Maxillary sinus grafting with Bio-Oss or Straumann Bone Ceramic: histomorphometric results from a randomized controlled multicenter clinical trial

Introduction: This investigation was designed to compare the histomorphometric results from sinus floor augmentation with anorganic bovine bone (ABB) and a new biphasic calcium phosphate, Straumann^® Bone Ceramic (BCP). Materials and methods: Forty‐eight maxillary sinuses were treated in 37 patients. Residual bone width was ≥6 mm and height was ≥3 mm and <8 mm. Lateral sinus augmentation was used, with grafting using either ABB (control group; 23 sinuses) or BCP (test group; 25 sinuses); sites were randomly assigned to the control or test groups. After 180–240 days of healing, implant sites were created and biopsies taken for histological and histomorphometric analyses. The parameters assessed were (1) area fraction of new bone, soft tissue, and graft substitute material in the grafted region; (2) area fraction of bone and soft tissue components in the residual alveolar ridge compartment; and (3) the percentage of surface contact between the graft substitute material and new bone. Results: Measurable biopsies were available from 56% of the test and 81.8% of the control sites. Histology showed close contact between new bone and graft particles for both groups, with no significant differences in the amount of mineralized bone (21.6±10.0% for BCP vs. 19.8±7.9% for ABB; P=0.53) in the biopsy treatment compartment of test and control site. The bone‐to‐graft contact was found to be significantly greater for ABB (48.2±12.9% vs. 34.0±14.0% for BCP). Significantly less remaining percentage of graft substitute material was found in the BCP group (26.6±5.2% vs. 37.7±8.5% for ABB; P=0.001), with more soft tissue components (46.4±7.7% vs. 40.4±7.3% for ABB; P=0.07). However, the amount of soft tissue components for both groups was found not to be greater than in the residual alveolar ridge. Discussion: Both ABB and BCP produced similar amounts of newly formed bone, with similar histologic appearance, indicating that both materials are suitable for sinus augmentation for the placement of dental implants. The potential clinical relevance of more soft tissue components and different resorption characteristics of BCP requires further investigation.     

Histomorphometry of human sinus floor augmentation using a porous beta-tricalcium phosphate: a prospective study

Tricalcium phosphate (TCP) has been historically a well-accepted material for bone augmentation. We examined the use of a porous beta-TCP (100%) in a split mouth model for sinus floor augmentation. Five patients were treated bilaterally, receiving 1-2 mm-sized beta-TCP particles (Cerasorb) on one side (test side) and autologous chin bone particles on the other (control) side. Four other patients were treated with a unilateral sinus floor augmentation using 100% beta-TCP (no controls). Biopsies of the augmented sites were taken at 6 months. Histomorphometry measurements were carried out in order to quantify bone augmentation at test and control sides. The average bone volume (BV) formed in the augmented sinus at the control side was 41% (32-56%) and 17% (9-27%) in the test side when all nine patients were included (statistically significant, P=0.04). When only the five bilateral patients were included, mean BV of the test side was 19% (13-27%), which was also significantly different from the control side (P=0.009). Osteoid formation tended to be higher in the test side biopsies (1.3%) than in the controls (0.3%) (marginally significant, P=0.1), indicating ongoing bone formation in the TCP material. The amount of lamellar bone at the test side was less than half the amount in the control side, indicating that remodelling had only recently started in the TCP-augmented side. The resorption surface, however, did not differ significantly between the two sides. These histological results indicate that Cerasorb is an acceptable bone substitute material for augmentation of the maxillary sinus. Due to the osteoconductive, but not osteoinductive properties of this material, the rate of bone formation is somewhat delayed in comparison to autologous bone.     

The use of Straumann® Bone Ceramic in a maxillary sinus floor elevation procedure: a clinical,radiological, histological and histomorphometric evaluation with a 6‐month healing period

