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Maxillary Sinus Augmentation With Calcium Phosphate Double-Coated Anorganic Bovine Bone

Comparative Multicenter Randomized Clinical Trial With Histological and Radiographic Evaluation

Pang, Kang-Mi, DDS, PhD*; Lee, Jeong-Keun, DDS, PhD; Choi, Seong-Ho, DDS, PhD; Kim, Young-Kyun, DDS, PhD§; Kim, Bong-Ju, PhD; Lee, Jong-Ho, DDS, PhD

doi: 10.1097/ID.0000000000000844
Basic and Clinical Research

Purpose: The purpose of this study was to evaluate the clinical, histological and radiographic outcomes of the calcium phosphate double-coated anorganic bovine bone (InduCera; Oscotec Inc., Seongnam, Gyeonggi, Republic of Korea) compared with that of anorganic bovine bone (Bio-Oss; Geistlich Biomaterials, Wolhusen, Switzerland) in maxillary sinus augmentation, prospectively.

Patients and Methods: Twenty-eight sinuses in 25 patients (3 bilateral) with vertical alveolar bone height from 2 to 5 mm were included in this study. The maxillary sinus was augmented with InduCera or Bio-Oss, followed by a healing period of 6 months. Trephine cores were obtained for histomorphometric evaluation with the implant placement. Cone-beam computed tomography (CBCT) scans were taken at 1 week and 6 months after sinus augmentation.

Results: The graft sites were healed without any notable complications in both groups. In histomorphometric analysis, the area of the newly formed bone was measured as 21.37 ± 8.87% for InduCera and 23.02 ± 5.88% for Bio-Oss, with no significant differences. Radiographically, no statistically significant differences were calculated between the groups in bone height at baseline, the height of bone augmentation, the final alveolar bone height (alveolar bone height + augmented height) after 6 months in panoramic radiograph. There were also no significant differences in the shrinkage rate of the grafted area volume in CBCT.

Conclusion: Although calcium phosphate double-coated anorganic bovine bone showed no additional effect compared with anorganic bovine bone from a histological and radiographical point of view, it could be used as the bone graft material in maxillary sinus augmentation.

*Clinical Associate Professor, Department of Oral and Maxillofacial Surgery, Seoul National University Gwanak Dental Hospital, Seoul, Korea.

Professor, Department of Dentistry, Oral and Maxillofacial Surgery, School of Medicine, Ajou University, Suwon, Korea.

Professor, Department of Periodontology, College of Dentistry, Yonsei University, Seoul, Korea.

§Professor, Department of Oral and Maxillofacial Surgery, Seoul National University Bundang Hospital, Seoul, Korea.

Professor, Clinical Trial Center, Seoul National University Dental Hospital, Seoul, Korea.

Reprint requests and correspondence to: Jong-Ho Lee, DDS, PhD, Department of Oral and Maxillofacial Surgery, Clinical Trial Center, Seoul National University Dental Hospital, 101 Daehakno, Jongno-Gu, Seoul 03080, Korea, Phone: +82-2-2072-2630, Fax: +82-2-766-4948, E-mail:

Since Tatum1 and Boyne and James2 described the techniques for bone grafting of the maxillary sinus, sinus floor augmentation has provided enough quantity of bone for dental implants and was considered as a predictable technique.3 Despite the clinical establishment of the surgical technique, studies still search for the optimal bone substitute. Many materials have been used including autogenous bone, allografts, xenografts, synthetics, and mixtures of various materials.4 Among them, anorganic bovine bone (Bio-Oss), produced by removing all the organic components of the bovine bone, has osteoconductive properties and has been used in the treatment of various bone deficiencies with clinically successful results.5 However, Bio-Oss has slower turnover rate and the low resorption rate may compromise the mechanical properties of the regenerated bone,6 and studies combining synthetic and osteoinductive materials have been conducted.7 Among them, calcium phosphate–based biomaterials are similar to natural bone in their biodegradability, bioactivity, and osteoconductivity.8

Calcium phosphate has been known to be resolved in vivo by chemical dissolution and cell migration degradation. In chemical dissolution, soluble ionic products from degradable bioceramics stimulate proliferation, aggregation, differentiation, bone matrix formation, and mineralization of osteogenic precursor cells via the AMPK-Erk1/2 pathway and provide calcium and phosphate ions for bone formation.9–13 The solubility of calcium phosphate depends on the Ca/P ratio and the crystallinity degree; less crystalline material has higher solubility.14 Calcium phosphate double-coated bovine porous bone mineral was developed and named as InduCera. The outer layer was coated with nonsintered, low-grade calcium phosphate crystal (hydroxyapatite) for rapid resorption rate, whereas the inner layer was sintered with mid-grade calcium phosphate crystal (hydroxyapatite) for slower resorption rate. Through these different resorption rates of calcium phosphate, early bone formation was reported to be promoted in the outer layer via differentiation of mesenchymal cells into osteoblasts by absorbing abundant growth factors and releasing bioactive ions.12 The inner layer affects continuous bone formation through additional recruitment of osteoblasts by slowly releasing bioactive ions.

