Maxillary sinus floor augmentation procedures

Transcription

1 New Bone Formation Following Sinus Membrane Elevation Without Bone Grafting: Histologic Findings in Humans Jae-Jin Ahn, DDS, MS, PhD 1 /Sung-Am Cho, DDS, MS, PhD 2 /Gerard Byrne, DDS 3 / Jae-Hyun Kim, DDS, MS 4 /Hong-In Shin, DDS, PhD 5 Purpose: To determine whether sinus membrane elevation alone can lead to new bone formation on the maxillary sinus floor. Materials and Methods: Among patients who were to receive implant treatment, those who had 4 to 5 mm of bone height in the maxillary sinus floor (as measured radiographically) were selected as candidates for sinus membrane elevation. The lateral sinus wall was exposed through a buccal mucoperiosteal incision. The sinus membrane was elevated through a bone window, and the space underneath the membrane was filled with absorbable collagen sponge (Collaplug). In the presence of blood in the space, the collagen sponge was left to soak up the blood; in the deficiency of blood, the sponge was saturated with venous blood drawn from the brachial vein. The mucoperiosteal flap was repositioned and closed with interrupted silk sutures. The sinus was left to heal for 6 months. Core specimens of the maxillary sinus floor were obtained using a trephine bur at 6 months after sinus elevation in patients treated between January 2006 and June The trephined sites were used for implant placement. The biopsy specimens were analyzed histologically to identify the presence and amount of new bone tissue. Results: Thirteen specimens from eight patients were included in the study. Microscopically, 11 specimens exhibited no recognizable new bone tissue. Two specimens exhibited a small amount of woven bone on the surface of the sinus floor. Conclusion: Within the limits of this study of eight patients, little to no new bone formation was observed on the maxillary sinus floor at 6 months following sinus membrane elevation and support with blood-soaked collagen sponges. Int J Oral Maxillofac Implants 2011;26:83 90 Key words: bone formation, bone graft, lateral window, maxillary sinus, membrane elevation, sinus floor augmentation 1 Affiliate Professor, School of Dentistry, Kyungpook National University, Daegu, South Korea; Private Practice, Daegu, South Korea. 2 Professor, Department of Prosthodotics, School of Dentistry, Kyungpook National University, Daegu, South Korea. 3 Associate Professor, Adult Restorative Dentistry Department, College of Dentistry, University of Nebraska Medical Center, Lincoln, Nebraska. 4 Chief, Department of Dentistry, Fatima Hospital, Daegu, South Korea. 5 Professor and Chief, Institute for Hard Tissue and Bio-tooth Regeneration, Department of Oral Pathology, School of Dentistry, Kyungpook National University, Daegu, South Korea. Correspondence to: Dr Jae-Jin Ahn, 109-1, Daebong-dong, Jung-gu, Daegu, , South Korea. Fax: ahn@drahn.asia Maxillary sinus floor augmentation procedures have been used successfully to increase bone volume in the posterior maxilla for the placement of dental implants. 1,2 In 1980, Boyne and James 3 reported a case of maxillary sinus floor augmentation with autogenous bone grafting through the lateral approach membrane elevation procedure; since then, many modifications of the technique have been reported. 4 6 Generally, the use of autogenous bone in the sinus floor has been regarded as a gold standard, but this requires an additional procedure to harvest the bone, with increased morbidity. 7 9 To overcome such problems, synthetic bone substitutes have been used as an osteoconductive scaffold material The International Journal of Oral & Maxillofacial Implants 83

2 Several recent studies showed that sinus membrane elevation and simultaneous insertion of titanium implants without any grafting material resulted in new bone formation on the sinus floor Lundgren et al 13 suggested that there is great potential for healing and bone formation in the maxillary sinus. Palma et al 14 observed the osteogenic potential of the sinus membrane in an animal study. Several studies have suggested that a prerequisite to sinus elevation without bone grafting is to use a dental implant as a space-maintaining device. However, two cases of spontaneous bone formation on the maxillary sinus floor have been reported after removal of a cyst and an impacted tooth, respectively. 