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Bioresorbable versus titanium space-maintaining mesh in maxillary sinus floor elevation: a split-mouth study
YIJOM-3657; No of Pages 10
Int. J. Oral Maxillofac. Surg. 2017; xxx: xxx–xxx http://dx.doi.org/10.1016/j.ijom.2017.04.001, available online at http://www.sciencedirect.com
Clinical Paper Pre-Implant Surgery
Bioresorbable versus titanium space-maintaining mesh in maxillary sinus floor elevation: a split-mouth study
M. Ahmed1, A. Abu Shama1, R. M. Hamdy2, M. Ezz1 1
Department of Oral and Maxillofacial Surgery, Faculty of Oral and Dental Medicine, Cairo University, Cairo, Egypt; 2Department of Oral and Maxillofacial Radiology, Faculty of Oral and Dental Medicine, Cairo University, Cairo, Egypt
M. Ahmed, A. Abu Shama, R.M. Hamdy, M. Ezz: Bioresorbable versus titanium spacemaintaining mesh in maxillary sinus floor elevation: a split-mouth study. Int. J. Oral Maxillofac. Surg. 2017; xxx: xxx–xxx. ã 2017 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved. Abstract. Maxillary sinus pneumatization limits implant placement in the edentulous posterior maxilla. Grafted sinus floor augmentation through Schneiderian membrane elevation and space obliteration with autogenous bone grafts, bone substitutes, or a combination of the two has often been used to resolve this problem. More recently, non-grafted sinus floor elevation has been established. This is based on the concept of membrane elevation and support either by tenting technique or using space-maintaining mesh. The aim of this study was to evaluate the predictability of new bone formation after sinus floor elevation using spacemaintaining mesh without graft material and to illustrate the difference between the use of bioresorbable and titanium meshes. Eight patients with bilateral sinus pneumatization were selected for implant placement in the edentulous posterior maxilla. Pneumatized sinuses were approached through the lateral window technique; these were elevated and maintained with resorbable or titanium meshes. All patients were evaluated clinically and radiographically immediately and at 6 months postoperative. At 6 months, a core bone biopsy was obtained from the planned implant position using a trephine drill, and the bone formed was examined histologically. Healing was uneventful in all patients, and radiographic, clinical, and histological evidence of new bone formation was seen in both groups. Titanium and resorbable meshes were found to be reliable and predictable as space-maintaining devices.
Implant therapy in the edentulous posterior maxilla becomes challenging in the presence of reduced maxillary bone height. Such a reduction in height may be due to maxillary sinus pneumatization. Numerous sinus augmentation techniques 0901-5027/000001+010
have been proposed to overcome this problem1. Maxillary sinus augmentation utilizing autogenous bone grafts, allografts, xenografts, or combinations of these through the lateral window approach has been the
Key words: maxillary sinus floor elevation; nongrafting technique; space-maintaining resorbable mesh; space-maintaining titanium mesh. Accepted for publication
classic technique for maxillary sinus floor elevation. This can be done either in a single stage with simultaneous implant placement, or in two stages with delayed implant placement, depending on whether the available residual alveolar ridge height
ã 2017 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Ahmed M, et al. Bioresorbable versus titanium space-maintaining mesh in maxillary sinus floor elevation: a split-mouth study, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.04.001
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is sufficient to attain primary implant stability2–4. Non-grafted sinus floor elevation is an innovative technique that aims to maintain the lifted membrane in position for a long enough time to allow stable blood clot formation during the postoperative healing stage5. The pioneering work of Lundgren et al. in 2004 showed that elevation of the Schneiderian membrane alone and its stabilization with implants resulted in new bone formation. This membrane is highly vascular and has osteogenic potential. It was found that the membrane and the antral walls together with the scaffold blood clot played an important role in the process of new bone formation. However, the results of other studies on nonsupported sinus membrane elevation have shown membrane collapse into the space created and a limited amount of bone gain, hence several attempts have been made to ensure fixed sinus membrane elevation using titanium screws, resorbable devices, hollow hydroxyapatite devices, and titanium mesh6–9 The studies by Cricchio et al.7, Johansson et al.8, Kaneko et al.9, and Atef et al.10 showed the positive effects of non-grafted sinus floor elevation with different spacemaintaining devices. Hence, the present study was performed to evaluate the predictability of new bone formation in non-grafted sinus floor elevation (assessed radiographically and histologically) and to illustrate the differences between resorbable and titanium mesh.
Materials and methods Inclusion criteria
Fig. 1. Digital panoramic radiograph obtained during preoperative screening. Materials
Stock 0.1-mm thickness dynamic microtitanium mesh (Leibinger, Stryker Co., Geneva, Switzerland) and stock 0.3-mm thickness resorbable mesh made of polydl-lactide (PDLLA) (Resorb-x; KLS Martin, Tuttlingen, Germany) were used in this study. Resorbable sonic pins, an ultrasound welder, and an Xcelsior water bath device were used for the sides treated with resorbable mesh (all from KLS Martin), and resorbable (lyophilized) collagen membranes (Biocollagen; Bioteck S.p.A., Torino, Italy) were utilized in all patients. Schilli Implantology Circle implants (SIC invent AG, Basel, Switzerland) were inserted in all patients; three types of implant drill were employed: classical, crestal, and tapping.
Preoperative preparation and radiographic examination
A thorough preoperative assessment of all patients was carried out, including historytaking and clinical and radiographic
examinations. Cone beam computed tomography (CBCT) (SCANORA 3D with AutoSwitch; Soredex, Helsinki, Finland) with exposure parameters of 85 kVp, 15 mA, and 6 cm field of view (FOV) were performed while the patient was wearing a radiographic/surgical stent for standardized measurement. The implant surgical stent was fabricated using implant sleeves seated on the ridge of the cast in the planned implant positions. Surgical procedures
First surgical stage
All patients were instructed to use povidone–iodine mouth rinse (Betadine) before the surgical procedures. All procedures were performed under maxillary nerve block anaesthesia with mepivacaine hydrochloride and 1:200,000 adrenaline solution (Scandonest 2%; Septodont, Saint-Maur-des-fosse´s, France). Bilateral maxillary sinus floor elevation using the lateral window technique was performed for each patient. A full-thickness
A split-mouth study was conducted on a consecutive series of eight patients with bilateral partial or completely edentulous posterior maxillary ridges. All selected patients had bilateral sinus pneumatization. The right side of the maxilla was allocated to the titanium mesh group and the left side to the resorbable mesh group for all patients. Patients who had undergone previous sinus surgery were excluded. Furthermore, the maxillary sinuses had to be free from any local pathological conditions. The distance between the crest of the ridge and the floor of the sinus in the areas planned for future implant placement had to be less than 3 mm. All patients were informed of the risks and benefits of the procedure, and they gave their approval to participate and written consent (Fig. 1). Fig. 2. Clinical photograph showing the first surgical stent in place. The stent was used to outline the extensions of the lateral window of the maxillary sinus using a round bur.
Please cite this article in press as: Ahmed M, et al. Bioresorbable versus titanium space-maintaining mesh in maxillary sinus floor elevation: a split-mouth study, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.04.001
YIJOM-3657; No of Pages 10
Bioresorbable vs. titanium mesh in sinus lift mucoperiosteal trapezoidal flap was reflected to expose the lateral wall of the maxilla according to the implant treatment plan and fabricated surgical stent (Fig. 2). A round diamond bur was used to outline both the inferior and superior horizontal osteotomies under copious water irrigation to carefully gain access to the Schneiderian membrane. The inferior osteotomy was approximately 3 mm from the sinus floor and the superior osteotomy was made 13–15 mm from the crest; these two osteotomies were connected by two vertical osteotomies. Once the window outline had been completed, special elevators (surgical sinus Freer elevators) were utilized to release the lateral bony window with the underlying Schneiderian membrane attached to it from the periphery of the osteotomy outline to gain a cleavage plane. It is imperative that the membrane is elevated across the sinus floor and up to the medial wall to the level of the proposed implant length (Figs. 3 and 4). A foil template was trimmed to fit into the superior boundary of the sinus space created, reaching the medial wall of the sinus (Fig. 5). For each patient, the right side was allocated to group A. Titanium mesh was cut guided by the foil template. The sharp projections of the mesh were removed and the mesh was then bent into an S-shape. The convex surface of the first curvature was positioned against the Schneiderian membrane, with the concave surface towards the sinus space created; the concave surface of the second curvature was positioned against the superior margin of the lateral window of the maxilla. The titanium mesh was fixed with a 1.5-mm microscrew to the lateral wall of the maxilla above the superior osteotomy (Figs. 6 and 7). The contralateral side of the same patient (left side) was allocated to group B. The resorbable mesh was softened in the Xcelsior water bath device, which was maintained at an operating temperature range of 70–90 C (158–194 F). The resorbable mesh was cut guided by the foil template and formed into an S-shape (Fig. 8). In order to facilitate the insertion of the resorbable mesh and at the same time guarantee wider Schneiderian membrane elevation, two V-shaped cutbacks were performed at the anterior and posterior margins of the mesh at the points where they met with the lateral bony window margins; this also eliminated the need for further enlargement of the lateral window. The mesh was then fixed to the lateral wall of the maxilla above the superior osteotomy with resorbable sonic
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Fig. 3. Clinical photograph showing the lateral window completely outlined.