Objectives: In this study, we evaluated the quality and quantity of bone formation in maxillary sinus floor elevation procedure using a new fully synthetic biphasic calcium phosphate (BCP) consisting of a mixture of 60% hydroxyapatite and 40% of β‐tricalcium phosphate (Straumann^® Bone Ceramic). Material and methods: A unilateral maxillary sinus floor elevation procedure was performed in six patients using 100% BCP. Biopsy retrieval for histological and histomorphometric analysis was carried out before implant placement after a 6‐month healing period. Results: In this study, the maxillary sinus floor elevation procedure with the use of BCP showed uneventful healing. Radiological evaluation after 6 months showed maintenance of vertical height gained immediately after surgery. Primary stability was achieved with all Straumann^® SLA dental implants of 4.1 mm diameter and 10 or 12 mm length. The implants appeared to be osseointegrated well after a 3‐month healing period. Histological investigation showed no signs of inflammation. Cranial from the native alveolar bone, newly formed mineralized tissue was observed. Also, osteoid islands as well as connective tissue were seen around the BCP particles, cranial from the front of newly formed mineralized tissue. Close bone‐to‐substitute contact was observed. Histomorphometric analysis showed an average bone volume/total volume (BV/TV) of 27.3% [standard deviation (SD) 4.9], bone surface/total volume (BS/TV) 4.5 mm²/mm³ (SD 1.1), trabecula‐thickness (TbTh) 132.1 μm (SD 38.4), osteoid‐volume/bone volume (OV/BV) 7.5% (SD 4.3), osteoid surface/bone surface (OS/BS) 41.3% (SD 28.5), osteoid thickness (O.Th) 13.3 μm (SD 4.7) and number of osteoclasts/total area (N.Oc/Tar) 4.4 1/mm (SD 5.7). Conclusions: Although a small number of patients were treated, this study provides radiological and histological evidence in humans confirming the suitability of this new BCP for vertical augmentation of the atrophied maxilla by means of a maxillary sinus floor elevation procedure allowing subsequent dental implant placement after a 6‐month healing period. The newly formed bone had a trabecular structure and was in intimate contact with the substitute material, outlining the osteoconductive properties of the BCP material. Bone maturation was evident by the presence of lamellar bone. To cite this article:
Frenken JWFH, Bouwman WF, Bravenboer N, Zijderveld SA, Schulten EAJM, ten Bruggenkate CM. The use of Straumann^® Bone Ceramic in a maxillary sinus floor elevation procedure: a clinical, radiological, histological and histomorphometric evaluation with a 6‐month healing period.
Clin. Oral Impl. Res. 21 , 2010; 201–208.
doi: 10.1111/j.1600‐0501.2009.01821.x     

Histological observations of a bilateral maxillary sinus floor elevation 6 and 12 months after grafting with osteogenic protein-1 device

OBJECTIVE: The purpose of this case study was to analyze the tissue formed in a maxillary sinus, 6 and 12 months after grafting with recombinant human osteogenic protein-1 (OP-1) linked to a collagen carrier of bovine origin. PATIENT AND METHODS: A 49-year-old woman referred for bilateral sinus floor elevation, was grafted with an OP-1 device. After 6 months, a biopsy was taken from one of the grafted areas. After 12 months, during implant placement, 5 biopsies were taken from the grafted area and the maxillary host bone. Biopsies were processed without decalcification for histological analyses. RESULTS: The biopsy taken after 6 months contained newly formed bone, fibrotic tissue and device remnants. After 12 months, however, bone was absent from all biopsies which were taken from the grafted area, while particles of the collagen carrier were still abundant. Inflammatory cells were observed between remnants of the collagen carrier in the grafted area. CONCLUSION: This study indicates that an onset of new bone formation, which was observed after 6 months, did not persist. 12 months after grafting no bone was present in the biopsies from the grafted area, while the collagen carrier had remained. Lack of mechanical loading, as a result of postponing implant placement from 6 to 12 months, may have resulted in resorption of the emerging bone which was present 6 months after grafting.     

Histologic and clinical evaluation for maxillary sinus augmentation using macroporous biphasic calcium phosphate in human

Objectives: This study evaluated both the clinical and histological aspects of bone formation in maxillary sinus augmentation using MBCP as the bone-grafting material.
Material and methods: MBCP was used as a primary bone substitute for maxillary sinus augmentation. Fifty-two patients were selected after a medical and dental examination, and were divided into the following three groups: those augmented with MBCP only; MBCP combined with irradiated cancellous bone; and MBCP combined with intraoral autogenous bone. After a healing period (average 6.78 months after surgery), bone cores were harvested for a histological evaluation and the implant fixtures were installed. These bone cores were evaluated via light microscope and implants were followed up for at least six months after loading.
Results: Four to ten months after surgery, new vital bone surrounding the MBCP particles was observed in 18 bone biopsies. Two out of the 130 implants installed were explanted due to a failure of osseointegration before the prosthetic procedure. All the remaining implants were functioning for 6 to 27 months (average 12.96 months). The cumulative survival rate of the implants was 98.46%.
Conclusion: These results show that MBCP can be used as a grafting material for sinus floor augmentation, whether combined with other bone graft materials or not, and lead to a predictable prognosis for dental implants in the posterior maxillary area where there is insufficient vertical height for fixture installation.     