19,20 The aforementioned studies imply that sinus floor augmentation is achievable without bone grafting, but the precise mechanism of new bone formation is still unclear When the residual bone volume or bone density at a site is too low to gain primary stability for an implant, a two-stage approach is preferably selected. The current authors planned two-stage operations for implant integration without bone grafting in a clinical study. Stage-one surgery was carried out to obtain a secluded space filled with blood clot between the elevated sinus membrane and the sinus floor, because such coagulum space was expected to develop into bone tissue, as indicated by the concept of guided tissue regeneration. 13,19,20 After 6 months, biopsy specimens were retrieved from the sinus floor prior to implant placement. The purpose of this study was to verify the likelihood of new bone formation through histologic analysis following sinus membrane elevation without bone grafting. MATERIALS AND METHODS The study protocol was approved by the Kyungpook National University Hospital ethics review committee, and written informed consent was obtained from all subjects. The selection of patients was based on radiographic and computed tomographic (CT) studies. Inclusion criteria were as follows: 1. A need for implant treatment in the posterior maxilla 2. Insufficient residual bone height (from alveolar crest to sinus floor), ie, 4 to 5 mm as measured on a radiograph of the planned implant placement site 3. No clinical and radiographic signs of sinus disease Core specimens of the maxillary sinus floor were obtained 6 months after sinus membrane elevation in patients treated between January 2006 and June Surgical Procedure A horizontal incision was made on the buccal alveolar mucosa of the treatment-planned area, and a mucoperiosteal flap was reflected to expose the lateral sinus wall. An oval bone window was made in the lateral sinus wall with a round bur, with care taken to avoid perforation of the sinus membrane. The bone window was kept attached to the underlying membrane during the procedure. The sinus membrane was elevated about 15 mm above the sinus floor using curved sinus curettes until the medial wall was clearly visible. After the sinus membrane was elevated, the space between the membrane and the floor was filled with five to eight bovine-origin absorbable collagen sponges (Collaplug, Zimmer Dental). The collagen sponges were left to soak up blood spontaneously in the sinus cavity. If the blood from the sinus did not fill the sponges sufficiently, venous blood was drawn from the patient s brachial vein and injected into the sponges to be saturated. Then the bone window was covered with collagen membranes (Collatape, Zimmer Dental). The buccal mucoperiosteal flap was repositioned and closed with interrupted silk sutures. Oral amoxicillin was administered 1 hour before surgery and three times per day for 3 days after the surgery. Sutures were removed on the seventh postoperative day. Harvesting of Specimens Six months after the sinus elevation, specimens were harvested simultaneously with implant placement surgery. The same buccal mucosal incision that had been made 6 months previously was used again, and the mucoperiosteal flap was reflected. Then the lateral sinus wall was reexposed. In most cases on this second exposure, the diameter of the bone window was much narrower than the initial one because of bone regeneration along the periphery of the window. Therefore, the bone window was widened with a Kerrison sinus bone rongeur to introduce sinus elevation curettes. The removed bone was particulated (approximately 1 mm in diameter) and kept in saline to be used as autogenous grafting material. Additional bone was collected from the tuberosity region to provide a total of approximately 0.2 ml of particulate bone graft per osteotomy site. The sinus membrane was elevated for a second time in the same way as the first elevation. A trephine bur ( mm) was used to obtain a biopsy core from the site where implant placement was planned. Through a crestal approach, the revolving trephine bur was inserted into the alveolar ridge, and it passed through and penetrated above the sinus floor bone while the sinus membrane was protected with a periosteal elevator. 84 Volume 26, Number 1, 2011