Fig. 4. Clinical photograph showing complete lifting of the Schneiderian membrane up to the medial wall of the sinus with the lateral bony window attached to it.
pins (2.1 4 mm) by ultrasound (sonic welder). A resorbable (lyophilized) collagen membrane was utilized to cover the lateral window of the sinus bilaterally, and was fixed in place with titanium tacks (Fig. 9). The soft tissue flap was then readapted and
sutured using interrupted mattress sutures (3–0 resorbable Vicryl). Second surgical stage
All patients were recalled at 6 months postoperative for implant insertion. All
Fig. 5. Clinical photograph showing adaptation of a foil template to measure the superior dimension of the new sinus floor.
Please cite this article in press as: Ahmed M, et al. Bioresorbable versus titanium space-maintaining mesh in maxillary sinus floor elevation: a split-mouth study, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.04.001
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Fig. 6. The titanium mesh bent into an S-shape.
tation sites using a trephine bur (2 mm in diameter) guided by the implant surgical stent. The specimens were collected in two bottles prefilled with 10% formalin, one for the right side (titanium mesh) and one for the left side (resorbable mesh). Specific implant condensers rather than rotary surgical drills were used for the preparation of the implant osteotomy sites in order to improve bone quality and minimize bone removal. An implant with a diameter larger than the final condenser was installed to guarantee better primary stability. Finally the flap was readapted and sutured. All patients were prescribed postoperative medication and given instructions on postoperative care as described below. Postoperative care
After closure of the wound, a pressure band was applied to the surgical field for 48 h postoperatively. The patients were instructed to apply ice packs over the surgical area for 20 min every hour for 6 h immediately postoperative and to rinse their mouth with warm saline solution starting on the second day. They were also told to avoid any positive or negative pressure on the nasal cavity for the first 24 h after the surgery (e.g., nose-blowing, drinking using a straw, spitting, and breathing down).
Fig. 7. Clinical photograph showing the S-shaped titanium mesh fixed with a titanium screw to the lateral wall of the maxilla.
patients were instructed to use povidone– iodine mouth rinse (Betadine) before the surgical procedures. All procedures were performed under maxillary nerve block anaesthesia with mepivacaine hydrochlo-
ride and 1:200,000 adrenaline solution (Scandonest 2%). A crestal incision was performed followed by minimal mucoperiosteal flap elevation. Core bone biopsy specimens were obtained from all implan-
Fig. 8. The resorbable mesh after bending into an S-shape.
Postoperative radiographic assessment
CBCT scans were obtained within 1 week after surgery and also at 6 months postoperative to evaluate bone regeneration along the sinus floor. Linear measurements of alveolar bone height were made from the alveolar crest to the sinus floor at positions indicated by radiopaque markers (gutta-percha). During the follow-up period, the alveolar bone height was measured from the crest to the future sinus floor after bone regeneration, formed around the titanium and resorbable mesh. Volumetric measurements of new bone formation were calculated by measuring the difference between the sinus volume immediately postoperative and the volume at 6 months postoperative. Based on the anatomical fact that the maxillary sinus is pyramidal in shape with an almost square base oriented medially and an apex located in the zygomatic bone, the sinus volume was calculated geometrically with the following equation: volume of the maxillary sinus pyramid = base surface area 1/3 height = (anteroposterior (depth) craniocaudal (width) mediolateral (height))/3.
Please cite this article in press as: Ahmed M, et al. Bioresorbable versus titanium space-maintaining mesh in maxillary sinus floor elevation: a split-mouth study, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.04.001
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Bioresorbable vs. titanium mesh in sinus lift
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Table 1. Demographic characteristics of the study patients. Patient number
Sex
Age (years)
Number of implants
1 2 3 4 5 6 7 8
Female Female Female Male Male Male Female Female
34 53 19 38 53 32 25 28
4 4 4 4 2 3 2 2
male, and their average age was 36 years (range 19–53 years) (Table 1). Fig. 9. Clinical photograph showing the lateral window of the maxillary sinus covered with a collagen membrane and stabilized with titanium tacks. Histological and histomorphometric assessments
The bone biopsy specimens obtained were decalcified and processed according to a standardized protocol, using a combination of ethylenediaminetetraacetic acid (EDTA) and formic acid. Specimens were then embedded longitudinally in paraffin blocks and oriented sequentially for labelling to differentiate the right side from the left side. The blocks were cut into longitudinal sections 5 mm thick using a manual rotary microtome. The sections were stained with Mayer’s haematoxylin and eosin stain (H&E) for histological analysis. The histological and histomorphometric assessments were performed by an examiner who was blinded to the group allocation. The percentage area of bone trabeculae was estimated using the Leica QWin 500 image analysis system (Leica,) (Cancer institute/Cairo/Egypt). The cursor was used to outline the areas of bone trabeculae, which were then masked with a binary blue colour that could be measured by the computer. The image analyzer was calibrated automatically to convert the measurement units (pixels) produced by the image analyzer program into actual micrometer units. The percentage area of bone trabeculae was estimated in five different fields on each slide at 200 magnification. Mean and standard deviation (SD) values were calculated for each group.
presented as the mean SD. The onesample Kolmogorov–Smirnov test was used to examine the normality of data distribution. Repeated measures analysis of variance (ANOVA) was used to compare variables within each study group, and a post hoc test was performed if the ANOVA was significant. The paired samples t-test was used to compare each pair of studied variables within each study group. The independent samples t-test was used to compare variables between the two groups studied. For all tests, the result was considered statistically significant if the P-value was equal to or less than 0.05.
Results
This study included a total of eight patients with bilateral sinus pneumatization. Five were female and three were
Clinical results
A total of 16 sinuses were elevated. Bleeding occurred in one sinus, which was controlled intraoperatively. Schneiderian membrane perforation occurred in five sinuses. The early postoperative followup was uneventful, without any complications; there was no infection, dehiscence, mesh exposure, or bleeding, and only minimal tenderness at the site of surgery. The wound had healed completely after 7– 10 days when the sutures were removed. Patients were assessed clinically on a regular basis (1 day, 1 week, 2 weeks, 1 month, 3 months, and 6 months postoperatively), and none of them showed signs or symptoms of tenderness, sinusitis, or mesh exposure. All core specimens harvested from the planned implant sites showed adequate rigidity during harvesting and during retrieval from the trephine drill. A total of 25 implants were placed in the 16 elevated sinuses at the planned implant sites according to the preoperative work-up, without intraoperative complications (Fig. 10).
Statistical analysis
All data were subjected to statistical analysis. The statistical analysis was performed using SPSS version X software (IBM SPSS Statistics version X (IBM Corp., Armonk, NY, USA). Data were
Fig. 10. Radiograph of the resorbable mesh side obtained at 1 year postoperative showing the height of the regenerated bone formed at the implant sites with re-pneumatization at non-implant sites, emphasizing the mesh resorption.
Please cite this article in press as: Ahmed M, et al. Bioresorbable versus titanium space-maintaining mesh in maxillary sinus floor elevation: a split-mouth study, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.04.001
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Fig. 11. Preoperative coronal image revealing ongoing sinus pneumatization and alveolar bone resorption leaving only the cortex; no alveolar height remains. Totally radiolucent sinuses, without any suggestive features of sinusitis.
