|Year : 2012 | Volume
| Issue : 2 | Page : 235-240
Alveolar ridge augmentation using chin bone graft, bovine bone mineral, and titanium mesh: Clinical, histological, and histomorphomtric study
Jihad Khamees1, Mohammad Atef Darwiche2, Nabil Kochaji3
1 Department of Periodontology, Dental School, University of Damascus, Damascus, Syria
2 Department of Periodontology, Former Dean of Dental School, University of Damascus, Damascus, Syria
3 Department of Histology and Pathology, Dental School, University of Damascus, Damascus, Syria
|Date of Submission||23-Aug-2010|
|Date of Acceptance||28-Nov-2011|
|Date of Web Publication||1-Aug-2012|
Department of Periodontology, Dental School, University of Damascus, Damascus
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Background: Resorption of the alveolar ridge often leaves insufficient bone volume. Very few studies have investigated the quantity and quality of bone formation in humans, following alveolar ridge augmentation, using autogenous bone and bovine bone mineral (BBM) under titanium mesh. Materials and Methods: Sixteen alveolar bone defects divided into two groups; control group with symphyseal autogenous bone covered by titanium mesh; and test group with symphyseal autogenous bone mixed with BBM in 1: 1 ratio and covered by titanium mesh. The outcomes were evaluated clinically, histologically, and histomorphometrically. Results: Clinical measurements showed that the horizontal bone gain was 3.44±0.54 mm and 2.88±0.57 mm, on average, for control group and test group, respectively. While graft absorption was 2.66±0.98 mm (43.62%) and 1.67±1.00 mm (36.65%), on average, for control group and test group, respectively. In the test group, BBM particles were still recognizable, on histologic analysis. They were surrounded completely or partly by newly formed bone. Clear signs of resorption of the BBM were found, with osteoclast cell noticed in the area. Histomorphometrically, the newly formed bone was 78.40%±13.97% and 65.58%±6.59%, whereas connective tissue constituted 21.60%±13.97% and 23.87%±4.79% for control group and test group, respectively. The remaining BBM particles occupied 10.55%±1.80%. All differences between the control and test groups were not significant (P>.05). Conclusion: This investigation suggests that horizonal ridge augmentation with titanium mesh and autogenous bone alone or mixed with BBM are predictable and ridges were augmented even if mesh exposure occurs.
Keywords: Alveolar ridge augmentation, bovine bone, chin bone graft, histomorphometry, titanium mesh
|How to cite this article:|
Khamees J, Darwiche MA, Kochaji N. Alveolar ridge augmentation using chin bone graft, bovine bone mineral, and titanium mesh: Clinical, histological, and histomorphomtric study. J Indian Soc Periodontol 2012;16:235-40
|How to cite this URL:|
Khamees J, Darwiche MA, Kochaji N. Alveolar ridge augmentation using chin bone graft, bovine bone mineral, and titanium mesh: Clinical, histological, and histomorphomtric study. J Indian Soc Periodontol [serial online] 2012 [cited 2019 Aug 22];16:235-40. Available from: http://www.jisponline.com/text.asp?2012/16/2/235/99268
| Introduction|| |
Resorption of the alveolar ridge often leaves insufficient bone volume for the placement of dental implants. Several surgical techniques have been used to augment the bone volume, including bone grafts taken from intraoral or extraoral sites,  guided bone regeneration with bioabsorbable  or non-resorbable membrane,  and alveolar distraction osteogenesis.  In 1996, von Arx et al, introduced titanium micromesh for reconstructive implant surgery and reported positive results for the staged approach (ridge augmentation performed before implant placement)  and the simultaneous procedure (implant placement and ridge augmentation performed at the same time).  Recent clinical studies ,, confirmed the reliability of this technique with different types of grafts: intraoral or extraoral autogenous bone or a mix of autogenous bone and bovine bone mineral (BBM). Very few studies ,, have investigated the quantity and quality of bone formation in humans, following alveolar ridge augmentation, using titanium micromesh and these biomaterials.
