The International Journal of Periodontics & Restorative Dentistry

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1 The International Journal of Periodontics & Restorative Dentistry

2 355 Vertical Ridge Augmentation Around Implants Using e-ptfe Titanium- Reinforced Membrane and Deproteinized Bovine Bone Mineral (Bio-Oss): A Case Report Luigi Canullo, DDS* Paolo Trisi, DDS** Massimo Simion, MD, DDS*** The aim of this case report was to evaluate the ability of Bio-Oss used together with an expanded polytetrafluoroethylene, titanium-reinforced membrane to restore a vertical bone defect. Bio-Oss served as a filler material. After the membrane was removed, screw-type implants were placed. During this phase, cylindric bone samples were retrieved from the augmented area for histologic examination. The biopsy samples were composed of low-density trabecular bone with numerous interspersed graft particles. Clinical and histologic results demonstrated that this surgical technique could be a successful and predictable procedure for rebuilding a resorbed ridge to place implants. (Int J Periodontics Restorative Dent 2006;26: ) *Private Practice, Rome, Italy. **Private Practice, Pescara, Italy. ***Professor, Department of Periodontology, School of Dentistry, University of Milan, Italy. Correspondence to: Prof Massimo Simion, Department of Periodontology, School of Dentistry, Clinica Odontoiatrica e Stomatologica, University of Milan, Via della Commenda, 10, Milan, Italy. Vertical ridge augmentation techniques by means of guided bone regeneration (BR) have been shown to be predictable in the treatment of atrophic partial edentulous ridges with implant-supported restorations. 1 9 A clinical and histologic study 1 demonstrated up to 4 mm of supracrestal bone formation when a titanium-reinforced expanded polytetrafluoroethylene (e-ptfe) membrane was used. No grafting materials were used and the space under the membrane was filled with blood clot. These results were confirmed in experimental studies in animals. 2 5 To increase the potential for bone regeneration, grafting materials such as autogenous bone chips or demineralized freeze-dried bone allograft (DFDBA) have been used to fill the space under the membrane. Tinti et al 6 achieved up to 7 mm of supracrestal bone regeneration by combining autogenous bone powder, which was collected from the same surgical site with a filter in the suction tip, with the membrane. Simion et al 7 treated two different groups of 10 patients each. In the first group, DBDFA was used as a grafting material, and in the second Volume 26, Number 4, 2006

3 356 Fig 1 Intraoperative view after a full-thickness flap has been elevated. Fig 2 Bio-Oss has been packed into the defect. Fig 3 The ore-tex membrane is secured in place with two screws on the buccal side to cover the graft. group autogenous bone chips were used. Results confirmed that the combination of grafting material with a membrane could achieve a significant amount of vertical bone regeneration. These findings were further confirmed in a histologic study in humans. 8 Simion et al 9 presented a retrospective study with 1 to 5 years of follow-up that considered 123 consecutive implants placed in vertically augmented bone. The procedure was deemed successful and predictable if a nonresorbable titanium-reinforced membrane was used, a healing period of at least 6 months was allowed, and autogenous bone chips were used to fill the space. Deproteinized bovine bone has been positively evaluated as a bone substitute, both in experimental and clinical studies, for the treatment of peri-implant defects 10 and atrophic sinuses. 11,12 These studies demonstrated the capability of native bone to integrate with the xenogenic material by penetrating its scaffold and forming vital bone layers on the trabeculae. The aim of the present case report was to evaluate the use of deproteinized bovine bone (Bio-Oss, eistlich Pharmaceuticals) in combination with the membrane technique for vertical ridge augmentation. The use of this material could avoid autogenous bone harvesting, thereby reducing the invasiveness of the technique and postoperative discomfort for the patient. Method and materials One 65-year-old man was selected for this case report. He showed excellent general health and no detectable systemic contraindications to surgical treatment. He presented with Applegate-Kennedy Class II partial edentulism. Surgical technique Surgery was carried out after administering local anesthesia (Ultracaine DS Forte, Hoechst) combined with sedative premedication (diazepam, 5 mg orally 30 minutes before surgery). The surgical technique was performed as described previously. 3,8 11 A full-thickness incision was made within the keratinized mucosa from the distal aspect of the last remaining tooth to the distal end of the edentulous ridge. The incision was extended intrasulcularly and anteriorly to the mesial aspect of the first premolar. A vertical releasing incision was made at the mesiobuccal angle and at the distal aspect of the crestal incision. Buccal and lingual flaps were reflected with a periosteal elevator, taking care not to damage the mental nerve. Once exposed, the cortical bone was curetted with a back-action chisel to remove all residual connective tissue and the periosteum (Fig 1). A titanium-reinforced nonresorbable membrane (ore-tex, W. L. ore) was shaped to adapt it to the vertical defect without touching the distal margin of the adjacent tooth. One screw (Osteomed, Osteoclub) was inserted in the bone at the level of the mesial bone peak to stabilize the membrane as a tent. Two micro-tacks (Fri-Oss, Friadent) were used to attach the membrane on the lingual aspect. Deproteinized bovine bone (Bio-Oss) was soaked with blood and saline and positioned under the membrane to completely fill the defect (Fig 2). The membrane was finally secured buccally with two additional microscrews to achieve optimal stabilization (Fig 3). The International Journal of Periodontics & Restorative Dentistry