Radiographic results
Preoperatively, all patients showed severe bilateral maxillary sinus pneumatization reaching the alveolar crest. The alveolar bone was almost a cortical shell, and there was no trabecular pattern at the sites intended for implant insertion (Fig. 11). Immediately postoperative, a radiopaque shadow filling the sinus (suggesting
haematoma formation) could be seen in all cases in both groups, above and below the mesh level, with variably sized randomly distributed radiolucent shadows within the filling defects of the haematoma. A thin radiopaque line representing the buccal cortical plate of the lateral bony window (trap door) was seen in both groups. It was denser on the resorbable side than on the titanium side. The trap
door was close to the medial wall of the sinus, making a V-shaped outline with the zygomatic buttress (Fig. 12). At 6 months postoperative, bone regenerate was seen as a convex dome-shaped radiopacity in the titanium mesh group; in contrast, the radiopacity was flatter or concave in the resorbable mesh group (Figs. 13 and 14). Radiopaque islands were revealed above the titanium mesh, indicating that the formed haematoma above the titanium mesh was organized into new bony spicules. Soft tissue ingrowth was not detected at the lateral bone window. In the titanium mesh group, the original bone height was ranging from 1 mm to 2 mm (mean 1.22 0.3 mm), preoperatively. While the regenerated bone height showed elevation of the Schneiderian membrane ranging from 12.4 mm to 18.8 mm (mean 15.76 1.98 mm) immediately postoperative and ranging from 12.2 mm to 18.3 mm (mean 15.39 1.92 mm) at 6 months postoperative (Table 2). In the resorbable mesh group, the original bone height was ranging from 1 mm to 2.1 mm (mean 1.2 0.32 mm) preoperatively. Whilethe regenerated bone height
Fig. 12. Sagittal and coronal images obtained immediately postoperative showing bilateral radiopaque shadows filling the sinuses under and above the meshes and a haematoma filling the gap at the ends of the meshes. A V-shaped radiopaque outline of the trap door and the zygomatic buttress can be seen bilaterally (red arrows).
Please cite this article in press as: Ahmed M, et al. Bioresorbable versus titanium space-maintaining mesh in maxillary sinus floor elevation: a split-mouth study, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.04.001
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Bioresorbable vs. titanium mesh in sinus lift
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Fig. 13. Images obtained at 6 months postoperative in the titanium mesh group: (A) sagittal cut showing bone build up in the area planned for future implant placement, with a convex superior border (red arrow); (b) bone height.
Fig. 14. Images obtained at 6 months postoperative in the resorbable mesh group: (A) sagittal cut showing a flatter/concave outline (yellow arrows); (B) bone height. Table 2. Bone height in group A (titanium mesh); descriptive statistics. Preoperative Immediately postoperative 6 months postoperative
Minimum
Maximum
Mean SD
P-value
1 12.4 12.2
2 18.8 18.3
1.22 0.3 15.76 1.98 15.39 1.92
0.001
SD, standard deviation.
showed elevation of the Schneiderian membrane ranging from 9.5 mm to 18.9 mm (mean 14.3 3.23 mm) immediately postoperative and ranging from 9.5 mm to 19.5 mm (mean 13.88 3.52 mm) at 6 months postoperative (Table 3). There was no statistically significant difference regarding bone height,
bone volume, or percentage of filling between the two study groups (Table 4). Histological results
Clinical interpretation of the core biopsies retrieved showed that the entire core in both groups was formed of regenerated
Table 3. Bone height in group B (resorbable mesh); descriptive statistics. Preoperative Immediately postoperative 6 months postoperative SD, standard deviation.
Minimum
Maximum
Mean SD
P-value
1 9.5 9.5
2.1 18.9 19.5
1.2 0.32 14.3 3.2 13.88 3.5
0.001
bone. The core biopsy sections were stained with H&E and examined under a light microscope. In the resorbable mesh group, new vascularization was seen in the form of small capillaries and small calibre blood vessels, mostly arteriolar in nature. New cortical bone formation was evident, which was surrounded by osteoblastic rimming, and there were also large lacunae in the bone spicules. The bone trabeculae were interconnected throughout the entire length of the core, from the mucosal side to the sinus side. No inflammatory cells were seen in any of the sections. The marrow spaces were all vascular. There was no evidence of the original native bone on apical view of the core examination, i.e. the entire core did not contain any of the old haversian system and did not show coarse woven bone differentiation. Multiple osteoblastic bone cratering was observed. At the top of the bone specimen, newly formed spicules had
Please cite this article in press as: Ahmed M, et al. Bioresorbable versus titanium space-maintaining mesh in maxillary sinus floor elevation: a split-mouth study, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.04.001
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Table 4. Comparison of bone height between group A (titanium mesh) and group B (resorbable mesh).
Preoperative Immediately postoperative 6 months postoperative Amount of resorption Percentage of resorption
Group A Mean SD
Group B Mean SD
P-value
1.22 0.3 15.76 1.98 15.39 1.92 0.37 0.17 2.34 1.0
1.2 0.32 14.3 3.2 13.88 3.5 0.46 0.68 3.63 4.87
0.89 0.23 0.23 0.67 0.40
SD, standard deviation.
Table 5. Comparison of histomorphometric bone density (% of ROI) and bone volume between group A (titanium mesh) and group B (resorbable mesh) at 6 months postoperative.
Histomorphometric bone density (% of ROI) Bone volume
Group A Mean SD
Group B Mean SD
P-value
38.52 16.81%
54.36 15.94%
0.165
12,308.2 3760.39%
14,824.86 4743.755%
0.417
ROI, region of interest; SD, standard deviation.
been remodelled, and there was fibrous collagen septation and fibroblastic infiltration around most of the marrow spaces. In the titanium mesh group, the apical side of the specimen showed bone trabeculae with interconnecting rods together with interposed fibro-fatty marrow spaces, with dilated blood vessels filling the marrow cavity moving towards the sinus. Significant remodelling was seen at the edges of these bone trabeculae. Inflammatory cells were seen surrounding the newly formed bony trabeculae. The remaining results were similar to those of the resorbable mesh side. There was no statistically significant difference between the two study groups regarding the histomorphometric bone density (% of a region of interest (ROI)) at the end of the follow-up period (at 6 months postoperative) (P = 0.165). At 6 months postoperative, the average histomorphometric bone density was 38.52 16.81%. In the resorbable mesh group, The average histomorphometric bone density was 54.36 15.94%. There was no statistically significant difference in bone volume between the two study groups six months postoperatively (P = 0.417) (Table 5). Discussion
Although, sinus lifting with different grafting materials has proven successful, cumulative studies over the past two decades have shown that elevation of the Schneiderian membrane alone, with simultaneous implant placement and without the addition of bone grafting materials, i.e. the ‘tenting technique’, leads to minimal new bone formation, possibly due to
collapse of the Schneiderian membrane11– 14 . This subsequently opened the door to the new concept of non-grafting mesh to preserve the sinus floor elevation. The selection of dynamic micro-titanium mesh for one of the groups in this study was based on the excellent biocompatibility of titanium with no risk of an allergic reaction, as well as its malleability for three-dimensional adaptation yet sufficient rigidity to maintain the designed shape required (S-shape). The material can also be cut with scissors for a precision fit and is perforated to permit direct contact between the Schneiderian membrane and the coagulum space. Furthermore, the titanium construction allows for radiological identification. This is in agreement with the findings of Atef et al., who emphasized the importance of this design of titanium mesh as a space-holding device in the non-grafted sinus lift10. The material can be appropriately adapted (including careful trimming of the sharp titanium mesh edges) and is non-resorbable, which prompted the use of a resorbable mesh for comparison in the present study10. Thus resorbable mesh was chosen for the second group in this study. This mesh presents the following advantages: first, it consists of poly-DL-lactide (racemic mixture of D- and L-lactides), with the two components present in the same proportion, which results in a predictable and safe biological degradation process through hydrolysis, without any signs or symptoms of irritation, inflammation, or foreign body reactions. Second, it can be easily and flexibly adapted after heating in a water bath, and once it has cooled the material becomes rigid again, hence this
mesh can maintain a smooth S-shape after adaptation without any deformation15,16. In this study, the S-shape adaptation of both the titanium and resorbable mesh guaranteed maximum elevation of the Schneiderian membrane in relation to the level of the superior osteotomy of the lateral window, thus preserving the lateral sinus wall, and allowed the insertion of longer implants (14.5 mm). The trap door lateral bony window with elevation of the Schneiderian membrane from the floor and medial wall of the sinus was performed in all cases. This was done in order to guarantee complete support of the membrane to the level of the medial wall and to be able to identify the trap door cortical bone (above the mesh) as a radiopaque reference line in the CBCT cuts for linear measurements of the elevated membrane immediately postoperative; this was particularly important in the resorbable mesh group, as the mesh was not radiographically visible in the CBCT cuts. The incidence of perforation of the Schneiderian membrane in the present study was 31.2%. Various methods have been proposed to deal with this complication, including leaving the perforation untreated, suturing the Schneiderian membrane, and sealing the perforation with a resorbable collagen membrane. The reported incidence of perforation in the literature ranges from 10% to 60% of cases17,18. Three arteries supply the maxillary sinus, all of which are ultimate branches of the maxillary artery. The posterior superior lateral nasal artery is relatively close to the sphenopalatine artery and may anastomose with the facial or other nasal arteries. It can take an intraosseous course in the medial wall of the sinus. There is thus the theoretical potential of a significant bleeding complication during lateral approach sinus elevation surgery. Bleeding occurred in one sinus in the present study. This artery also positively increases the blood supply to the sinus space created, which enhances blood clot formation and the subsequent bone regeneration19,20. In this study, blood clot preservation with subsequent new bone regeneration under the elevated sinus floor was governed by two factors. The first was the fixed tenting of the sinus membrane, which played an important role in stabilization of the blood clot volume and subsequent bone formation. In 2005, Xu et al. found that the newly formed blood clot decreased significantly in volume during the first weeks of healing, indicating the importance of a space holder for the Schneiderian membrane to decrease its