The use of barriers made of titanium micro-mesh in combination with bone grafts and bone substitutes has been proposed and tested for the partial and full augmentation of the alveolar process in implant surgery. ,, Although the use of autogenous bone beneath the titanium meshes is advised, , because of its intrinsic osteogenetic properties and a more rapid course of bone regeneration, situations exist in which autogenous bone grafts are not feasible, or patients refuse to have bone harvested from extraoral sources. The combination of an osteoconductive scaffold with autogenous bone harvested intraorally would allow the surgeon to reduce the quantity of bone grafts necessary, enhance graft conservation over time, treat patients under local anesthesia, and decrease postoperative morbidity. Among the available bone substitutes, BBM has been successfully used to correct bone defects adjacent to implants as well as in sinus lift and alveolar ridge-augmentation procedures. ,, Maiorana et al,  clinically and histologically demonstrated, for the first time, the efficacy of using a titanium mesh for alveolar ridge augmentation with a mixture of autogenous extraorally harvested bone and bovine bone mineral in humans. All, but one of the 59 implants placed in the grafted bone achieved osseointegration within five months after placement. A recent comparative histologic study  in humans with regard to bone formation showed that similar results can be obtained using a combination of autogenous bone and bovine bone mineral or autogenous bone alone under titanium meshes.
Questions remain as to whether there is an advantage in using autogenous bone alone compared to a mixture of bone substitute with autogenous bone under a titanium mesh, to reduce the bone harvested. Therefore, the purpose of the present study was to evaluate the quantity and quality of newly regenerated bone; clinically, histologically, and histomorphometrically, by means of direct clinical measuring, and biopsies of alveolar ridges augmented by autogenous bone alone versus a combination of autogenous bone (50%) and BBM (50%) with titanium micromesh in the anterior maxillae.
| Materials and Methods|| |
Sixteen alveolar bone defects in 13 consecutive partially edentulous patients (11 men and 2 women), with a mean age of 28.19±11.39 years (range, 13 to 55 years) were selected for the study [Table 1] and [Table 2]. We divided the participants into two groups; control group with autogenous bone-harvested from mandibular symphysis- only applied and covered with titanium mesh¶ ; and test group with autogenous bone- harvested from mandibular symphysis- applied mixed with bovine bone mineral # in 1: 1 ratio and covered with titanium mesh. Patients were seen at the Department of Periodontology, Damascus University. The main inclusion criterion was the presence of at least one atrophic edentulous area (Class IV -V), according to the Cawood and Howell classification,  with an insufficient amount of residual bone (<5.5 mm in width) to place one to two implants in the correct prosthetic position in the maxilla. In addition, patients had to agree to participate in a postoperative control program, and a signed informed consent form approved by the Department of Periodontology of the University of Damascus was obtained in accordance with the Helsinki Declaration on human experimentation. The exclusion criteria were as follows:
- local infections;
- uncontrolled diabetes (glycosylated hemoglobin level >7 mg%);
- a history of radiation therapy in the head or neck region;
- current antitumor chemotherapy;
- liver, blood, or kidney disease;
- current corticosteroid use;
- inflammatory and autoimmune diseases of the oral cavity; and
- poor oral hygiene and motivation.
After a medical history interview and clinical examination in preparation for treatment planning, all patients received a session of prophylaxis. Preoperative evaluation was performed at baseline and included a study cast, periapical radiographs, and panoramic radiograph.
Individual stent and clinical measurements
An acrylic individual stent was made for each patient to be used for clinical measurements. The body of stent was placed on the palatal teeth surfaces, with an extension raised over the alveolar ridge defect towards the buccal vestibule with sufficient space between the defect and the inner side of the extension to achieve a free stent-graft contact [Figure 1]. The stent is then perforated opposite to the ridge defect in three levels; at the top, middle, and base of the ridge defect. Clinical measurements were gotten using endodontic file#35 with its determinant. After stent takes its place, the file is inserted in each hole to penetrate soft tissue until it sticks to the ridge bone, and the determinant sticks to stent [Figure 1]. So, the working length of the file equals the measurement. We repeated this measurement technique three times; before applying the graft, immediately after grafting, and six months after grafting. The subtraction between third measurement and first measurement gives the increasing amount of the alveolar ridge, while the subtraction between third measurement and second measurement gives the amount of graft absorption.
|Figure 1: The individual stent and endodontic file used in performing the clinical measurement|
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The surgical procedures were performed under local anesthesia only or local anesthesia with oral sedation. The patients were premedicated one hour, preoperatively, with ampicillin 1g (IV). They were asked to rinse with 0.12% chlorhexidine for one minute twice a day, two days before the surgery. Surgical access was through a mid-crestal incision, maximizing the keratinized mucosa on each side of the incision, and an intrasulcular buccal incision at the adjacent teeth including vestibular divergent-releasing incisions. Full-thickness flaps were reflected to expose the alveolar bone.