关于上颌窦底提升术骨增量策略的研究进展

上颌后牙区骨高度不足是种植手术常见的问题之一。而上颌窦底提升术拓宽了上颌后牙区种植的适应证。随着临床技术的进步和口腔材料学的发展,上颌窦底提升术的植骨策略不断更新。尽管上颌窦内的成骨机制尚未完全阐明,但上颌窦底提升术不植骨已经得到了越来越多的认可,如何选择和把握适应证是该策略的关键。经典传统的骨移植材料存在不同程度的缺陷,新型骨组织工程辅助材料应运而生,部分已得到临床应用。该文就上颌窦底提升术是否植骨、骨移植材料等方面的研究进展作一综述。     

Maxillary sinus augmentation using xenogenic bone substitute material Bio-Oss in combination with venous blood. A histologic and histomorphometric study in humans

The aim of the present study was to evaluate bone formation following maxillary sinus augmentation using bovine bone substitute material Bio‐Oss^® in combination with venous blood by means of histologic and histomorphometric examination of human biopsies. This involved a total of 15 sinus floor elevation procedures being carried out on 11 patients (average age of 49.6 years) according to the technique described by Tatum (1986). The subantral sinus cavity was augmented using bovine apatite combined with venous blood. After an average healing phase of 6.8 months, trephine burrs were used to take 22 bone biopsies from the augmented sinus region. Then 38 Brånemark^® implants were inserted in both the osteotomies resulting from bone sampling and in regular sites in the augmented posterior maxilla. Histomorphometric analysis of ground sections from the bone biopsies prepared according to the standard method of Donath & Breuner (1982) produced an average percentage of newly‐formed bone of 14.7% (±5.0%) and a proportion of residual xenogenic bone substitute material of 29.7% (±7.8%). Some 29.1% (±8.1%) of the surface of the Bio‐Oss^® granulate was in direct contact with newly‐formed bone. Histologically, newly‐developed bone became evident, partly invaginating the particles of apatite and forming bridges in the form of trabeculae between the individual Bio‐Oss^® particles. Despite the absence of osteoclastic activity, the inward growth of bone indicates slow resorption of the xenogenic bone graft material. When the implants were uncovered, after an average healing phase of 6 months, 4 of the 38 implants had become loose. Of these 4 implants, 1 had to be subsequently explanted, while the others remained as “sleeping implants” and were not included in the implants superstructure. Thus, the resulting clinical survival rate, prior to prosthetic loading, was 89.5%.     

Injectable calcium phosphate cement as a graft material for maxillary sinus augmentation: an experimental pilot study

Objectives: The aim of the present study was to evaluate the efficiency of injectable CaP cement as a graft material around dental implants in the maxillary sinus augmentation procedure. Material and methods: Bilateral sinus augmentation process was carried out in three sheep and two implants were inserted during the same session. Out of a total of 12 installed implants, eight belonged to the so‐called experimental group. In the experimental group, injectable CaP cement was used as augmentation material while autologous bone served as control. Results: Histological examination revealed that newly formed bone surrounded the cement completely without an intervening fibrous tissue layer. Following a healing period of 12 weeks, mean bone‐to‐implant contact (BIC) values in the experimental and control groups were 36±5 and 37±3, respectively. The percentage of BIC was comparable with other experimental sinus augmentation studies. Further, it appeared that the thickness of the cortical bone that covered the outer surface of the maxillary sinus was <2–3 mm, which affected the primary stability of the implants negatively. Conclusion: CaP cement is indeed effective to stimulate bone formation in the sinus elevation procedure. Nevertheless, additional improvements in the cement composition are required to allow final clinical utilization of the material.     

Healing of rabbit calvarial bone defects using biphasic calcium phosphate ceramics made of submicron‐sized grains with a hierarchical pore structure

Objectives: This study investigated the efficacy of new bone graft substitutes – biphasic calcium phosphates (BCP) made of submicron‐sized grains with fully interconnected wide‐range micron‐scale pores in two different macrodesigns: donut shaped with a 300–400 μm central macropore (n‐BCP‐1) or rod‐shaped (n‐BCP‐2) – in the healing of rabbit calvarial defects, and compared their bone‐healing properties with those of various commercial bone substitutes, which included substitutes with similar BCP composition (MBCP and Osteon), anorganic bovine bone (Bio‐Oss), and β‐TCP (Cerasorb). Material and methods: The surface morphology of the bone substitutes was investigated using scanning electron microscopy (SEM). Defects 8 mm in diameter were created in the calvaria of 30 adult male New Zealand White rabbits and were filled with six types of bone substitutes. The percentage of newly formed bone (NB%) was evaluated histomorphometrically 4 and 8 weeks after implantation. Results: SEM observation showed submicron‐sized grains with fully interconnected micropore structures in the n‐BCP‐1 and n‐BCP‐2 groups; these groups also showed considerable new bone formation in inner micropores as well as on the outer surfaces. The n‐BCP‐1 group exhibited enhanced new bone formation and direct ingrowth of bone tissue with blood vessels into central pores. Histomorphometric analysis showed significantly greater NB% in the n‐BCP‐1 group when compared with the other groups at 4 and 8 weeks (P<0.05). Conclusion: A new BCP ceramics made of submicron‐sized grains with a hierarchical pore structure was an effective osteoconductive material for the treatment of osseous defects of rabbit calvaria. To cite this article:
Park J‐W, Kim E‐S, Jang J‐H, Suh J‐Y, Park K‐B, Hanawa T. Healing of rabbit calvarial bone defects using biphasic calcium phosphate ceramics made of submicron‐sized grains with a hierarchical pore structure.
Clin. Oral Impl. Res. 21 , 2010; 268–276.
doi: 10.1111/j.1600‐0501.2009.01846.x     