3 Table 1 Patient Data and Summary of Biopsy Results Patient Biopsy site(s) Sex Age (y) Residual bone height (mm) on radiograph Histologic evidence of new bone 1 L second premolar, first molar M , 4.5 No 2 R first molar F Yes 3 L second premolar F Yes 4 R second premolar M No 5 L second premolar, first molar, second molar M , 4.5, 5.0 No 6 R first molar M No 7 R second premolar, first molar M , 4.5 No 8 R second premolar, first molar F , 4.5 No Fig 1a Preoperative CT of patient 1. Sinus elevation was performed in the left second premolar area. Fig 1b Histologic sample at 6 months after sinus membrane elevation. There was no recognizable new bone formation on the surface of the sinus floor bone plate (H&E; original magnification 20). a b 1 mm Then the trephined site was prepared for implant placement. Implant sites were developed using convexend osteotomes sequentially (3.25 to 4.5 mm in diameter). The osteotome was gently pushed upward with hand pressure so that its tip protruded 3 to 5 mm beyond the floor. The bone around the periphery of the osteotomy site was elevated by 2 to 3 mm with osteotomes. Then the sinus membrane was returned to the sinus floor. Transcrestally, the collected autogenous bone graft was placed into the osteotomy site with a spoon grafting instrument. The bone particles were pushed up over the sinus floor and collected beneath the membrane using a graft packer. Then a tapered implant (8 mm long, 4.1 mm in apical diameter, and 4.7 mm in collar diameter) was placed in the prepared osteotomy site. The buccal mucoperiosteal flap was repositioned and closed with interrupted silk sutures. Histologic Preparation of Specimens All the biopsy specimens were fixed in 10% buffered formalin and demineralized in 10% ethylenediaminetetraacetic acid solution. A hematoxylin and eosin (H&E) stained 7-µm-thick longitudinal section representing the central part of each core specimen was made for histologic examination. The histologic sections were examined using a light microscope (Olympus BX51), and photographs were taken using an installed camera. RESULTS Thirteen specimens from eight patients (five men and three women) aged 30 to 65 years (mean 52.2) were included in the study (Table 1). The mean residual bone height on radiographs was 4.6 mm. Every patient underwent a unilateral sinus surgery. Biopsy specimens were obtained from six maxillary premolar regions and seven maxillary molar regions. Small membrane perforations occurred in two patients, but no membrane closure was attempted. The perforations were covered with collagen membranes. Postoperative healing was uneventful in all patients. Upon reentry to the sinuses, the lateral windows were smaller and the membranes were thicker than during the initial surgeries. Elevation of the membrane the second time was somewhat easier than the first time because the membrane had thickened. Fibrous adhesion between the membrane and the sinus floor bone was not found. After a 5-month healing period for implant integration, all the implants, which were placed immediately after harvesting of specimens, were verified to be clinically stable. Abutment connections were carried out at 35 Ncm of torque, and all sites were successfully restored (three single-unit restorations and five multiple-unit fixed prostheses). The International Journal of Oral & Maxillofacial Implants 85

4 a c Fig 2a CT image of patient 2. Arrow indicates the lateral sinus window that was created during the sinus membrane elevation. Fig 2b Tissue specimen at 6 months after sinus membrane elevation. Active new bone formation was not apparent on the sinus floor bone (H&E; original magnification 20). b Fig 2c Higher magnification of the inset from Fig 2b. A small amount of newly formed woven bone (arrow) is apparent on the surface of the sinus floor bone (H&E; original magnification 100). Microscopically, 11 specimens exhibited no recognizable active osteoid or new bone tissue on the surface of the sinus floor bone at 6 months after membrane elevation (Fig 1). Two specimens exhibited a small amount of newly formed bone on the surface of the sinus floor bone in patients 2 and 3 (Figs 2 and 3, Table 1). In patient 2, only a few layers of osteoblasts were found in the limited area of the bone surface (Fig 2c). The specimen from patient 3 showed horizontally arranged trabeculae of woven bone and osteoid, which had been growing on the preexisting sinus floor bone. The amount of new bone tissue was as much as 0.5 mm in vertical height (Fig 3g). The alveolar crestal bone was generally thick and irregular, whereas sinus floor bone plates showed a thin and smooth surface in most sites. Generally, the trabeculae within medullary spaces showed sparse arrangement with no active bone metabolism, and the marrow spaces were filled with fibrovascular tissue. DISCUSSION In recent years, researchers have hypothesized that elevation of the sinus membrane without insertion of any grafting material is a suitable technique for bone graft augmentation of the maxillary sinus floor There has been controversy concerning the role of the sinus 86 Volume 26, Number 1, 2011