All fibrous tissue was removed from the recipient site, and perforations into the marrow space were produced using surgical burs to improve vascularization and incorporation of the graft. In all cases, the donor site was the mandibular symphysis [Figure 2]a. The bone graft was harvested, using a trephine bur #5** [Figure 2]b, in the form of small cylindrical blocks [Figure 2]c, and then particulated [Figure 2]d using a bone miller.
|Figure 2: The autogenous chin bone harvested from the symphisis by trephine bur and then particulated using a bone miller|
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The autogenous bone particles were applied alone or mixed with anorganic bovine bone mineral (BBM) in a 1:1 mixture by volume. A titanium mesh was trimmed and fixed in position with two or more titanium microscrews ** in the buccal and palatal portion of the native bone to maintain and protect the particulate bone in situ. Then the graft was covered by performing release periosteal incisions to extend the flap over the mesh as far coronally as required. Sutures were used to obtain tension-free closure of the soft tissues and to adapt the incision line. The postoperative regimen included ampicillin 1 g every 12 hours for 7 days, ibuprofen, 400 mg every 8 hours for 4 to 5 days, and 0.12% chlorhexidine mouthrinses every 12 hours for 1 week. The patients were instructed to avoid brushing and trauma to the surgical site, and to avoid smoking for a few days, post-surgery. Sutures were removed after 15 days. Patients were seen on one, three, and six months after the reconstructive procedure, to plan for implant surgery.
At this time, after reflecting labial and palatal full-thickness flaps [Figure 3]b, the titanium screws and mesh were removed [Figure 3]c, and using the individual stent, direct clinical measurements were taken. Before threading the implant osteotomy sites, histological specimens were obtained using a trephine bur#2** [Figure 3]c. Specimens were preserved in a formol solution for histological and histomorphometric analyses.
|Figure 3: (a) Deficient ridge (b) Six months post-augmentation, some new bone deposited on the titanium mesh (c) Removing the mesh, and trephine bur used for getting specimen for the histological analysis (d) Two inserted implants in the augmented ridge|
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The bone specimens were fixed in 10% buffered formaldehyde, deminerlization was achieved using nitric acid 14% for 48 hours, then samples dehydrated in a graded alcohol series (24 hours each in 50%, 75%, 95%, and 100% alcohol), and embedded in paraffin wax. The blocks were sectioned along the major axis of the sample using a microtome yielding sections 5 ΅m thick. The sections were stained with hematoxilin-iozine stain, and finally, they were analyzed using a light microscope. For the bone histological analysis, the following points were detected: type of bone found, signs of active remodeling, and inflammatory and foreign body reaction.
Histomorphometric analysis was performed on three consecutive sections under an optical microscope using software¶¶ for image analysis. For the histomorphometric analysis, the following values were measured: total bone volume (TBV), soft tissue volume (STV), and residual BBM volume (RBV). The measurements were expressed as percentages of the total sample area.
The data distribution was plotted using box plots and characterized by the mean±SD. The t-test was used for two sample comparisons (control group versus test group). The level of statistical significance was set at P≤0.05.
| Results|| |
In all cases, patients did not complain about significant side effects at the donor site. Postoperative discomforts included swelling, ecchymosis, and pain for the first week, and did not require specific additional treatment. In four sites, the titanium mesh completely exposed one to two months, postoperatively, and then it was removed. The other sites healed successfully, and from a clinical point of view, the bucco-lingual dimension of the augmented alveolar ridges followed the mesh configuration, enabling good placement of dental implants.
Clinical measurements taken by the individual stent showed that the horizontal bone gain in the ridge width was 3.44±0.54 mm, on average, for the control group, and 2.88±0.57 mm, on average, for the test group, while the amount of graft absorption was 2.66±0.98 mm (43.62%), on average, for the control group, and 1.67±1.00 mm (36.65%), on average, for the test group. The differences in the horizontal bone gain and amount of graft absorption between the control and test groups were not significant (P=0.84)
In specimens taken from the control group, the newly formed bone consisted mainly of mature lamellar bone. No signs of inflammatory infiltrate, necrosis, or foreign body reaction were observed in any of the specimens.