Please cite this article in press as: Ahmed M, et al. Bioresorbable versus titanium space-maintaining mesh in maxillary sinus floor elevation: a split-mouth study, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.04.001
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Bioresorbable vs. titanium mesh in sinus lift pumping pressure11. The second factor was the coverage of the lateral window with a collagen membrane, which was not installed in the study by Atef et al.; this might explain the better bone regeneration results in the present study compared to that of Atef et al.10. This is also in agreement with the findings of Marinucci et al., who found that collagen membranes enhance the secretion of type I collagen, transforming growth factor beta 1 (TGFb1), and alkaline phosphatase, and may promote bone regeneration through their activity on osteoblasts21. Thus, it could be that the good results achieved are not only due to the mechanical shielding of the lateral sinus window against soft tissue ingrowth, but are also due to membranespecific features that support new bone formation in terms of both quality and quantity22. Neovascularization was observed on histological examination in both groups and was notable for the accompanying significant neogenesis of bone lamellae. The bone lamellae were seen filling the entire core, from the coronal end up to the depth of the sinus. These features indicate that there is an active process of bone formation and maturation. Enlow stressed that the sinus lining possesses bone remodelling capability, leading to alterations in deposition and resorption. However, the lack of osteoclastic activity seen in the bone sections in this study could be explained by the increased deposition effect of the Schneiderian membrane being more obvious at this stage of bone loading (before implant placement)23–28. The CBCT obtained immediately postoperative showed randomly distributed radiolucencies below the meshes in both groups. This was attributed to shrinkage of the blood clot formed during the first healing stage. However, at 6 months postoperative, the radiopacity upon radiographic examination of the bone regenerate in the resorbable mesh group was flatter or concave; this could be attributed to the laminar flow effect of air going in and out the sinus, thus massaging the upper surface of the regenerated bone (after complete degradation of the resorbable mesh). This was not seen in the titanium mesh group in which the regenerated bone maintained its convex dome shape throughout the follow-up period, as the rigidity of the integrated titanium/bone shielded the bone regenerate from resorption after loading by laminar flow of air. In the present study, the preoperative mean residual alveolar ridge height was 1.2 0.3 mm, and the mean regenerated
bone height at 6 months postoperative was 15.39 1.92 mm in the titanium mesh group and 13.88 3.5 mm in the resorbable mesh group; this means that the bone gain was average of 11 times in both groups. The mean volume of the regenerated bone in the current study was 38.52 16.81% in the titanium mesh group and 54.36 15.94% in the resorbable mesh group. On comparing these results with those of Thor et al.13 and Atef et al.10, the volumes measured in the present study are significantly higher. This may be attributed to the use of the collagen membrane and the fact that the preoperative mean residual alveolar ridge height in their cases was 4 mm10,13. Finally, although this study was considered a continuation of the study by Atef et al. in evaluating the non-grafted sinus lift technique, significant major changes were implemented to move this technique forward: (1) resorbable mesh was used in accordance with the trend of using biodegradable materials in the maxillofacial region, (2) the lateral window was covered with a resorbable collagen membrane with the aim of enhancing the quality of the regenerated bone, (3) cases with a nearly totally resorbed alveolar ridge were selected so that the core biopsy retrieved actually represented total bone regenerate (no native bone), reflecting the predictability of this technique, and (4) the mesh was fashioned into an S-shape to ensure maximum ridge gain at the centre of the ridge for subsequent implant placement and at the same time the dimensions of the lateral bony window were minimized. However, questions have been raised concerning the need for long-term follow-up of the regenerated bone in cases in which resorbable mesh has been used, as after the complete degradation of the resorbable mesh, this bone will be exposed to the laminar flow effect of air going in and out of the sinus thus massaging the upper surface of the regenerated bone (similar to the ebbing and tide forming waves on the water surface). This phenomenon will not occur in the titanium mesh group, in which there is fixed tenting. The findings of this study showed that the non-grafted sinus lift technique using space-maintaining mesh is a reliable method for maxillary sinus augmentation. The resorbable and titanium meshes were comparable as space-maintaining devices in the non-grafted sinus lifting technique regarding tenting and bone formation. There is a need for long-term follow-up of the resorbable mesh group to evaluate the maintenance of the regenerated bone.
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Funding
This study was self-funded. There are no financial relationships between the authors and any manufacturer/supplier of any commercial products or services related to this work. Competing interests
The authors declare that they have no significant competing financial, professional, or personal interests that might have influenced the performance or presentation of the work described in this manuscript. Ethical approval
All patients were selected from the outpatient clinic of the Department of Oral and Maxillofacial Surgery, Faculty of Oral and Dental Medicine, Cairo University. The present study was approved by the Ethics Committee of the Faculty of Oral and Dental Medicine, Cairo University. Patient consent
Written consent was obtained from all patients for the use of their clinical photographs as a scientific demonstration in this paper. References 1. Altintas N, Senel F, Kayıpmaz S, Taskesen F, Pampu AA. Comparative radiologic analyses of newly formed bone after maxillary sinus augmentation with and without bone grafting. J Oral Maxillofac Surg 2013;71: 1520–30. 2. Wood RM, Moore DL. Grafting of the maxillary sinus with intraorally harvested autogenous bone prior to implant placement. Int J Oral Maxillofac Implants 1988;3:209–14. 3. Riben C, Thor A. The maxillary sinus membrane elevation procedure: augmentation of bone around dental implants without grafts—a review of a surgical technique. Int J Dent 2012;2012:105483. 4. Smiler D. The sinus lift graft: basic technique and variations. Pract Periodontics Aesthet Dent 1997;9:885–93. 5. Palma VC, Magro-Filho O, Oliveria D, Ame´rico J, Lundgren S, Salata LA, Sennerby L. Bone reformation and implant integration following maxillary sinus membrane elevation: an experimental study in primates. Clin Implant Dent Relat Res 2006;8:11–24. 6. Lundgren S, Anderson S, Gualini F, Sennerby L. Bone reformation with sinus membrane elevation: a new surgical technique for maxillary sinus floor augmentation. Clin Implant Dent Relat Res 2004;6:165–73.
Please cite this article in press as: Ahmed M, et al. Bioresorbable versus titanium space-maintaining mesh in maxillary sinus floor elevation: a split-mouth study, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.04.001
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7. Cricchio G, Palma VC, Faria PE, de Olivera JA, Lundgren S, Sennerby L, Salata LA. Histological outcomes on the development of new space-making devices for maxillary sinus floor augmentation. Clin Implant Dent Relat Res 2011;13:224–30. ˚ ., Isaksson S, Adolfsson E, 8. Johansson L.A Lindh C, Sennerby L. Bone regeneration using a hollow hydroxyapatite space- maintaining device for maxillary sinus floor augmentation–a clinical pilot study. Clin Implant Dent Relat Res 2012;14:575–84. 9. Kaneko T, Masuda I, Horie N, Shimoyama T. New bone formation in nongrafted sinus lifting with space maintaining management: a novel technique using a titanium bone fixation device. J Oral Maxillofac Surg 2012;70:e217–24. 10. Atef M, Hakam MM, ElFaramawey MI, Abou-ElFetouh A, Ekram M. Nongrafted sinus floor elevation with a space-maintaining titanium mesh: case-series study on four patients. Clin Implant Dent Relat Res 2014;16:893–903. 11. Xu H, Shimizu Y, Ooya K. Histomorphometric study of the stability of newly formed bone after elevation of the floor of the maxillary sinus. Br J Oral Maxillofac Surg 2005;43:493–9. 12. Chen TW, Chang HS, Leung KW, Lai YL, Kao SY. Implant placement immediately after the lateral approach of the trap door window procedure to create a maxillary sinus lift without bone grafting: a 2-year retrospective evaluation of 47 implants in 33 patients. J Oral Maxillofac Surg 2007; 65:2324–8. 13. Thor A, Sennerby L, Hirsch JM, Rasmusson L. Bone formation at the maxillary sinus floor following simultaneous elevation of the mucosal lining and implant installation without graft material: an evaluation of 20 patients treated with 44 Astra Tech implants. J Oral Maxillofac Surg 2007;65:64–72.