4 357 Fig 4 (left) Clinical presentation after 6 months of uneventful healing. Fig 5 (right) At the second surgery, the e- PTFE membrane is visible. Fig 6 (left) Three Brånemark implants have been placed in the vertically augmented bone. Fig 7 (right) Radiograph of definitive prosthetic restoration. A releasing incision in the periosteum was made at the base of the buccal flap to enhance the elasticity and to achieve tension-free adaptation at closure. On the lingual aspect, flap elevation to the mylohyoid line was sufficient to allow optimal mobility. Closure was performed with alternating nonresorbable horizontal mattress sutures and interrupted sutures. The patient received antibiotic prophylaxis (amoxicillin and clavulanic acid, 1 g every 8 hours for 7 days postoperatively) and 0.2% chlorhexidine gluconate mouth rinses (every 12 h starting 1 day preoperatively for 15 days). To minimize swelling and pain, the patient received steroids (4 mg once postoperatively; Soldesam, Laboratorio Farmacologico Milanese) and anti-inflammatory agents (200 mg every 12 h for 4 days postoperatively; Orudis Retard, Aventis Pharma). The sutures were removed after 12 days, following application of 0.2% chlorhexidine gel for 2 minutes to reduce bacterial contamination of the wound. The patient was then checked weekly for the first month and then once a month until second-stage surgery. Stage 2 surgery After 6 months of uneventful healing (Fig 4), the membrane (Fig 5) was removed. The thickness of the residual soft tissue layer was measured and the screw was removed. Two biopsies, one at each mandibular right premolar site and encompassing regenerated tissues, were collected with a 2.75-mm internal diameter trephine. Using a surgical stent, three Mark III Brånemark implants (Nobel Biocare) were placed in prosthetically ideal positions, with their heads located about 2 mm apical of the cementoenamel junction of the adjacent tooth (Fig 6). Sutures were removed after 12 days. Three months after implant placement, prosthetic restoration was finalized (Fig 7). Volume 26, Number 4, 2006

5 358 Histology and histomorphometry The specimens were infiltrated with resin, from a starting solution of 50% ethanol/resin and subsequently 100% resin, with each step lasting 24 hours. Photopolymerization was obtained with 48 hours of exposure to blue light. After polymerization, the block was ground to remove excess resin and then was fixed to plastic slides using a methacrylate-based glue. A Micromet high-speed rotating blade microtome (Remet) was used to separate the section from the block, thus obtaining a 250-µm-thick section. The section was then ground down to about 40 µm using a LS-2 grinding machine (Remet) equipped with waterproof grinding paper. After grinding was finished, each section was polished with a polishing paper and a 3-µm polishing cream. Toluidine blue staining was used to analyze the different ages and remodeling patterns of the bone, and basic fuchsin was used to distinguish fibrous tissue and increase contrast. The histomorphometric analysis was performed by digitizing the images from the microscope via a JVC TK-C1380 color video camera and a frame grabber. The images were acquired with a 10 objective that included the entire specimen surface. Subsequently the digitized images were analyzed with IAS 2000 image analysis software (Delta Sistemi). For each section, the most central portion was analyzed, and for each, the percentage was calculated and was expressed by considering the total length of the specimen. The parameters calculated using the IAS 2000 software were the following: Percent bone volume (%BV), indicating the area occupied by the bone matrix over the entire microscopic field. This is measured by outlining the bone surface area to determine the surface area of bone in the microscopic field and expressed as percentage of the total biopsy area. Percent graft volume (%V), indicating the amount of graft still present; expressed as the percentage of the total surface. Results Clinical results After 1 week, the patient showed moderate swelling in the submandibular region without pain, but no inflammatory symptoms were detectable. After 12 days, the sutures were removed. At the time of membrane removal, after 6 months of healing, the membrane appeared to be integrated with the surrounding tissues, with no signs of inflammation. Under the membrane, a 1.5-mm-thick soft tissue was present with minimal bleeding. The soft tissue was removed, exposing the regenerated, hard, bone-like tissue. Histologic results The sample was composed of lowdensity trabecular bone (%BV = 25.3%) with numerous interspersed graft particles (%V = 25.94%) (Fig 8). The graft particles were uniformly and widely dispersed in the biopsy space and were covered almost everywhere by layers of bone (Fig 9). On one side of the biopsy, continuous thin trabeculae of composite bone were visible, similar to cortical bone (Fig 10). Also, the trabeculae of the inner space were made of composite bone, with a central core of woven bone and external layers of lamellar bone. The bone surface was covered by osteoid bands, with mature and plump osteoblasts, and few signs of resorption were seen (Fig 11). The surfaces of the graft particles were mostly covered by newly formed bone. Some areas of these surfaces were exposed to the marrow soft tissue, as evidenced by the typical white unstained band (Fig 12), and some macrophages were seen (Fig 13). Osteoid bands and osteoblasts were seen on the surfaces of the graft that were exposed to the marrow spaces (Fig 14). A mild chronic inflammatory infiltrate was present in the marrow tissue. The International Journal of Periodontics & Restorative Dentistry