In the specimens taken from the test group, BBM particles were still recognizable on histologic analysis, although they were surrounded completely or partly by newly formed bone, without any connective tissue between the particles and bone [Figure 4]c. Clear signs of resorption of the material were found [Figure 4]a. Osteoclast cells were noticed in the area [Figure 4]b, without signs of inflammatory reaction, and mass of woven bone detected adjacent to lamellar bone and BBM particles [Figure 4]d.
|Figure 4: (a) Absorption gaps in a BBM particle (b) Osteoclast cells (c) BBM particles completely embedded in new formed bone (d) Mass of woven bone adjacent to lamellar bone and BBM particles|
Click here to view
For the sites augmented only with particulate autologous bone (control group), the amount of newly formed bone was 78.40%±13.97%, whereas connective tissue constituted 21.60%±13.97% of the entire area. For the sites augmented with equal mixture of autologous bone and BBM (test group), the amount of new bone was 65.58%±6.59%, the soft tissue was 23.87%±4.79%, and the remaining 10.55%±1.80% was filled with BBM particles. The difference in new bone formation between the control and test groups was not significant (P=0.89).
| Discussion|| |
This paper reports alveolar ridge augmentation of 16 severely atrophied alveolar ridges, by means of titanium mesh with autogenous bone alone or mixed with BBM. The excellent biocompatibility of titanium and the easy handling of the titanium micromesh allowed their application for three-dimensional reconstruction of alveolar bone defects. The importance of bone quality in horizontally (and vertically when needed) augmented sites is particularly important because of the limited amount of residual native bone available for implant osseointegration.  The results observed here show that autogenous bone alone and a combination of autogenous bone (50%) and BBM (50%) could be used successfully for ridge augmentation with titanium mesh in reconstructive pre-implant surgery.
The pre- and post-augmentation clinical measurements demonstrated significant bone regeneration, with a mean horizontal augmentation of 3.44±0.54 mm for control group and 2.88±0.57 mm for test group. These results are comparable to those reported in other studies; Pieri et al,  used pre- and post-augmentation computed tomography (CT) scan measurements demonstrating significant bone regeneration, with a mean horizontal augmentation of 3.71±1.24 mm. Authors referred to that high cost and risk for radiation exposure with this method limits its routine application. Matsui et al,  evaluated the combined of autografts and titanium meshes in a series of 15 patients with cleft lip-palate, and reported a mean increased bone width of 4.6 mm. Proussaefs and Lozada  reported a mean horizontal augmentation 3.82±1.47 mm, using titanium meshes and a 50:50 combination of autogenous bone and BBM in 17 consecutive patients.
Corinaldesi et al,  mentioned that during mesh removal at the time of implant insertion, a layer of connective tissue, ''pseudoperiosteum,'' was observed consistently under the mesh. For our study this is true for all patients of the specimen except two patients who manifested bone deposited on the titanium mesh passing through its gaps [Figure 5]c.
|Figure 5: (a) Alveolar bone defect (b) Six months post-augmentation, lingual softtissue dehiscence occurred (c) Buccally, new bone deposited on the titanium mesh (d) Local graft absorption took place under the dehiscence and replaced by soft tissue|
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It must be noted, in fact, that 50% of specimen developed a soft-tissue dehiscence [Figure 5]b during the healing period, local graft absorption took place under the dehiscence and replaced by soft tissue [Figure 5]d. All alveolar bone defects-except the four failed sites- were successfully repaired, and the success of the grafting procedure was not affected by titanium mesh exposure, what agree with Louis et al,  who mentioned that although titanium mesh exposure rate was 51.11%, the success of bone grafting was not affected, and the success rate in their study was 97.72%. Considering that Maiorana et al, Roccuzzo et al,  and Corinaldesi  reported less rate of mesh exposure, while Eising et al,  -in an experimental study in dogs- reported dehiscence occurred in 22 of 32 experimental sites. Seven of these twenty two dehisced sites showed increased ridge width.
Most likely, the used 0.2 mm mesh thickness gave the flap sufficient retention to prevent dehiscence in the rest of cases. The question of whether titanium mesh may offer sufficient support for a 'safe' use of provisional prosthesis is still open.  So, the provisional prosthesis should be supported by the adjacent teeth. Autogenous bone from chin was reported to present minimal discomfort for the patients. This is in accordance with Hunt and Jovanovic  and D'Addona and Nowzari.  However, more morbidity of chin bone harvesting was mentioned by Nkenke et al,  Raghoebar et al,  and Roccuzzo et al. 