5 a b c Fig 3a Preoperative panoramic radiograph of patient 3 showing a recent extraction socket (arrow). Fig 3b Radiograph at 6 months after sinus membrane elevation (arrow indicates biopsy area). Fig 3c An implant was placed immediately after trephine biopsy in this second premolar area (arrow indicates elevated area). d Fig 3d CT image of the extraction area shown in Fig 3a. Very thin sinus floor bone was observed. Fig 3e CT image of the elevated area shown in Fig 3b. The sinus floor looked unchanged, but the extraction socket seemed to be filled with newly formed tissue. Fig 3f A biopsy specimen was obtained from the area using a trephine bur. e f Fig 3g New bone tissue (A) developed on the sinus floor bone at 6 months following the membrane elevation. The dotted lines delineate the area of pre-existing sinus floor bone (B) from the newly formed tissue (C) in the extraction socket (H&E; original magnification 40). A B C g membrane. Some studies suggested that the sinus membrane did not possess osteogenic potential. 3,21,22 Kirker-Head et al 22 reported that the maxillary sinus floor augmentation procedure with absorbable collagen sponges failed to mineralize by 4 weeks in an animal study. However, recent studies strongly indicated an osteogenic potential for the sinus membrane ,23 25 In a rabbit experiment, Xu et al 24 observed newly formed woven bone in the augmented space after sinus membrane elevation and grafting of blood clot. The current authors applied the aforementioned bone regeneration hypothesis to actual patients who required sinus floor augmentation for primary implant stability and tried to verify new bone formation on the sinus floor microscopically. In fact, the current authors expected that new bone would develop following sinus elevation. However, contrary to expectations, new bone formation was not demonstrated microscopically in 11 of the 13 specimens. In one specimen (patient 2), newly formed woven bone was found on the host bone, but the amount of new bone was too small to be measurable (Fig 2c). In the other specimen (patient 3), measurable new bone was as much as 0.5 mm thick, but this amount was too small to be clinically significant (Fig 3g). In sinus floor augmentation without bone grafting, it is crucial to keep the membrane elevated and to maintain a new compartment filled with blood clot The International Journal of Oral & Maxillofacial Implants 87

6 The current authors used absorbable collagen sponges rather than suturing of the membrane to the upper border of the bone window. Compared to suturing, the use of collagen sponge was considered to be easy and safe. When suturing is attempted with a very thin membrane, a suture needle can tear the membrane inadvertently, resulting in troublesome membrane perforation. Collagen sponges can support the membrane evenly in all corners of the sinus, and they can be used to repair small perforations as well. In addition, the collagen sponge stabilizes blood clot very well. It resorbs completely within 2 weeks, according to the manufacturer. However, it may remain longer in the sinus cavity, because sinus elevation may compromise blood circulation, resulting in delayed resorption of the sponge. In any event, rapid resorption would be considered a disadvantage of the absorbable sponge. Ideally, a space-maintaining material must survive for a few months while the provisional matrix develops into new bone tissue, and it should disappear afterward. The current authors believe that, although a closed blood clot space is maintained with an ideal space-maintaining material or device following membrane elevation, substantial augmentation of new bone on the sinus floor may not be achievable without the inclusion of an osteoinductive material (eg, bone morphogenic protein). Several clinical studies 13,15,18,26 demonstrated that sinus membrane elevation with simultaneous implant placement resulted in new bone formation without the use of a grafting material. Radiographs and/or CTs were used to assess new bone formation. Palma et al, 14 Sul et al, 17 and Kim et al 27 performed animal studies corresponding to these human studies 13,15,18,26 and observed histologic evidence of new bone formation following sinus membrane elevation with simultaneous implant placement. In their studies, implants were used as tent poles to support the membrane. 