Although recent studies doubt the necessity of a bone graft in sinus augmentation and proved bone formation only with space maintenance,15–17 Nedir et al16 warned the absence of a graft in case of severely deficient posterior maxilla with residual bone height less than 2 mm. Also, the grafted bone was histologically more mature and seemed to be clinically harder compared with the nongraft area.15 Therefore, comparing the histological and radiological bone quality seemed to be reasonable to evaluate 2 bone graft materials in sinus augmentation with alveolar bone height less than 5 mm.

The purpose of the study was to test the bone-regenerating efficacy of this new grafting material in the human maxillary sinus floor augmentation procedures. The clinical, histological and radiographical characteristics of the calcium phosphate double-coated anorganic bovine bone was evaluated and compared with those of standard anorganic bovine bone.

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Patients and Methods

Characteristics of Bone Graft Material

In this randomized, controlled clinical trial, 2 kinds of bone graft materials were used for the sinus augmentation: Calcium phosphate crystal double-coated bovine bone (InduCera) and anorganic bovine bone (Bio-Oss). Bio-Oss is a natural, nonantigenic, porous bone mineral matrix produced by the removal of all organic components from the bovine bone.

InduCera is a bovine porous bone mineral coated dually with calcium phosphate (Ca-P). A thin layer of low-grade Ca-P crystals was formed by immersing deproteinized bovine bone into calcium phosphate–supersaturated solution at low temperature.18 Briefly after fabrication of the deproteinized bovine bone, the materials were left in Ca-P-supersaturated solution at low temperature (under 60°C) for 16 hours and were sintered from 100°C to 600°C. Sintered materials were recoated with the Ca-P-supersaturated solution at low temperature again as described above. Thus, the inner layer was coated with sintered mid-grade Ca-P crystal, and the outer layer was a nonsintered low-grade Ca-P crystal. Scanning electron microscope images are shown in Figure 1. The X-ray diffraction (XRD) data showed that the percentage of hydroxyapatite was 99.7% and the Ca/P ratio was 1.65.

Fig. 1

Fig. 1

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Patients and Entry Criteria

This clinical trial was conducted from November 2011 to November 2016 at 4 hospitals: Seoul National University Dental Hospital, Seoul National University Bundang Hospital, Severance Dental Hospital, and Ajou University Hospital (IRB No. CDE11002 at Seoul National University Dental Hospital). Patients requiring unilateral or bilateral sinus floor augmentation for dental implants with residual alveolar ridge bone height of 2–5 mm, as measured by a panoramic radiograph, were included in this randomized, controlled multicenter clinical trial. They also did not have any wound healing–related diseases and smoking habit.

Forty-one patients were screened and 33 patients satisfied the inclusion criteria to be selected for this study, and the types of bone graft materials were assigned by block randomization by a research nurse. However, only 25 of 33 patients appeared for the appointment and were operated on. Different graft materials were used in each sinus in 3 patients who needed bilateral maxillary sinus augmentation. Eleven maxillary sinuses (mean age = 56.67 ± 10.53 years, male:female = 6:5, right sinus: left sinus = 5:6) were grafted using InduCera, and 17 maxillary sinuses (mean age = 52.89 ± 12.69, male:female = 8:9, right sinus: left sinus = 12:5) were treated using Bio-Oss. The assignment of which graft material was to be used was concealed from the patients and the examiner who conducted the histomorphometric analysis.

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Sinus Elevation

Before sinus augmentation, cone-beam computed tomography (CBCT) was performed to measure the topography of the maxillary sinus and the vertical residual alveolar bone height in the region of interest. Lateral sinus augmentation was performed under local anesthesia. After mucoperiosteal incision, the lateral sinus wall was exposed and the Schneiderian membrane was elevated through a lateral bone window created using a round bur under sterile saline irrigation, with the inferior border of about 5 mm upper to the alveolar crest margin.19 Then, the bone graft materials (InduCera or Bio-Oss) were inserted. After augmentation of the graft material, the window was covered with a collagen membrane (BioGide; Geistlich AG, Baden-Baden, Germany). After suturing, all patients were prescribed postoperative antibiotics (Augmentin 625 mg) and acetaminophen (Tylenol 600 mg) for 5 days and were instructed not to blow through the noses for 2 weeks. After 7 days, the sutures were removed and postoperative panoramic radiography and CBCT were performed.