14. Lin IC, Gonzalez AM, Chang HJ, Kao SY, Chen TW. A 5-year follow-up of 80 implants in 44 patients placed immediately after the lateral trap-door window procedure to accomplish maxillary sinus elevation without bone grafting. Int J Oral Maxillofac Implants 2011;26:1079–86. 15. Cutright DE, Hunsuck E, Beasley J. Fracture reduction using a biodegradable material, polylactic acid. J Oral Surg 1971;29:393–7. 16. Rozema F, Levendag P, Bos R, Boering G, Pennings A. Influence of resorbable poly (Llactide) bone plates and screws on the dose distributions of radiotherapy beams. Int J Oral Maxillofac Surg 1990;19:374–6. 17. Vlassis JM, Fugazzotto PA. A classification system for sinus membrane perforations during augmentation procedures with options for repair. J Periodontol 1999;70:692–9. 18. Stammberger H. Endoscopic endonasal surgery—concepts in treatment of recurring rhinosinusitis. Part II. Surgical technique. Otolaryngol Head Neck Surg 1986;94: 147–56. 19. Solar P, Geyerhofer U, Traxler H, Windisch A, Ulm C, Watzek G. Blood supply to the maxillary sinus relevant to sinus floor elevation procedures. Clin Oral Implants Res 1999;10:34–44. 20. Hatano N, Sennerby L, Lundgren S. Maxillary sinus augmentation using sinus membrane elevation and peripheral venous blood for implant-supported rehabilitation of the atrophic posterior maxilla: case series. Clin Implant Dent Relat Res 2007;9:150–5. 21. Marinucci L, Lilli C, Baroni T, Becchetti E, Belcastro S, Balducci C, Locci P. In vetro comparsion of bioresorbable and nonresorbable membranes in bone regeneration. J Periodontol 2001;72:753–9. 22. Dahlin C, Linde A, Gottlow J, Nyman S. Healing of bone defects by guided tissue regeneration. Plast Reconstr Surg 1988;81: 672–6.
23. Balloni S, Calvi EM, Damiani F, Bistoni G, Calvitti M, Locci P, Becchetti E, Marinucci L. Effects of titanium surface roughness on mesenchymal stem cell commitment and differentiation signaling. Int J Oral Maxillofac Implants 2009;24:627–35. 24. Srouji S, Kizhner T, David DB, Riminucci M, Bianco P, Livne E. The Schneiderian membrane contains osteoprogenitor cells: in vivo and in vitro study. Calcif Tissue Int 2009;84:138–45. 25. Pjetursson BE, Tan WC, Zwahlen M, Lang NP. A systematic review of the success of sinus floor elevation and survival of implants inserted in combination with sinus floor elevation. J Clin Periodontol 2008;35(8 Suppl):216–40. 26. Ellegaard B, Kølsen-Petersen J, Baelum V. Implant therapy involving maxillary sinus lift in periodontally compromised patients. Clin Oral Implants Res 1997;8:305–15. 27. Cricchio G, Sennerby L, Lundgren S. Sinus bone formation and implant survival after sinus membrane elevation and implant placement: a 1- to 6-year follow-up study. Clin Oral Implants Res 2011;22:1200–12. 28. Enlow D. Facial growth. Third edition. Philadelphia, PA: W.B. Saunders Company; 1990: 115–50.
Address: Mamdouh Ahmed Department of Oral and Maxillofacial Surgery Faculty of Oral and Dental Medicine Cairo University 3 Asem Abd El Hameed Street Nagaty Serg – 8th District Nasr City Cairo Egypt Tel.: +20 2 01222173262; 01067987111 E-mails: [email protected], [email protected]
Please cite this article in press as: Ahmed M, et al. Bioresorbable versus titanium space-maintaining mesh in maxillary sinus floor elevation: a split-mouth study, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.04.001
Int. J. Oral Maxillofac. Surg. 2017; xxx: xxx–xxx http://dx.doi.org/10.1016/j.ijom.2017.04.001, available online at http://www.sciencedirect.com
Clinical Paper Pre-Implant Surgery
Bioresorbable versus titanium space-maintaining mesh in maxillary sinus floor elevation: a split-mouth study
M. Ahmed1, A. Abu Shama1, R. M. Hamdy2, M. Ezz1 1
Department of Oral and Maxillofacial Surgery, Faculty of Oral and Dental Medicine, Cairo University, Cairo, Egypt; 2Department of Oral and Maxillofacial Radiology, Faculty of Oral and Dental Medicine, Cairo University, Cairo, Egypt
M. Ahmed, A. Abu Shama, R.M. Hamdy, M. Ezz: Bioresorbable versus titanium spacemaintaining mesh in maxillary sinus floor elevation: a split-mouth study. Int. J. Oral Maxillofac. Surg. 2017; xxx: xxx–xxx. ã 2017 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved. Abstract. Maxillary sinus pneumatization limits implant placement in the edentulous posterior maxilla. Grafted sinus floor augmentation through Schneiderian membrane elevation and space obliteration with autogenous bone grafts, bone substitutes, or a combination of the two has often been used to resolve this problem. More recently, non-grafted sinus floor elevation has been established. This is based on the concept of membrane elevation and support either by tenting technique or using space-maintaining mesh. The aim of this study was to evaluate the predictability of new bone formation after sinus floor elevation using spacemaintaining mesh without graft material and to illustrate the difference between the use of bioresorbable and titanium meshes. Eight patients with bilateral sinus pneumatization were selected for implant placement in the edentulous posterior maxilla. Pneumatized sinuses were approached through the lateral window technique; these were elevated and maintained with resorbable or titanium meshes. All patients were evaluated clinically and radiographically immediately and at 6 months postoperative. At 6 months, a core bone biopsy was obtained from the planned implant position using a trephine drill, and the bone formed was examined histologically. Healing was uneventful in all patients, and radiographic, clinical, and histological evidence of new bone formation was seen in both groups. Titanium and resorbable meshes were found to be reliable and predictable as space-maintaining devices.
Implant therapy in the edentulous posterior maxilla becomes challenging in the presence of reduced maxillary bone height. Such a reduction in height may be due to maxillary sinus pneumatization. Numerous sinus augmentation techniques 0901-5027/000001+010
have been proposed to overcome this problem1. Maxillary sinus augmentation utilizing autogenous bone grafts, allografts, xenografts, or combinations of these through the lateral window approach has been the
Key words: maxillary sinus floor elevation; nongrafting technique; space-maintaining resorbable mesh; space-maintaining titanium mesh. Accepted for publication
classic technique for maxillary sinus floor elevation. This can be done either in a single stage with simultaneous implant placement, or in two stages with delayed implant placement, depending on whether the available residual alveolar ridge height
ã 2017 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
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is sufficient to attain primary implant stability2–4. Non-grafted sinus floor elevation is an innovative technique that aims to maintain the lifted membrane in position for a long enough time to allow stable blood clot formation during the postoperative healing stage5. The pioneering work of Lundgren et al. in 2004 showed that elevation of the Schneiderian membrane alone and its stabilization with implants resulted in new bone formation. This membrane is highly vascular and has osteogenic potential. It was found that the membrane and the antral walls together with the scaffold blood clot played an important role in the process of new bone formation. However, the results of other studies on nonsupported sinus membrane elevation have shown membrane collapse into the space created and a limited amount of bone gain, hence several attempts have been made to ensure fixed sinus membrane elevation using titanium screws, resorbable devices, hollow hydroxyapatite devices, and titanium mesh6–9 The studies by Cricchio et al.7, Johansson et al.8, Kaneko et al.9, and Atef et al.10 showed the positive effects of non-grafted sinus floor elevation with different spacemaintaining devices. Hence, the present study was performed to evaluate the predictability of new bone formation in non-grafted sinus floor elevation (assessed radiographically and histologically) and to illustrate the differences between resorbable and titanium mesh.
Materials and methods Inclusion criteria
Fig. 1. Digital panoramic radiograph obtained during preoperative screening. Materials
Stock 0.1-mm thickness dynamic microtitanium mesh (Leibinger, Stryker Co., Geneva, Switzerland) and stock 0.3-mm thickness resorbable mesh made of polydl-lactide (PDLLA) (Resorb-x; KLS Martin, Tuttlingen, Germany) were used in this study. Resorbable sonic pins, an ultrasound welder, and an Xcelsior water bath device were used for the sides treated with resorbable mesh (all from KLS Martin), and resorbable (lyophilized) collagen membranes (Biocollagen; Bioteck S.p.A., Torino, Italy) were utilized in all patients. Schilli Implantology Circle implants (SIC invent AG, Basel, Switzerland) were inserted in all patients; three types of implant drill were employed: classical, crestal, and tapping.