6 359 Fig 8 (left) eneral overview of the biopsy sample, which is composed of low-density trabecular bone with numerous interspersed graft particles () uniformly and widely dispersed in coronal zone of the biopsy. The apical zone of the biopsy is composed of a low-density trabecular bone from regeneration of bony socket (toluidine blue/basic fuchsin stain; original magnification 25). Fig 9 (top right) The graft particles () were almost completely covered by layers of bone (arrows) (toluidine blue/basic fuchsin stain; original magnification 50). Fig 10 (bottom right) On the surface of this sample, continuous thin trabeculae of composite bone are present, resembling cortical bone (arrows) (toluidine blue/basic fuchsin stain; original magnification 25). * O Fig 11 (left) The trabeculae were made of a composite type of bone, with a central core of woven bone (asterisk) and external layers of lamellar bone (arrows). The bone surfaces were covered by osteoid bands (O) with mature and plump osteoblasts on them (toluidine blue/basic fuchsin stain; original magnification 100). B Fig 12 (right) In some zones where the surfaces of the graft () were exposed to marrow soft tissue, the typical white unstained bands were found (arrows) (toluidine blue/basic fuchsin stain; original magnification 200). B = bone. Fig 13 (left) Some macrophages (arrows) were found on the surfaces of the graft particles () (toluidine blue/basic fuchsin stain; original magnification 200). Fig 14 (right) Osteoid bands and osteoblasts (arrows) were also seen on graft particle surfaces () that were exposed to the marrow spaces (toluidine blue/basic fuchsin stain; original magnification 200). Volume 26, Number 4, 2006

7 360 Discussion The aim of this preliminary case report was to evaluate the possibility of promoting vertical ridge augmentation in atrophic partially edentulous ridges with a combination of a titanium-reinforced membrane and deproteinized bovine bone (Bio-Oss). Several studies have demonstrated the capability of titanium-reinforced membranes to regenerate bone vertically when used in association with autogenous bone chips On the other hand, the use of a bone substitute could avoid bone harvesting from a donor site, thus reducing the invasiveness of the procedure and patient discomfort in the postoperative period. Deproteinized bovine bone has proven to be highly biocompatible and is also osteoconductive in that it is able to integrate with vital newly formed bone with a low rate of resorption. In an experimental study in dogs, Schlegel et al 16 compared the resorption pattern of autogenous bone chips with that of xenogenic Bio-Oss particles in sinus floor elevations. The authors observed that Bio-Oss was nearly undisturbed by resorption and measured a total bone volume loss of approximately 15% after 180 days, whereas the autogenous bone showed a 40% bone volume loss. Similar findings have been noted by others. 11,15,17 19 Simion et al, 9 in a long-term retrospective clinical study, demonstrated that jawbone augmented vertically by means of BR in association with autogenous bone chips has a tendency to show a slightly greater amount of marginal bone remodeling (1.71 mm, SD = 0.97) than in native bone. From this point of view, the slow degradation process of Bio-Oss could be of some benefit in maintaining the stability of the regenerated bone. This preliminary case report can be considered the first human observation of an atrophic ridge augmented vertically with ore-tex membranes in association with deproteinized natural bovine cancellous bone. Clinical and histologic findings demonstrated new bone formation up to the implant shoulder. However, upon membrane removal, a soft tissue layer (1.5 mm thick) was observed between the membrane and the regenerated, hard, bone-like tissue. This finding is in accordance with previous reports 1,7,13,14 demonstrating a periosteal-like soft tissue, which was quite thick (1 to 3 mm) when membrane alone was used and almost absent when the membrane was associated with autogenous bone chips. Little information can be drawn from the present single case report, but the relatively thick layer of residual soft tissue could indicate that a combination of Bio-Oss with autogenous bone chips may be more appropriate in the future for a demanding technique such as vertical ridge augmentation. The histologic examination confirmed the presence of newly formed vital bone (25.3%) almost completely surrounding Bio-Oss particles (25.94%) throughout the extent of the biopsy samples. The vital bone graft ratio was approximately 50%. This is in agreement with previous observations demonstrating that Bio-Oss particles can be well integrated with new bone; their replacement with natural bone appears to be a slow process. 11,15 19 Further clinical and histologic studies are needed to confirm these data, which must be interpreted with extreme caution because they have been obtained from a single case report. Long-term longitudinal studies are also needed to confirm the hypothesis of improved bone volume maintenance after implant loading when deproteinized bovine bone and membrane are used for vertical ridge augmentation. Conclusion Bio-Oss used together with titaniumreinforced e-ptfe membrane proved to be a clinically successful means for restoring a vertical bone defect. The predictability of this technique depends on a meticulous surgical protocol. The use of bovine bone matrix as filler material resulted in newly formed vital bone. The regenerated bone was proven clinically and histologically to accommodate implants. The International Journal of Periodontics & Restorative Dentistry