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Implantation and Biopsies

After a healing period of 6 months, CBCT was performed to visualize the bone graft site. Trephine cores at sites planned for implant fixture placement were harvested using a trephine bur (outer diameter 3.0 mm, inner diameter 2.3 mm, length 14 mm; Dentium, Suwon, Korea) for histological and histomorphometric analysis. The trephine bur was drilled as apically as possible to contain the residual alveolar bone and the augmented bone under saline irrigation. After further drilling, implants were placed. The harvested trephine cores were immersed in 10% formalin solution and were sent for histological assessment. Postoperative panoramic radiography was performed.

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Radiographic Analysis

Panoramic radiograph and CBCT were performed before the sinus lift procedure (T0), 1 week after surgery (T1) and 6 months after surgery (T2) for volumetric analysis. The CBCT scan data were analyzed using an image processing software (Simplant, Materialise, Beuven, Belgium). The grafted bone area (B) and total volume (T), including bone and soft-tissue volume, which was temporarily thickened by the operation, were outlined manually by the examiner in each axial image; the volume was calculated automatically in the software (Fig. 2). The bone volume (B), the ratio of soft-tissue volume (T-B)/total volume (T) at T1, T2, and the ratio of remaining bone volumes (B at T2/B at T1) were calculated for each sinus to evaluate the volumetric change.

Fig. 2

Fig. 2

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Histomorphometric Analysis

The harvested specimens were dehydrated using a dehydration system with agitation and vacuum in graded ethanol dilutions and were embedded in light-cured methacrylate (Technovit 7200 VCL; HeraeusKulzer GmbH, Wehrheim, Germany). Then, they were cut along the median longitudinal axis using the sawing and grinding technique (EXAKT Apparatebau, Norderstedt, Germany). Because the specimens contained both residual alveolar bone and augmented bone, the evaluation parameters were different in 2 areas. In the residual alveolar bone, (1) the ratio of bone volume compared with total volume (mineralized components) and (2) the ratio of intertrabecular volume compared with total volume (soft tissue components) were evaluated. In the augmented region in the maxillary sinus, quantitative evaluations of (1) the ratio of newly formed bone volume compared with total volume, (2) the ratio of residual graft material volume compared with total volume, and (3) the ratio of soft-tissue component volume compared with total volume (calculated by subtracting 1 and 2 from the total area) were performed by a single examiner who is unaware of the kind of grafted material used because of blinding.

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The statistical tests were based on the sinus as the unit. The statistical analysis was performed using SPSS version 18 (SPSS, Chicago, IL). The Mann-Whitney test was used to compare the numerical measurements between the 2 groups. The differences were considered statistically significant when the P values were less than 0.05. To evaluate the relationship between the percentage of the remaining bone measured by CBCT and the histomorphometric result, the Spearman correlation coefficient was used.

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Twenty-seven sinuses in 25 patients healed uneventfully. Any postoperative infection or wound dehiscence were not observed, and all dental implants were placed as planned.

Twenty-eight bone biopsies using a trephine were performed from the implant site, and 4 samples (1 InduCera and 3 Bio-Oss samples) were lost during removal, thus 10 InduCera and 14 Bio-Oss samples were evaluated for histomorphometric analysis. For the radiological analysis, only 6 patients in the InduCera group and 6 patients in the Bio-Oss group were analyzed because other patients did not accept to have CBCT performed at T1.

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Histomorphometrical Results

The transition from residual alveolar bone to augmented bone was discernible in most cases. In the augmented region, the grafted bone substitute materials showed good tissue integrity (Fig. 3). Direct contact was observed between the graft materials and the newly formed bone in both groups, demonstrating osteoconductive properties.

Fig. 3

Fig. 3

The mineralized and soft-tissue components in the residual maxillary alveolar bone were measured to assess alveolar bone quality. The mineralized component was 37.03 ± 16.10% for InduCera and 43.06 ± 14.22% for Bio-Oss. No significant differences were found in the composition of the alveolar bone between the 2 groups (P = 0.408), which meant similar distribution of the patients.

In the augmented region, the histomorphometric evaluation showed that the amounts of the newly formed bone and the remaining grafted material fractions were similar in the 2 groups (Table 1). The mineralized components (newly formed bone + residual graft material) occupied approximately half of the total area of harvested regenerated tissues.

