15 In this study, a subperiosteal tunneling technique with Bio-Oss block onlay grafting was performed for bone augmentation in an atrophic alveolar ridge, and the results were analyzed histologically and clinically after 9 months to evaluate its usefulness.
Patients and Methods
This prospective study included 9 consecutive patients aged between 26 and 46 years (average, 41.2 years) with an edentulous atrophic posterior mandibular ridge. The primary inclusion criteria were healthy implantation sites, an edentulous mandibular molar area, a severely atrophic alveolar bone, and the need for bone grafting (Figs. 1 and 2). The primary exclusion criteria were health conditions that did not permit surgical treatment, any disorders in the planned implant area such as previous tumors, chronic bone diseases, infections in the adjacent tissues of the planned implantation sites, previous oromaxillofacial radiotherapy, any interfering medication such as steroid therapy or bisphosphate therapy, alcohol or drug abuse, heavy smoking (>10 cigarettes per day), uncontrolled diabetes, severe bruxism or other destructive habits, and pregnancy. Computed tomography (CT) scans were taken to assess the amount of bone available for implant placement. The patients had a buccolingual ridge dimension ranging from 2 to 4 mm or a less than 6-mm bone height above the inferior alveolar nerve. A total of 9 subperiosteal tunneling procedures with Bio-Oss block onlay grafting were performed on the 9 patients. Before surgery, the augmentation procedures were simulated using both the CT and the SimPlant (Materialise, Leuven, Belgium) software. The simulation was performed to determine both the shape of the defect area of the mandible and the shape of augmentation (Fig. 3). On the preoperative simulation, the maximum height of new bone needed ranged from 4.1 to 6.0 mm and averaged 5.1 mm. A Bio-Oss (Geistlich Biomaterials, Wolhuser, Switzerland) block was shaped based on the simulation (Fig. 4).
Using conventional methods, the inside and outside of the oral cavity were sterilized, and local anesthesia was administered with 2% lidocaine containing 1:100,000 epinephrine. A vertical incision of full thickness was made approximately 8 mm away from the defect area of the mandible, and a subperiosteal tunnel to the defect area was established. Tunneling was performed by lifting the periosteum using a periosteal elevator without a releasing incision on the periosteum. Care was taken not to damage the mental nerve while detaching the periosteum. The Bio-Oss shaped block was placed in the defect area of the mandible through the subperiosteal tunnel (Fig. 5). The block was used as the sole grafting material. After placing it in the defect, it was stabilized with a screw that had been placed at the bottom of the block without a barrier membrane (Figs. 6 and 7). The fragility of the bovine bone block should be noted, to prevent a fracture of the integrity of the block. If the block had a close adaptation to the recipient site and was stable under the periosteum, it was not fixed to the recipient site with screws (Fig. 8). After grafting, the vertical incision was closed using interrupted silk sutures (Fig. 9). The patients were not allowed to wear a removable denture before implant placement. The patients were assessed clinically and radiologically after 1 day, 1 month, and 6 months postoperatively (Fig. 10). CT scans were taken 6 months postoperatively to assess the postsurgical changes in the graft site (Fig. 11). The fixation screw that had been used to stabilize the block was removed with a stab incision over the screw 6 months postoperatively. Bone tissue segments were harvested 9 months later, at the time of implant placement (Fig. 12). To minimize the inclusion of original bone tissues in the sample, a bone core was harvested from the graft site at the implant site using a trephine bur with an internal diameter of 2.0 mm by an experienced oral surgeon (B-H.C). The new bone formation in the augmented site was then analyzed. In all, 18 implants (GSII; Osstem Implant, Co., Seoul, Korea) were placed in the graft sites, with a mean diameter of 4.5 mm and mean length of 10 mm, using a flapless implant procedure (Figs. 13 and 14).
The collected bone samples were immediately fixed in 10% formalin for 24 hours and then decalcified with Calci-Clear Rapid (National Diagnostics, Atlanta, GA) for 12 hours. The decalcified tissues were washed under running water, embedded in paraffin, sectioned at 5-μm thickness, stained with hematoxylin and eosin, and analyzed using light microscopy.
None of the patients developed complications such as wound dehiscence, infection, or fistula formation. None of the patients complained of paresthesia. In all patients, sufficient initial fixation of implants was obtained during implant placement. The stability of implants was evaluated with Periotest (Siemens AG, Bensheim, Germany) and ranged from −1 to −6 (average, −4.1). Using a conventional method, a permanent prosthesis was delivered approximately 3 months after implant placement.
In the radiographic evaluation, the bovine block was integrated with the basal bone, its bone density was normal, and the initial grafted height was maintained. The bone near the implant was examined using root apex radiographs, and the resorption of the marginal bone ranged from 0.1 to 1.1 mm (average, 0.5 mm). After placing the final prosthesis, occlusal loading was performed, and no macroscopic movement or displacement was detected during a 1-year clinical observation period (Fig. 15).