Preoperative preparation and radiographic examination
A thorough preoperative assessment of all patients was carried out, including historytaking and clinical and radiographic
examinations. Cone beam computed tomography (CBCT) (SCANORA 3D with AutoSwitch; Soredex, Helsinki, Finland) with exposure parameters of 85 kVp, 15 mA, and 6 cm field of view (FOV) were performed while the patient was wearing a radiographic/surgical stent for standardized measurement. The implant surgical stent was fabricated using implant sleeves seated on the ridge of the cast in the planned implant positions. Surgical procedures
First surgical stage
All patients were instructed to use povidone–iodine mouth rinse (Betadine) before the surgical procedures. All procedures were performed under maxillary nerve block anaesthesia with mepivacaine hydrochloride and 1:200,000 adrenaline solution (Scandonest 2%; Septodont, Saint-Maur-des-fosse´s, France). Bilateral maxillary sinus floor elevation using the lateral window technique was performed for each patient. A full-thickness
A split-mouth study was conducted on a consecutive series of eight patients with bilateral partial or completely edentulous posterior maxillary ridges. All selected patients had bilateral sinus pneumatization. The right side of the maxilla was allocated to the titanium mesh group and the left side to the resorbable mesh group for all patients. Patients who had undergone previous sinus surgery were excluded. Furthermore, the maxillary sinuses had to be free from any local pathological conditions. The distance between the crest of the ridge and the floor of the sinus in the areas planned for future implant placement had to be less than 3 mm. All patients were informed of the risks and benefits of the procedure, and they gave their approval to participate and written consent (Fig. 1). Fig. 2. Clinical photograph showing the first surgical stent in place. The stent was used to outline the extensions of the lateral window of the maxillary sinus using a round bur.
Please cite this article in press as: Ahmed M, et al. Bioresorbable versus titanium space-maintaining mesh in maxillary sinus floor elevation: a split-mouth study, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.04.001
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Bioresorbable vs. titanium mesh in sinus lift mucoperiosteal trapezoidal flap was reflected to expose the lateral wall of the maxilla according to the implant treatment plan and fabricated surgical stent (Fig. 2). A round diamond bur was used to outline both the inferior and superior horizontal osteotomies under copious water irrigation to carefully gain access to the Schneiderian membrane. The inferior osteotomy was approximately 3 mm from the sinus floor and the superior osteotomy was made 13–15 mm from the crest; these two osteotomies were connected by two vertical osteotomies. Once the window outline had been completed, special elevators (surgical sinus Freer elevators) were utilized to release the lateral bony window with the underlying Schneiderian membrane attached to it from the periphery of the osteotomy outline to gain a cleavage plane. It is imperative that the membrane is elevated across the sinus floor and up to the medial wall to the level of the proposed implant length (Figs. 3 and 4). A foil template was trimmed to fit into the superior boundary of the sinus space created, reaching the medial wall of the sinus (Fig. 5). For each patient, the right side was allocated to group A. Titanium mesh was cut guided by the foil template. The sharp projections of the mesh were removed and the mesh was then bent into an S-shape. The convex surface of the first curvature was positioned against the Schneiderian membrane, with the concave surface towards the sinus space created; the concave surface of the second curvature was positioned against the superior margin of the lateral window of the maxilla. The titanium mesh was fixed with a 1.5-mm microscrew to the lateral wall of the maxilla above the superior osteotomy (Figs. 6 and 7). The contralateral side of the same patient (left side) was allocated to group B. The resorbable mesh was softened in the Xcelsior water bath device, which was maintained at an operating temperature range of 70–90 C (158–194 F). The resorbable mesh was cut guided by the foil template and formed into an S-shape (Fig. 8). In order to facilitate the insertion of the resorbable mesh and at the same time guarantee wider Schneiderian membrane elevation, two V-shaped cutbacks were performed at the anterior and posterior margins of the mesh at the points where they met with the lateral bony window margins; this also eliminated the need for further enlargement of the lateral window. The mesh was then fixed to the lateral wall of the maxilla above the superior osteotomy with resorbable sonic
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Fig. 3. Clinical photograph showing the lateral window completely outlined.
Fig. 4. Clinical photograph showing complete lifting of the Schneiderian membrane up to the medial wall of the sinus with the lateral bony window attached to it.
pins (2.1 4 mm) by ultrasound (sonic welder). A resorbable (lyophilized) collagen membrane was utilized to cover the lateral window of the sinus bilaterally, and was fixed in place with titanium tacks (Fig. 9). The soft tissue flap was then readapted and
sutured using interrupted mattress sutures (3–0 resorbable Vicryl). Second surgical stage
All patients were recalled at 6 months postoperative for implant insertion. All
Fig. 5. Clinical photograph showing adaptation of a foil template to measure the superior dimension of the new sinus floor.
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Fig. 6. The titanium mesh bent into an S-shape.
tation sites using a trephine bur (2 mm in diameter) guided by the implant surgical stent. The specimens were collected in two bottles prefilled with 10% formalin, one for the right side (titanium mesh) and one for the left side (resorbable mesh). Specific implant condensers rather than rotary surgical drills were used for the preparation of the implant osteotomy sites in order to improve bone quality and minimize bone removal. An implant with a diameter larger than the final condenser was installed to guarantee better primary stability. Finally the flap was readapted and sutured. All patients were prescribed postoperative medication and given instructions on postoperative care as described below. Postoperative care
After closure of the wound, a pressure band was applied to the surgical field for 48 h postoperatively. The patients were instructed to apply ice packs over the surgical area for 20 min every hour for 6 h immediately postoperative and to rinse their mouth with warm saline solution starting on the second day. They were also told to avoid any positive or negative pressure on the nasal cavity for the first 24 h after the surgery (e.g., nose-blowing, drinking using a straw, spitting, and breathing down).
Fig. 7. Clinical photograph showing the S-shaped titanium mesh fixed with a titanium screw to the lateral wall of the maxilla.
patients were instructed to use povidone– iodine mouth rinse (Betadine) before the surgical procedures. All procedures were performed under maxillary nerve block anaesthesia with mepivacaine hydrochlo-
ride and 1:200,000 adrenaline solution (Scandonest 2%). A crestal incision was performed followed by minimal mucoperiosteal flap elevation. Core bone biopsy specimens were obtained from all implan-
Fig. 8. The resorbable mesh after bending into an S-shape.
Postoperative radiographic assessment
CBCT scans were obtained within 1 week after surgery and also at 6 months postoperative to evaluate bone regeneration along the sinus floor. Linear measurements of alveolar bone height were made from the alveolar crest to the sinus floor at positions indicated by radiopaque markers (gutta-percha). During the follow-up period, the alveolar bone height was measured from the crest to the future sinus floor after bone regeneration, formed around the titanium and resorbable mesh. Volumetric measurements of new bone formation were calculated by measuring the difference between the sinus volume immediately postoperative and the volume at 6 months postoperative. Based on the anatomical fact that the maxillary sinus is pyramidal in shape with an almost square base oriented medially and an apex located in the zygomatic bone, the sinus volume was calculated geometrically with the following equation: volume of the maxillary sinus pyramid = base surface area 1/3 height = (anteroposterior (depth) craniocaudal (width) mediolateral (height))/3.
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Table 1. Demographic characteristics of the study patients. Patient number
Sex
Age (years)
Number of implants
1 2 3 4 5 6 7 8
Female Female Female Male Male Male Female Female
34 53 19 38 53 32 25 28
4 4 4 4 2 3 2 2
male, and their average age was 36 years (range 19–53 years) (Table 1). Fig. 9. Clinical photograph showing the lateral window of the maxillary sinus covered with a collagen membrane and stabilized with titanium tacks. Histological and histomorphometric assessments
The bone biopsy specimens obtained were decalcified and processed according to a standardized protocol, using a combination of ethylenediaminetetraacetic acid (EDTA) and formic acid. Specimens were then embedded longitudinally in paraffin blocks and oriented sequentially for labelling to differentiate the right side from the left side. The blocks were cut into longitudinal sections 5 mm thick using a manual rotary microtome. The sections were stained with Mayer’s haematoxylin and eosin stain (H&E) for histological analysis. The histological and histomorphometric assessments were performed by an examiner who was blinded to the group allocation. The percentage area of bone trabeculae was estimated using the Leica QWin 500 image analysis system (Leica,) (Cancer institute/Cairo/Egypt). The cursor was used to outline the areas of bone trabeculae, which were then masked with a binary blue colour that could be measured by the computer. The image analyzer was calibrated automatically to convert the measurement units (pixels) produced by the image analyzer program into actual micrometer units. The percentage area of bone trabeculae was estimated in five different fields on each slide at 200 magnification. Mean and standard deviation (SD) values were calculated for each group.
presented as the mean SD. The onesample Kolmogorov–Smirnov test was used to examine the normality of data distribution. Repeated measures analysis of variance (ANOVA) was used to compare variables within each study group, and a post hoc test was performed if the ANOVA was significant. The paired samples t-test was used to compare each pair of studied variables within each study group. The independent samples t-test was used to compare variables between the two groups studied. For all tests, the result was considered statistically significant if the P-value was equal to or less than 0.05.