8 361 References 1. Simion M, Trisi P, Piattelli A. Vertical ridge augmentation using a membrane technique associated with osseointegrated implants. Int J Periodontics Restorative Dent 1994;14:497 51l. 2. Jovanovic SA, Schenk RK, Orsini M, Kenney EB. Supracrestal bone formation around dental implants: An experimental dog study. Int J Oral Maxillofac Implants 1995;10: Jensen OT, reer RO, Johnson L, Kassebaum D. Vertical guided bone-graft augmentation in a new canine mandibular model. Int J Oral Maxillofac Implants 1995;10: Renvert S, Claffey N, Orafi H, Albrektsson T. Supracrestal bone growth around partially inserted titanium implants in dogs. Clin Oral Implants Res 1996;7: Hammerle CHF, Schmid J, Olah AJ, Lang NP. A novel model system for the study of experimental bone formation in humans. Clin Oral Implants Res 1996;7: Tinti C, Parma-Benfenati S, Polizzi. Vertical ridge augmentation: What is the limit? Int J Periodontics Restorative Dent 1996;16: Simion M, Jovanovic SA, Trisi P, Scarano A, Piattelli A. Vertical ridge augmentation around dental implants using a membrane technique and autogenous bone or allografts in humans. Int J Periodontics Restorative Dent 1998;18: Tinti C, Parma-Benfenati S. Vertical ridge augmentation: Surgical protocol and retrospective evaluation of 48 consecutively inserted implants. Int J Periodontics Restorative Dent 1998;18: Simion M, Jovanovic SA, Tinti C, Parma- Benfenati S. Long-term evaluation of osseointegrated implants inserted at the time or after vertical ridge augmentation. Clin Oral Implants Res 2001;12: Fugazzotto PA. BR using bovine bone matrix and resorbable and non-resorbable membranes. Part 1: Histologic results. Int J Periodontics Restorative Dent 2003;23: Valentini P, Abensur D, Wenz B, Peetz M, Schenk R. Sinus grafting with porous bone mineral (Bio-Oss): A study on 15 patients. Int J Periodontics Restorative Dent 2000;20: Piattelli M, Favero -A, Scarano A, Orsini, Piattelli A. Bone reactions to anorganic bovine bone (Bio-Oss) used in sinus augmentation procedures: A histologic long term report of 20 cases in humans. Int J Oral Maxillofac Implants 1999;14: Dahlin C, Simion M, Nanmark U, Sennerby L. Histological morphology of the e- PTFE/tissue interface in humans subjected to guided bone regeneration in conjunction with oral implant treatment. Clin Oral Implants Res 1998;9: Simion M, Dahlin C, Blair K, Schenk RK. Effect of different microstructures of e- PTFE membranes on bone regeneration and soft tissue response: A histologic study in canine mandible. Clin Oral Implants Res 1999;10: Zitzmann N, Scharer P, Marinello C, Schubach P, Berglundh T. Long term results of implants treated with BR: A 5-year prospective study. Int J Oral Maxillofac Implants 2001;16: Schlegel KA, Fichtner, Schultze-Mosgau S, Wiltfang J. Histologic findings in sinus augmentation with autogenous bone chips versus a bovine bone substitute. Int J Oral Maxillofac Implants 2003;18: Araujo M, Sonohara M, Hayacibara R, Cardaropoli, Lindhe J. Lateral ridge augmentation by the use of grafts comprised of autologous bone or a biomaterial. An experiment in the dog. J Clin Periodontol 2002;29: Dies F, Etienne D, Abboud NB, Ouhayoun JP. Bone regeneration in extraction sites after immediate placement of an e-ptfe membrane with or without a biomaterial. A report on 12 consecutive cases. Clin Oral Implants Res 1996;7: Skoglund A, Hising P, Young C. A clinical and histologic examination in humans of the osseous response to implanted natural bone mineral. Int J Oral Maxillofac Implants 1997;12: Volume 26, Number 4, 2006