Histologically, compact, mature cortical bone lined by newly formed bone was observed at the top of the specimen. The osteotomized segment was composed of cortical bone, and no soft tissue ingrowth was observed in the segment. New bone formation was observed around the graft particles, and there was direct deposition of bone on the surface of the particles. New bone filled the spaces between graft particles, most of which were buried within new bone (Fig. 16). Osteoid was detected in some cases, indicating active bone formation within the graft material. No infiltration of inflammatory cells was detected.
The current procedures for the treatment of the atrophic alveolar ridge often require intraoral or extraoral bone harvesting, inferior alveolar nerve transposition, or distraction osteogenesis. These procedures have increased the morbidity and discomfort to the patient.16 In the present study, a Bio-Oss block was placed in an atrophic alveolar ridge through the subperiosteal tunnel. There were no soft tissue complications encountered during the 9-month post-grafting healing phase, such as soft tissue wound dehiscence, infection, or fistula formation. The subperiosteal tunneling procedure is attractive because it is minimally invasive. The technique offers the advantages of a more conservative surgical entry and less postoperative morbidity, thereby reducing the surgery time and minimizing the level of postoperative pain, edema, and infection. Therefore, the use of Bio-Oss block grafting combined with a tunneling technique avoids many of the difficulties associated with current therapies.
Several studies have reported the use of xenogenous block graft for ridge augmentation. In a study by Araujo et al,17 a Bio-Oss block was fixed on the buccal aspect of the jaw of dogs and covered with a collagen membrane using mucoperiosteal flap elevation. The authors found that after a 6-month healing period, large portions of the blocks were filled with connective tissue, with only moderate amounts of new bone formed at the base of the graft. With regards to the biological effect of the blocks on new bone formation, the present findings are in direct contrast to the findings of Araujo et al17 The 9 patients presented here provide evidence of the successful use of Bio-Oss block. In these patients, there was a considerable amount of newly formed bone surrounding the xenograft trabeculae. The results might be dependent on the effect of the periosteum. In the present study, the periosteum was lifted without flap elevation or a releasing incision of the periosteum. The preservation of the periosteum might help optimize bone formation. The role of the periosteum in osteogenesis, in which it serves as a source for pluripotent mesenchymal cells and osteoblasts, is well documented.18–21
Unlike traditional GBR procedures, in which the placement of an appropriate barrier membrane is integral to the success of the procedure, this study showed that new bone formation through the bovine bone block trabeculae can occur in the absence of a barrier membrane. This supports the hypothesis that barrier membranes are not required in xenogenous block grafting. The concept of a barrier membrane to create a secluded space and prevent the ingrowth of competing nonosteogenic cells into the defect area has been challenged by recent studies.22–25 Preclinical and clinical studies have supported the use of xenografts without a membrane for significant ridge augmentation in both horizontal and vertical defects, showing no significant differences in the sites treated with a xenogenous block with or without a mechanical barrier membrane.22–25 In addition, it is believed that a membrane might inhibit progenitor cell migration and angiogenesis by presenting a physical barrier to chemotaxis.
An interesting finding in this study was that the level of bone augmentation measured in height ranged from 4.1 to 6.0 mm. There were some limitations in the bone augmentation height in subperiosteal tunneling for ridge augmentation, possibly because of the limitations in lifting the periosteum. It is important to elevate the periosteum without perforation when using this technique. Based on the data, a subperiosteal tunneling procedure with a Bio-Oss block onlay graft is indicated when <6 mm of bone augmentation in an atrophic area of the mandible is needed to place the implants.
Many local variables are related to graft maturation, including the healing time, graft materials, and graft volume, all of which are related to the speed and amount of new bone formation. The healing time is perhaps the most significant value. The amount of new bone increases continuously with time. More new bone is formed as more time has elapsed from a graft. The materials affect the rate of bone formation. New bone forms mostly within the first 4–6 months with autogenous bone and within 6–10 months with Bio-Oss.26 The time required to form new bone is closely related to the graft volume. A large volume of the graft material placed into the defect requires a longer time before implant insertion. In the present study, implants were placed in the graft site 9 months later. Radiographic analysis revealed that the radiopaque area increased gradually in the time.
To evaluate bone regeneration in the graft site, a bone core biopsy is often used in clinical studies. The bone core sample in the present study was composed of cortical bone, and no soft tissue ingrowth was observed. But it is well recognized that the histological evaluation of core biopsy sample is not sufficient for a detailed quantitative analysis of the entire graft site. The findings from this study encourage further investigation of a subperiosteal tunneling procedure with a block onlay graft; further studies with animals will be necessary to determine how much of the entire graft block will become bone.
When a Bio-Oss block without the use of a barrier membrane was placed in an atrophic alveolar ridge through the subperiosteal tunnel, new bone formation through the bovine bone block was observed consistently in our series of bone augmentations. With implant placement performed 9 months after bone augmentation, sufficient initial fixation was obtained, with high resulting stability. Based on these results, ridge augmentation using a subperiosteal tunneling procedure with Bio-Oss bone blocks might be useful for implant placement in the atrophic alveolar ridges.
The authors claim to have no financial interests in any of the products mentioned in this article.
This work was supported by a research grant from Yonsei University Wonju College of Medicine (YUWCM 2009-13).
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