Results
This study included a total of eight patients with bilateral sinus pneumatization. Five were female and three were
Clinical results
A total of 16 sinuses were elevated. Bleeding occurred in one sinus, which was controlled intraoperatively. Schneiderian membrane perforation occurred in five sinuses. The early postoperative followup was uneventful, without any complications; there was no infection, dehiscence, mesh exposure, or bleeding, and only minimal tenderness at the site of surgery. The wound had healed completely after 7– 10 days when the sutures were removed. Patients were assessed clinically on a regular basis (1 day, 1 week, 2 weeks, 1 month, 3 months, and 6 months postoperatively), and none of them showed signs or symptoms of tenderness, sinusitis, or mesh exposure. All core specimens harvested from the planned implant sites showed adequate rigidity during harvesting and during retrieval from the trephine drill. A total of 25 implants were placed in the 16 elevated sinuses at the planned implant sites according to the preoperative work-up, without intraoperative complications (Fig. 10).
Statistical analysis
All data were subjected to statistical analysis. The statistical analysis was performed using SPSS version X software (IBM SPSS Statistics version X (IBM Corp., Armonk, NY, USA). Data were
Fig. 10. Radiograph of the resorbable mesh side obtained at 1 year postoperative showing the height of the regenerated bone formed at the implant sites with re-pneumatization at non-implant sites, emphasizing the mesh resorption.
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Fig. 11. Preoperative coronal image revealing ongoing sinus pneumatization and alveolar bone resorption leaving only the cortex; no alveolar height remains. Totally radiolucent sinuses, without any suggestive features of sinusitis.
Radiographic results
Preoperatively, all patients showed severe bilateral maxillary sinus pneumatization reaching the alveolar crest. The alveolar bone was almost a cortical shell, and there was no trabecular pattern at the sites intended for implant insertion (Fig. 11). Immediately postoperative, a radiopaque shadow filling the sinus (suggesting
haematoma formation) could be seen in all cases in both groups, above and below the mesh level, with variably sized randomly distributed radiolucent shadows within the filling defects of the haematoma. A thin radiopaque line representing the buccal cortical plate of the lateral bony window (trap door) was seen in both groups. It was denser on the resorbable side than on the titanium side. The trap
door was close to the medial wall of the sinus, making a V-shaped outline with the zygomatic buttress (Fig. 12). At 6 months postoperative, bone regenerate was seen as a convex dome-shaped radiopacity in the titanium mesh group; in contrast, the radiopacity was flatter or concave in the resorbable mesh group (Figs. 13 and 14). Radiopaque islands were revealed above the titanium mesh, indicating that the formed haematoma above the titanium mesh was organized into new bony spicules. Soft tissue ingrowth was not detected at the lateral bone window. In the titanium mesh group, the original bone height was ranging from 1 mm to 2 mm (mean 1.22 0.3 mm), preoperatively. While the regenerated bone height showed elevation of the Schneiderian membrane ranging from 12.4 mm to 18.8 mm (mean 15.76 1.98 mm) immediately postoperative and ranging from 12.2 mm to 18.3 mm (mean 15.39 1.92 mm) at 6 months postoperative (Table 2). In the resorbable mesh group, the original bone height was ranging from 1 mm to 2.1 mm (mean 1.2 0.32 mm) preoperatively. Whilethe regenerated bone height
Fig. 12. Sagittal and coronal images obtained immediately postoperative showing bilateral radiopaque shadows filling the sinuses under and above the meshes and a haematoma filling the gap at the ends of the meshes. A V-shaped radiopaque outline of the trap door and the zygomatic buttress can be seen bilaterally (red arrows).
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Fig. 13. Images obtained at 6 months postoperative in the titanium mesh group: (A) sagittal cut showing bone build up in the area planned for future implant placement, with a convex superior border (red arrow); (b) bone height.
Fig. 14. Images obtained at 6 months postoperative in the resorbable mesh group: (A) sagittal cut showing a flatter/concave outline (yellow arrows); (B) bone height. Table 2. Bone height in group A (titanium mesh); descriptive statistics. Preoperative Immediately postoperative 6 months postoperative
Minimum
Maximum
Mean SD
P-value
1 12.4 12.2
2 18.8 18.3
1.22 0.3 15.76 1.98 15.39 1.92
0.001
SD, standard deviation.
showed elevation of the Schneiderian membrane ranging from 9.5 mm to 18.9 mm (mean 14.3 3.23 mm) immediately postoperative and ranging from 9.5 mm to 19.5 mm (mean 13.88 3.52 mm) at 6 months postoperative (Table 3). There was no statistically significant difference regarding bone height,
bone volume, or percentage of filling between the two study groups (Table 4). Histological results
Clinical interpretation of the core biopsies retrieved showed that the entire core in both groups was formed of regenerated
Table 3. Bone height in group B (resorbable mesh); descriptive statistics. Preoperative Immediately postoperative 6 months postoperative SD, standard deviation.
Minimum
Maximum
Mean SD
P-value
1 9.5 9.5
2.1 18.9 19.5
1.2 0.32 14.3 3.2 13.88 3.5
0.001
bone. The core biopsy sections were stained with H&E and examined under a light microscope. In the resorbable mesh group, new vascularization was seen in the form of small capillaries and small calibre blood vessels, mostly arteriolar in nature. New cortical bone formation was evident, which was surrounded by osteoblastic rimming, and there were also large lacunae in the bone spicules. The bone trabeculae were interconnected throughout the entire length of the core, from the mucosal side to the sinus side. No inflammatory cells were seen in any of the sections. The marrow spaces were all vascular. There was no evidence of the original native bone on apical view of the core examination, i.e. the entire core did not contain any of the old haversian system and did not show coarse woven bone differentiation. Multiple osteoblastic bone cratering was observed. At the top of the bone specimen, newly formed spicules had
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Ahmed et al.
Table 4. Comparison of bone height between group A (titanium mesh) and group B (resorbable mesh).
Preoperative Immediately postoperative 6 months postoperative Amount of resorption Percentage of resorption
Group A Mean SD
Group B Mean SD
P-value
1.22 0.3 15.76 1.98 15.39 1.92 0.37 0.17 2.34 1.0
1.2 0.32 14.3 3.2 13.88 3.5 0.46 0.68 3.63 4.87
0.89 0.23 0.23 0.67 0.40
SD, standard deviation.
Table 5. Comparison of histomorphometric bone density (% of ROI) and bone volume between group A (titanium mesh) and group B (resorbable mesh) at 6 months postoperative.
Histomorphometric bone density (% of ROI) Bone volume
Group A Mean SD
Group B Mean SD
P-value
38.52 16.81%
54.36 15.94%
0.165
12,308.2 3760.39%
14,824.86 4743.755%
0.417
ROI, region of interest; SD, standard deviation.