Table 1

Table 1

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Radiological Results

The mean alveolar bone height at baseline and the mean height of bone augmentation measured through panoramic radiography are shown in Table 2. No statistically significant differences were calculated between the groups (P = 0.433 bone height at baseline, P = 0.704 height of bone augmentation, and P = 0.535 height of bone after 6 months).

Table 2

Table 2

The mean and the change in volume of the grafted area are presented in Table 3. The mean bone volume at T1 was 1709 ± 302 mm3 (range from 1368 to 2190 mm3) in the InduCera group and 1910 ± 945 mm3 (range from 835 to 3160 mm3) in the Bio-Oss group. At T2, the bone volume was 1324 ± 302 mm3 (range from 853 to 1763 mm3) and 1,517,810 ± 684,762 mm3 (range from 644 to 2478 mm3) in InduCera and Bio-Oss, respectively. No significant difference was found between the 2 groups (P = 0.631, 0.589 at T1, T2, respectively). The average percent volume of graft materials that remained after 6 months was 78.12 ± 17.33% (range from 62.37% to 106.08%) in InduCera and 107.55 ± 86.22%% (range from 32.17% to 249.47%) in Bio-Oss. Although the average percentage was much higher in the Bio-Oss group, the statistical analysis showed no significant differences (P = 0.024). This increased value seemed to be influenced by 1 outlier in the Bio-Oss group, where the bone volume at T2 was increased by 249%.

Table 3

Table 3

As for the soft-tissue volume, the initial volume at T1 was larger than the graft bone volume, occupying 69.20% and 63.13% of the total volume in InduCera and Bio-Oss, respectively. Then, the swelling of the soft tissue was decreased by 27.71% and 6.72% in InduCera and Bio-Oss, respectively, at 6 months postoperatively. There were no significant differences between the 2 groups (P = 0.631 and 0.4 at T1 and T2).

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Relationship Between Histomorphometric and Radiologic Results

To evaluate whether there was any relationship between the percent volume of graft materials that remained after 6 months measured by CBCT and the percentage of mineralized component (new bone + graft material) measured by histomorphometric analysis, the Spearman correlation coefficient was used, and there was no statistically significant relationship (P = 0.143). Also, no relationship was found between the percent volume of graft materials that remained in CBCT and the percentage of remained graft material in histomorphometry (P = 0.536).

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The present study evaluated the histomorphometric and radiographical result of the calcium phosphate double-coated anorganic bovine bone and anorganic bovine bone for sinus augmentation.

In histomorphometric analysis, there were no statistically significant differences between the 2 groups in newly formed bone, connective tissue, and remaining graft material particles. The use of InduCera or Bio-Oss resulted in 21.37% or 23.02% of newly formed bone and 30.66% or 30.14% of remaining graft particle, respectively, at 6 months of healing. Studies comparing pure biphasic calcium phosphate and anorganic bovine bone showed that pure biphasic calcium phosphate induced similar or more new bone formation and had a lower percentage of residual graft particles than anorganic bovine bone. Schmitt et al4 found 24.9% of newly formed bone with anorganic bovine bone, whereas 30.28% with biphasic calcium phosphate graft. Froum et al20 found that biphasic calcium phosphate and anorganic bovine bone graft cores revealed a new bone of 28.35% and 22.27%, respectively, without significant differences, and residual graft particles of 28.4% and 26.0%, respectively. The study by Cordaro et al21 reported a similar amount of new bone, whereas less percentage of grafted materials were left in biphasic calcium phosphate. Considering our results and literatures, histological characteristics of calcium phosphate coating on anorganic bovine bone did not seem to act like pure calcium phosphate material but have similarity with anorganic bovine bone.

Graft height reduction using panoramic radiographs showed that alveolar bone height of InduCera 6 months after sinus augmentation were similar with anorganic bovine bone. Studies comparing anorganic bovine bone and beta tricalcium phosphate reported a loss of graft height of 0.94 mm (4.75%) and 1.50 mm (7.7%) 6–8 months after sinus augmentation.22 In another study, the average height of the remaining alveolar bone before the surgery, immediately after the surgery, and 1 year after the surgery was 4.9, 19.0, and 17.2 mm, respectively, in anorganic bovine bone graft and 4.0, 19.2, and 17.8 mm, respectively, in a mixture of demineralized bone matrix and anorganic bovine bone.23 Because of the anorganic bovine bone portion, which resorbed slowly, reduction of alveolar bone height in InduCera seems similar to Bio-Oss.