Histologically, the absence of inflammatory signs around the xenogenic particles suggested that bovine bone graft material is safe and biocompatible. Moreover, the histomorphometric analysis revealed that almost the same predictable response was obtained at control sites and test sites, with total bone volume (TBV) of 78.40% and 65.58%, respectively. Obviously, the TBV in the test group should be smaller compared to that in the control group because part of the defect space is filled with BBM particles. When the RBV is added to the calculation, similar total values were obtained for both groups. These results demonstrated that BBM particles represent a valid clinical alternative to autogenous bone and could partially replace it in alveolar bone augmentations with titanium mesh. Further studies could attempt to evaluate if good bone formation can be obtained under titanium micromesh with a higher proportion of BBM. Meijndert  applied three augmentation techniques (chinbone with or without a resorbable membrane and BBM with a resorbable membrane). Clinically and radiographically, he did not find significant differences in the treatment outcomes of the three augmentation modalities.
The TBV found here was higher than that reported by Proussaefs et al,  and Corinaldesi et al,  for seven patients, Proussaefs et al,  performed alveolar bone augmentation procedures using titanium mesh and a mixture of intraorally harvested intramembranous bone graft and BBM applied as a composite graft. The histomorphometric measurements showed that the specimen area was occupied by new bone (36.4%±9.05%), fibrous tissue (51.6%±7.89%), and BBM (12.0%±6.71%). An explanation may account for this quantitative difference; the type of bone graft used for alveolar bone augmentation differed: we used a 50:50 mixture of autogenous bone and BBM, whereas the composition of the mixture was not specified in their study. Corinaldesi et al applied autogenous bone alone and a 70:30 mixture of autologous bone and bovine bone mineral in 18 patients. For the sites augmented only with particulate autologous bone the amount newly formed bone was 62.38%, and for the sites augmented with a mixture of autologous bone and BBM, the amount of new bone was 52.88%, and the residual BBM volume was 17.15%.
In our study, the histologic analysis clearly showed that after six months of healing, the newly regenerated bone consisted mainly of lamellar bone with a regular architecture that was almost indistinguishable from the pre-existing bone. These results concur with those of other studies, [29,30] with longer healing time using titanium-reinforced non-resorbable membranes. In our histologic examination, in specimens with BBM particles present, the granules were well integrated in the regenerated bone, and a mass of woven bone was observed mass of woven bone adjacent to lamellar bone and BBM particles adjacent to lamellar bone and BBM particles. On the surface of the BBM particles, signs of resorption were observed six months after grafting as many holes were digged in the body of the particle. The literature differs on the resorption of BBM material after grafting. Meijndert et al,  found no osteoclastic activity six months after bone grafting in the anterior maxilla in humans, and Corinaldesi et al,  were unable to demonstrate the presence of resorption lacunae or osteoclasts, while in our study, obvious signs of BBM absorption were clearly observed, as we could see many absorption gaps in the single particle [Figure 4]a. Additionally, osteoclast cells were detected in the area to sign that active remodeling was taking place [Figure 4]b.
Another study  evaluated the histology of an implant retrieved from sinus augmentation after four years showed that BBM particles seemed to undergo very slow active resorption. These observations agreed with a histologic analysis performed by Fugazzotto,  in which BBM appeared to be resorbed progressively during a 12- to 13-month period after guided bone regeneration procedures in humans, being almost completely replaced by newly formed bone. Similar to Corinaldesi et al, study,  our study showed new bone deposition between the granules, which were in tight contact with the surrounding bone without signs of inflammation. Moreover, we detected most of BBM particles completely embedded in newly formed bone [Figure 4]c. This indicated that the material was osteoconductive and acted as a natural scaffold for new bone formation. This finding is in accord with the description of Maiorana et al, who reported that the BBM particles were surrounded and interconnected by newly formed bone; they continued to undergo remodeling and apposition of more ordered lamellar bone.
According to other studies, [32,33] it can be assumed that once the grafted BBM particles have been embedded in mineralized bone, and as long as no special stimuli occur, the xenograft acts similarly to the host bone, which often undergoes remodeling process at a very slow rate.
| Conclusion|| |
Results of this clinical investigation suggest that horizonal ridge augmentation with titanium mesh and autogenous bone or autogenous bone mixed with bovine bone mineral are predictable and do not go through major resorption, and ridges were augmented even if mesh exposure occurs. Implants can be inserted six months following surgical placement of the autograft.
¶ Normed Company, Germany
# Bio-Oss, Geistlich Pharmaceutical, Wolhusen, Switzerland.
** Medicon Company, Germany.
¶¶ PhotoshopCS2, Microsoft Corporation,USA
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2]