14,17,27 Since the sinus membrane is as thin as 0.5 mm and friable, 28 the membrane can collapse with gravity and air pressure in the sinus cavity and cannot be kept elevated on its own. Thus, the range of the tented membrane is limited to the exposed implant. For this reason, new bone formation was observed around the exposed implants. 14,17,27 Based on the present findings, it was thought that human sinus membrane would not react like animal membrane. Especially in younger and smaller animals (eg, young rabbits), membrane elevation alone can result in new bone formation. 20,24 However, the current authors think that such a phenomenon is not likely to happen in the human sinus of a person older than 50 years. No sign of new bone formation was observed in the present study in patients above 50 years of age. However, two specimens from two patients in their 40s showed a small amount of new bone formation. Accordingly, patient age could be one of the factors influencing bone formation. The precise mechanism of new bone formation in the sinus is still not fully understood. It has been generally accepted that a secluded coagulum space created by the elevated membrane and the protruding implant resulted in new bone formation, as indicated by the concept of guided tissue regeneration. 13 The current authors also admit the previous explanations but would suggest another mechanism as well. First, one contribution to new bone formation would be reactive bone formation to the surgical trauma caused by implant insertion and membrane elevation. This kind of new bone formation would be one of the general bone reactions to trauma. Another bone formation mechanism could be postulated: a rotating selftapping implant shaves maxillary bone to produce minute bone particles. Such particles surround the implant surface, and some particles get stuck firmly in between threads. All the particles move together with the penetrating implant into the sinus and serve as autogenous grafting material. In addition, the implant-supported membrane and the sinus floor create a closed space. Accordingly, new bone tissue will develop from the bone particle coagulum mixture within the confined space. Finally, morphologic deformation of the floor could be caused by the implant penetrating into the sinus. While a self-tapping implant is being inserted, it displaces the sinus floor upward and causes a slight elevation of the bone floor. If an osteotome is used as well, the sinus floor bone can be elevated to a certain degree, and such elevation may be interpreted as new bone on a radiograph. Hatano et al 15 performed implant placement and maxillary sinus membrane elevation simultaneously and filled the empty space with venous blood. They described a mean gain in bone height of 10 mm after 6 months of healing in a human study. 15 Bone heights were measured on radiographs. 15 In contrast, Sul et al 17 and Kim et al 27 demonstrated only about 3.5 mm of new bone gain beyond the sinus floor in histologic sections from experimental dogs. Although such animal studies are not identical to human studies, the observation of Hatano et al of a 10-mm increase in bone height may be regarded as overinterpretation of radiographs. 15 Other authors carried out similar clinical studies in which implants were placed after transalveolar maxillary sinus floor elevation without bone grafting. They used an indirect membrane elevation technique that employed osteotomes Leblebicioglu et al 29 reported a gain of 3 to 4 mm of bone from the sinus floor to the implant apex on a radiograph, Nedir et al 30 reported a mean radiographic bone gain within the 88 Volume 26, Number 1, 2011

7 sinus of 2.5 mm, and Pjetursson et al 31 reported that the mean radiographic bone gain was 1.7 mm. When the aforementioned data were considered comprehensively, 15,17,27,29 31 the current authors deduced that approximately 3 mm gain of new bone can be expected if the sinus membrane is elevated simultaneously with implant placement to maintain the space without bone grafting. Also, the current authors think that there may be no difference in the amount of bone gain when the lateral approach technique (direct membrane elevation) is compared to the transalveolar approach technique (indirect membrane elevation), because both elevation techniques employ basically the same concept for bone regeneration. When the histologic figures that other authors had presented in their articles 14,17,27 were closely scrutinized, the current authors came to understand that, although a lateral approach and direct membrane elevation were performed simultaneously with implant placement, new bone