To evaluate the effect of bone graft materials in maxillary sinus augmentation, recent studies used histological specimens or CBCT, which became a popular technique for diagnosis and design in dental treatment.3–5,24 However, previous studies usually measured the shrinkage rate of the grafted bone, and only a few studies focused on the dimensional changes of the Schneiderian membrane, which might be influenced by the surgery. This study evaluated the volumetric change of the bone graft area and soft-tissue area, which contain membrane swelling and hemorrhagic fill or fluid extravasation inside the graft. It has been reported that Schneiderian membrane undergoes swelling after sinus augmentation25–27; this is because initial bleeding causes vasoactive substance release, leading to primary clot formation, followed by an inflammatory phase that causes membrane swelling.28 Makary et al showed that sinus membrane thickness increased at the first week after surgery and then decreased at 6 months. The thickness was influenced by the graft volume and the membrane thickness immediately after surgery but not by the sinus membrane thickness nor the type of bone substitute.26 On the other hand, Pommer et al27 suggested that membrane reactions differ significantly according to the type of graft material. In this study, soft-tissue volume/total volume after 1 week of sinus augmentation was significantly higher than that of 6 months postoperatively, and the difference between the 2 types of bone graft material was not observed. However, because of the small sample size, it is difficult to conclude the effect of bone graft material on sinus membrane swelling and further study may be necessary.

This study showed a grafted bone volume change after sinus floor augmentation by a 21.88% decrease in InduCera and 7.55% increase in Bio-Oss after 6 months of sinus augmentation. It is still controversial whether the graft volume would be increased or decreased. Mazzocco et al29 compared the 3D volumetric changes immediately and 8–9 months after sinus augmentation with Bio-Oss and found that 90 ± 12% of the initial volume remained after 8–9 months, meaning a graft volume contraction of 10%. On the contrary, Klein et al3 showed an increase in graft volume under the same condition. Our result, 1 case in InduCera and 2 cases in Bio-Oss (n = 6, each group), showed an increased volume, whereas other cases showed decreased volume. A decrease in the graft volume 6 months after surgery seemed rational because of the graft bone resorption and resorption of the blood and fluid that exist between graft materials 7 days postoperatively. In 3 cases in which graft volume increased, if the soft-tissue volumes were added to the grafted bone volume at T1 in this study, the bone volume at T2 decreased in all cases. Recent studies have shown predictable bone formation after membrane elevation without adding any graft materials.30 Increased bone volume in our study also maybe the result of the elevation of the sinus membrane, however, further scientific study is necessary.

This study showed no significant correlation between the percent volume of graft materials that remained after 6 months measured by CBCT and the percentage of mineralized component (new bone + graft material) or the percentage of remaining graft material measured by histomorphometric analysis. Ozyuvaci et al22 reported that tricalcium phosphate, which remained lower in the graft material than anorganic bovine bone in histology, showed more reduced alveolar bone height radiographically without statistical significance. So, it seems hard to find a significant relationship between histomorphometric result and radiographic result, and further study with more number of cases would be necessary.

Data of calcium phosphate double-coated anorganic bovine bone and anorganic bovine bone were not statistically significant, and the Bio-Oss group showed slightly higher mean values. Therefore, it seems that calcium phosphate double coating does not have additive effect in comparison with anorganic bovine bone, although anorganic bovine bone in the test and control group was not the same.

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Calcium phosphate double-coated anorganic bovine bone and anorganic bovine bone grafted for the augmentation of the maxillary sinus showed no significantly different regenerative potential, histomorphometrically. The CBCT image also showed no differences in percentages of soft-tissue swelling inside the maxillary sinus 1 week after operation and volumetric change of the grafted bone after 6 months. Although slightly lower mean values were observed in the percentage of newly formed bone and remaining bone volume after 6 months, these were not statically significant. Pursuant to current findings, although calcium phosphate coating does not have additional effect, calcium phosphate double-coated anorganic bovine bone could be used as the bone graft material in maxillary sinus augmentation.

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Roles/Contributions by Authors

K. -M. Pang: Conceptualization, data analysis, and writing of the manuscript. J. -K. Lee: Clinical investigation. S. -H. Choi: Clinical investigation. Y. -K. Kim: Clinical investigation. B. -J. Kim: Conceptualization, and data analysis. J. -H. Lee: Conceptualization, clinical investigation, review, and editing of the manuscript.

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The authors claim to have no financial interest, either directly or indirectly, in the products or information listed in the article.

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This clinical trial was conducted from November 2011 to November 2016 at 4 hospitals: Seoul National University Dental Hospital, Seoul National University Bundang Hospital, Severance Dental Hospital and Ajou University Hospital (IRB No. CDE11002 at Seoul National University Dental Hospital).

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This research was supported by a grant of the Korea Health Technology R&D Project (HI15C1535) through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea.

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calcium phosphates coating; xenogenic bone; sinus floor augmentation

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