Maxillary sinus floor grafting with beta-tricalcium phosphate in humans: density and microarchitecture of the newly formed bone

OBJECTIVES: Graft insertion can effectively enhance the regeneration of debilitated bone. The effects of an alloplastic bone-replacing material, beta-tricalcium phosphate (Cerasorb), and of autogenous bone graft were compared. MATERIALS AND METHODS: In 17 edentulous patients, the maxillary sinus floor was extremely atrophied to such an extent that implant placement was impossible. The Schneiderian membrane was surgically elevated bilaterally by insertion of Cerasorb (experimental side) and autogenous bone graft (control side). After surgery, the recovery was followed clinically and radiologically. After 6 months, 68 bone cylinders were excised from the grafted areas and implants were inserted into their places. The bone samples were embedded into resin, and the osteointegration of the grafts was studied histologically. Trabecular bone volume (TBV) and trabecular bone pattern factor (TBPf) were quantified by histomorphometry. RESULTS: Cerasorb proved to be an effective bone-replacing material with osteoconductivity; it was capable of gradual disintegration, thereby providing space for the regenerating bone. The new bone density was not significantly different on the experimental and control sides (32.4+/-10.9% and 34.7+/-11.9%, respectively). However, the graft biodegradation was significantly slower on the experimental side than the control side. The TBPf value was lower on the control side than on the experimental side (-0.53+/-1.7 and -0.11+/-1.4 mm(-1), respectively), but this difference was not significant. CONCLUSIONS: Six months after insertion of the grafts, the bone of the augmented sinus floor was strong and suitable for anchorage of dental implants, irrespective of whether autogenous bone or Cerasorb particles had been applied.     

Bovine hydroxyapatite for maxillary sinus grafting: comparative histomorphometric findings in sheep

This experimental study in animals examines the value of bovine hydroxyapatite as grafting material in one-stage sinus lift procedure. The Schneiderian membrane was elevated from extraorally in 54 sinuses of 27 adult female mountain sheep. Two titanium plasma-flame-spray coated cylindrical implants were placed in each sinus in the same session. In 2 groups of 18 sinuses each, the subantral hollow space was filled with bovine hydroxyapatite and autogenous cancellous bone from the iliac crest, respectively. Eighteen sinuses that were left empty served as a control group. Polyfluorochrome sequential labelling (tetracycline, calcein green, alizarin complexon) was carried out 4 weeks postoperatively, 2 weeks before the animals were sacrificed, and halfway through the observation period to assess new bone formation. The selected observation periods were 12 weeks, 16 weeks, and 26 weeks. Six sinuses per observation period and test group were available for histologic evaluation. All implants showed favourable osseointegration into local bone. New bone formation was observed in a triangular area bound by the implant surface, the local buccal antral wall, and submucous connective tissue in all implants. Bovine hydroxyapatite adjacent to local bone was mainly surrounded by bone tissue. There was a great variation in the extent of bony sheathing of the hydroxyapatite particles, irrespective of the animals' survival time. Macrophages were found around HA particles that were not surrounded by bone as well as on free implant surfaces. The mean length of the bone-implant bond was 3.86 mm in the group of empty sinuses, 4.87 mm in the group augmented with hydroxyapatite, and 5.66 mm in the group augmented with autogenous cancellous bone. During the observation period, the relative length of bone in direct contact with the implant surface increased from 20.0% to 25.1% in the control group, from 30.4% to 35.5% in the group treated with autogenous cancellous bone, and from 27.4% to 34.7% in the HA group. Autogenous cancellous bone showed a significantly greater bone-implant contact than did the control group (P=0.0004) and the HA group (P=0.0499). When the apical implant portions were examined separately, both HA (P=0.006) and autoge-nous cancellous bone (P=0.005) showed a significantly better bone-implant bond than did the control group.     

How to avoid intraoperative and postoperative complications in maxillary sinus elevation

Maxillary sinus floor elevation, via the lateral approach, is one of the most predictable bone augmentation procedures performed in implant dentistry. but both intra‑ and postoperative complications can occur, and some of them are severe. Our aim is as follows:

1. To review the pertinent literature on the topic, especially assessing the risk factors related to complications.
2. To give clinical recommendations to minimize intra‑ and postoperative complications with the ultimate scope of improving the standard of clinical care and patient safety.