formation did not occur in every area of the membrane-elevated sinus floor. The current authors acknowledge that the new bone formation reported 14,17,27 occurred only in the area of the protruding implant and its perimeter. From the results of the present study it may be concluded that if a substantial amount of new bone is necessary for primary implant stability, sinus elevation should be performed in conjunction with the application of bone or bone substitute grafting material. If bone grafting is not performed, sinus elevation should be performed simultaneously with implant placement to maintain the closed coagulum space for new bone formation. CONCLUSION The present study of 13 maxillary specimens in eight consecutive patients did not show any apparent new bone formation on the sinus floor at 6 months after sinus membrane elevation and support with bloodsoaked collagen sponges. ACKNOWLEDGMENT This work was supported by the Korea Science and Engineering Foundation (KOSEF) grant funded by the Korea government (MOST) (No. M N ). REFERENCES 1. Wood RM, Moore DL. Grafting of the maxillary sinus with intraorally harvesting autogenous bone prior to implant placement. Int J Oral Maxillofac Implants 1988; 3: Schliephake H, Neukam F, Wichmann M. Survival analyses of endosseous implants in bone grafts used for treatment of severe alveolar ridge atrophy. J Oral Maxillofac Surg 1997; 55: Boyne P, James RA. Grafting of the maxillary floor with autogenous marrow and bone. J Oral Surg 1980;38: Lundgren S, Moy P, Johansson C, Nilson H. 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8 17. Sul SH, Choi BH, Li J, Jeong SM, Xuan F. Effects of sinus membrane elevation on bone formation around implants placed in the maxillary sinus cavity: An experimental study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;105: Jeong SM, Choi BH, Li J, Xuan F. A retrospective study of the effects of sinus membrane elevation on bone formation around implants placed in the maxillary sinus cavity. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2009;107: Lundgren S, Andersson S, Sennerby L. Spontaneous bone formation in the maxillary sinus after removal of a cyst: Coincidence or consequence? Clin Implant Dent Relat Res 2003; 5: Jung YS, Chung SW, Nam W, Cho IH, Cha IH, Park HS. Spontaneous bone formation on the maxillary sinus floor in association with an extraction socket. Int J Oral Maxillofac Surg 2007;36: Hürzerler MB, Quiñones CR, Kirsch A, et al. Maxillary sinus augmentation using different grafting materials and dental implants in monkeys. Part III. Evaluation of autogenous bone combined with porous hydroxyapatite. Clin Oral Implants Res 1997;8: Kirker-Head CA, Nevins M, Palmer R, Nevins ML, Schelling SH. A new animal model for maxillary sinus floor augmentation: Evaluation parameters. Int J Oral Maxillofac Implants 1997; 12: Gruber R, Kandler B, Fuerst G, Fischer MB, Watzek G. Porcine sinus mucosa holds cells that respond to bone morphogenetic protein BMP-6 and BMP-7 with increased osteogenic differentiation in vitro. Clin Oral Implants Res 2004;15: 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: Srouji S, Kizhner T, Ben-David D, Riminucci M, Bianco P, Livne E. The Schneiderian membrane contains osteoprogenitor cells: In vivo and in vitro study. Calcif Tissue Int 2009;84: Sohn DS, Lee JS, Ahn MR, Shin HI. New bone formation in the maxillary sinus without bone grafts. Implant Dent 2008; 17: Kim HR, Mo DY, Lee CU, Yoo JH, Choi BH. The use of autologous blood for maxillary sinus floor augmentation in conjunction with the sinus membrane elevation: An experimental study. J Kor Oral Maxillofac Surg 2009;35: Sul SH, Choi BH, Li J, Jeong SM, Xuan F. Histologic changes in the maxillary sinus membrane after sinus membrane elevation and the simultaneous insertion of dental implants without the use of grafting materials. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;105(4):e1 e Leblebicioglu B, Ersanli S, Karabuda C, Tosun T, Gokdeniz H. Radiographic evaluation of dental implants placed using an osteotome technique. J Periodontol 2005;76: Nedir R, Nurdin N, Szmukler-Moncler S, Bischof M. Placement of tapered implants using an osteotome sinus floor elevation technique without bone grafting: 1-year results. Int J Oral Maxillofac Implants 2009;24: Pjetursson BE, Ignjatovic D, Matuliene G, Brägger U, Schmidlin K, Lang NP. Transalveolar maxillary sinus floor elevation using osteotomes with or without grafting material. Part II: Radiographic tissue remodeling. Clin Oral Implants Res 2009; 20: Volume 26, Number 1, 2011