been remodelled, and there was fibrous collagen septation and fibroblastic infiltration around most of the marrow spaces. In the titanium mesh group, the apical side of the specimen showed bone trabeculae with interconnecting rods together with interposed fibro-fatty marrow spaces, with dilated blood vessels filling the marrow cavity moving towards the sinus. Significant remodelling was seen at the edges of these bone trabeculae. Inflammatory cells were seen surrounding the newly formed bony trabeculae. The remaining results were similar to those of the resorbable mesh side. There was no statistically significant difference between the two study groups regarding the histomorphometric bone density (% of a region of interest (ROI)) at the end of the follow-up period (at 6 months postoperative) (P = 0.165). At 6 months postoperative, the average histomorphometric bone density was 38.52 16.81%. In the resorbable mesh group, The average histomorphometric bone density was 54.36 15.94%. There was no statistically significant difference in bone volume between the two study groups six months postoperatively (P = 0.417) (Table 5). Discussion
Although, sinus lifting with different grafting materials has proven successful, cumulative studies over the past two decades have shown that elevation of the Schneiderian membrane alone, with simultaneous implant placement and without the addition of bone grafting materials, i.e. the ‘tenting technique’, leads to minimal new bone formation, possibly due to
collapse of the Schneiderian membrane11– 14 . This subsequently opened the door to the new concept of non-grafting mesh to preserve the sinus floor elevation. The selection of dynamic micro-titanium mesh for one of the groups in this study was based on the excellent biocompatibility of titanium with no risk of an allergic reaction, as well as its malleability for three-dimensional adaptation yet sufficient rigidity to maintain the designed shape required (S-shape). The material can also be cut with scissors for a precision fit and is perforated to permit direct contact between the Schneiderian membrane and the coagulum space. Furthermore, the titanium construction allows for radiological identification. This is in agreement with the findings of Atef et al., who emphasized the importance of this design of titanium mesh as a space-holding device in the non-grafted sinus lift10. The material can be appropriately adapted (including careful trimming of the sharp titanium mesh edges) and is non-resorbable, which prompted the use of a resorbable mesh for comparison in the present study10. Thus resorbable mesh was chosen for the second group in this study. This mesh presents the following advantages: first, it consists of poly-DL-lactide (racemic mixture of D- and L-lactides), with the two components present in the same proportion, which results in a predictable and safe biological degradation process through hydrolysis, without any signs or symptoms of irritation, inflammation, or foreign body reactions. Second, it can be easily and flexibly adapted after heating in a water bath, and once it has cooled the material becomes rigid again, hence this
mesh can maintain a smooth S-shape after adaptation without any deformation15,16. In this study, the S-shape adaptation of both the titanium and resorbable mesh guaranteed maximum elevation of the Schneiderian membrane in relation to the level of the superior osteotomy of the lateral window, thus preserving the lateral sinus wall, and allowed the insertion of longer implants (14.5 mm). The trap door lateral bony window with elevation of the Schneiderian membrane from the floor and medial wall of the sinus was performed in all cases. This was done in order to guarantee complete support of the membrane to the level of the medial wall and to be able to identify the trap door cortical bone (above the mesh) as a radiopaque reference line in the CBCT cuts for linear measurements of the elevated membrane immediately postoperative; this was particularly important in the resorbable mesh group, as the mesh was not radiographically visible in the CBCT cuts. The incidence of perforation of the Schneiderian membrane in the present study was 31.2%. Various methods have been proposed to deal with this complication, including leaving the perforation untreated, suturing the Schneiderian membrane, and sealing the perforation with a resorbable collagen membrane. The reported incidence of perforation in the literature ranges from 10% to 60% of cases17,18. Three arteries supply the maxillary sinus, all of which are ultimate branches of the maxillary artery. The posterior superior lateral nasal artery is relatively close to the sphenopalatine artery and may anastomose with the facial or other nasal arteries. It can take an intraosseous course in the medial wall of the sinus. There is thus the theoretical potential of a significant bleeding complication during lateral approach sinus elevation surgery. Bleeding occurred in one sinus in the present study. This artery also positively increases the blood supply to the sinus space created, which enhances blood clot formation and the subsequent bone regeneration19,20. In this study, blood clot preservation with subsequent new bone regeneration under the elevated sinus floor was governed by two factors. The first was the fixed tenting of the sinus membrane, which played an important role in stabilization of the blood clot volume and subsequent bone formation. In 2005, Xu et al. found that the newly formed blood clot decreased significantly in volume during the first weeks of healing, indicating the importance of a space holder for the Schneiderian membrane to decrease its
Please cite this article in press as: Ahmed M, et al. Bioresorbable versus titanium space-maintaining mesh in maxillary sinus floor elevation: a split-mouth study, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.04.001
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Bioresorbable vs. titanium mesh in sinus lift pumping pressure11. The second factor was the coverage of the lateral window with a collagen membrane, which was not installed in the study by Atef et al.; this might explain the better bone regeneration results in the present study compared to that of Atef et al.10. This is also in agreement with the findings of Marinucci et al., who found that collagen membranes enhance the secretion of type I collagen, transforming growth factor beta 1 (TGFb1), and alkaline phosphatase, and may promote bone regeneration through their activity on osteoblasts21. Thus, it could be that the good results achieved are not only due to the mechanical shielding of the lateral sinus window against soft tissue ingrowth, but are also due to membranespecific features that support new bone formation in terms of both quality and quantity22. Neovascularization was observed on histological examination in both groups and was notable for the accompanying significant neogenesis of bone lamellae. The bone lamellae were seen filling the entire core, from the coronal end up to the depth of the sinus. These features indicate that there is an active process of bone formation and maturation. Enlow stressed that the sinus lining possesses bone remodelling capability, leading to alterations in deposition and resorption. However, the lack of osteoclastic activity seen in the bone sections in this study could be explained by the increased deposition effect of the Schneiderian membrane being more obvious at this stage of bone loading (before implant placement)23–28. The CBCT obtained immediately postoperative showed randomly distributed radiolucencies below the meshes in both groups. This was attributed to shrinkage of the blood clot formed during the first healing stage. However, at 6 months postoperative, the radiopacity upon radiographic examination of the bone regenerate in the resorbable mesh group was flatter or concave; this could be attributed to the laminar flow effect of air going in and out the sinus, thus massaging the upper surface of the regenerated bone (after complete degradation of the resorbable mesh). This was not seen in the titanium mesh group in which the regenerated bone maintained its convex dome shape throughout the follow-up period, as the rigidity of the integrated titanium/bone shielded the bone regenerate from resorption after loading by laminar flow of air. In the present study, the preoperative mean residual alveolar ridge height was 1.2 0.3 mm, and the mean regenerated
bone height at 6 months postoperative was 15.39 1.92 mm in the titanium mesh group and 13.88 3.5 mm in the resorbable mesh group; this means that the bone gain was average of 11 times in both groups. The mean volume of the regenerated bone in the current study was 38.52 16.81% in the titanium mesh group and 54.36 15.94% in the resorbable mesh group. On comparing these results with those of Thor et al.13 and Atef et al.10, the volumes measured in the present study are significantly higher. This may be attributed to the use of the collagen membrane and the fact that the preoperative mean residual alveolar ridge height in their cases was 4 mm10,13. Finally, although this study was considered a continuation of the study by Atef et al. in evaluating the non-grafted sinus lift technique, significant major changes were implemented to move this technique forward: (1) resorbable mesh was used in accordance with the trend of using biodegradable materials in the maxillofacial region, (2) the lateral window was covered with a resorbable collagen membrane with the aim of enhancing the quality of the regenerated bone, (3) cases with a nearly totally resorbed alveolar ridge were selected so that the core biopsy retrieved actually represented total bone regenerate (no native bone), reflecting the predictability of this technique, and (4) the mesh was fashioned into an S-shape to ensure maximum ridge gain at the centre of the ridge for subsequent implant placement and at the same time the dimensions of the lateral bony window were minimized. However, questions have been raised concerning the need for long-term follow-up of the regenerated bone in cases in which resorbable mesh has been used, as after the complete degradation of the resorbable mesh, this bone will be exposed to the laminar flow effect of air going in and out of the sinus thus massaging the upper surface of the regenerated bone (similar to the ebbing and tide forming waves on the water surface). This phenomenon will not occur in the titanium mesh group, in which there is fixed tenting. The findings of this study showed that the non-grafted sinus lift technique using space-maintaining mesh is a reliable method for maxillary sinus augmentation. The resorbable and titanium meshes were comparable as space-maintaining devices in the non-grafted sinus lifting technique regarding tenting and bone formation. There is a need for long-term follow-up of the resorbable mesh group to evaluate the maintenance of the regenerated bone.
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Funding
This study was self-funded. There are no financial relationships between the authors and any manufacturer/supplier of any commercial products or services related to this work. Competing interests
The authors declare that they have no significant competing financial, professional, or personal interests that might have influenced the performance or presentation of the work described in this manuscript. Ethical approval
All patients were selected from the outpatient clinic of the Department of Oral and Maxillofacial Surgery, Faculty of Oral and Dental Medicine, Cairo University. The present study was approved by the Ethics Committee of the Faculty of Oral and Dental Medicine, Cairo University. Patient consent
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Address: Mamdouh Ahmed Department of Oral and Maxillofacial Surgery Faculty of Oral and Dental Medicine Cairo University 3 Asem Abd El Hameed Street Nagaty Serg – 8th District Nasr City Cairo Egypt Tel.: +20 2 01222173262; 01067987111 E-mails: [email protected], [email protected]
Please cite this article in press as: Ahmed M, et al. Bioresorbable versus titanium space-maintaining mesh in maxillary sinus floor elevation: a split-mouth study, Int J Oral Maxillofac Surg (2017), http://dx.doi.org/10.1016/j.ijom.2017.04.001