Microarchitecture of the Augmented Bone Following Sinus Elevation with an Albumin Impregnated Demineralized Freeze-Dried Bone Allograft (BoneAlbumin) versus Anorganic Bovine Bone Mineral: A Randomized Prospective Clinical, Histomorphometric, and Micro-Computed Tomography Study

Abstract

Serum albumin has been identified as an endogenous protein that is integral to early bone regeneration. We hypothesized that albumin addition to allografts may result in better bone remodeling than what can be achieved with anorganic xenografts. Sinus elevations were performed at 32 sites of 18 patients with the lateral window technique. Sites either received filling with an anorganic bovine bone mineral (ABBM, BioOss, Geistlich, CH) or albumin impregnated allograft (BoneAlbumin, OrthoSera, AT). After 6-months patients received dental implants and 16 bone core biopsy samples were obtained from the ABBM filled, and 16 from the BoneAlbumin augmented sites. The biopsies were examined by histomorphometry and µCT. Percentage of the residual graft in the BoneAlbumin group was 0-12.7%, median 5.4% vs. ABBM 6.3-35.9%, median 16.9%, p < 0.05. Results of the µCT analysis showed that the microarchitecture of the augmented bone in the BoneAlbumin group resembles that of the native maxilla in morphometric parameters Trabecular Pattern Factor and Connectivity. Our data show that while ABBM successfully integrates into the newly formed bone tissue as persisting particles, BoneAlbumin is underway towards complete remodeling with new bone closely resembling that of the intact maxilla.

Keywords: allograft; bone graft material; histology; histomorphometry; maxillary sinus floor augmentation; x-ray microtomography; xenograft.

Figure 1

Presents pre- and postoperative cone beam computed tomography (cbCT) images of the augmented sinuses in both study groups. (A) preoperative and (B) postoperative images of one of the patients of the BoneAlbumin group, (C) preoperative and (D) postoperative images of one of the patients in the ABBM group. On each image the coronal view is presented on the upper left, the sagittal view is presented on the upper right and the axial view is presented on the lower left window.

Figure 2

Histological assessment of the graft and the newly formed bone tissue. (A) A representative histological section with Hematoxylin-Eosin staining of a bone core biopsy sample harvested from the area augmented using BoneAlbumin. New trabecular bone formation (newly formed bone, nfb) is evident and the intertrabecular space is filled with bone marrow (bm). Only limited acellular graft residues (bone graft particles, bgp) are seen. (B) A corresponding ABBM grafted section. Trabecular new bone (nfb) is present in a similar manner; however, the marrow (bm) is partially filled with the residues of the acellular graft material (bgp). Panel (C) shows the histomorphometry data of the stained sections. Graft residues in the BoneAlbumin group are significantly less than those grafted with ABBM, at the expense of marrow space. Data are presented as median–quartiles–ranges, * represents p < 0.05 with Kruskal Wallis One-way ANOVA test between the two experimental groups, respectively.

Figure 3

Panels (A–C) show representative µCT images of the bone core biopsy samples at the level of the residual native bone of the alveolar ridge (A), the level of the augmented bone grafted using BoneAlbumin (B) and ABBM (C). Bone volume fraction (BV/TV) is still somewhat lower the BoneAlbumin group, while in the ABBM group it is comparable to that of native bone—note that what is calculated as ‘bone’ in this metric contains the unresorbed graft ceramic (D). Trabecular thickness of the BoneAlbumin group has not yet reached the level of that of the native bone (E). Trabecular pattern factor (F) which describe bone geometry is closer to native bone in the BoneAlbumin group than in the ABBM group. Open porosity is still somewhat higher than native in the BoneAlbumin group (G), while connectivity has reached the native level (H). Please note that in these parameters the bone value is a surrogate number for the newly formed bone and the residual graft. * signals p < 0.05 versus native bone.

Figure 3

Panels (A–C) show representative µCT images of the bone core biopsy samples at the level of the residual native bone of the alveolar ridge (A), the level of the augmented bone grafted using BoneAlbumin (B) and ABBM (C). Bone volume fraction (BV/TV) is still somewhat lower the BoneAlbumin group, while in the ABBM group it is comparable to that of native bone—note that what is calculated as ‘bone’ in this metric contains the unresorbed graft ceramic (D). Trabecular thickness of the BoneAlbumin group has not yet reached the level of that of the native bone (E). Trabecular pattern factor (F) which describe bone geometry is closer to native bone in the BoneAlbumin group than in the ABBM group. Open porosity is still somewhat higher than native in the BoneAlbumin group (G), while connectivity has reached the native level (H). Please note that in these parameters the bone value is a surrogate number for the newly formed bone and the residual graft. * signals p < 0.05 versus native bone.