Comparative Histological and Histomorphometric Results of Six Biomaterials Used in Two-Stage Maxillary Sinus Augmentation Model after 6-Month Healing

Abstract

Objectives: To evaluate the performances of six different bone substitute materials used as graft in maxillary sinus augmentation by means of histological and histomorphometric analysis of bone biopsies retrieved from human subjects after a 6-month healing period.

Materials and methods: Six consecutive patients (3 males, 3 females, aged 50-72 years), healthy, nonsmokers, and with good oral hygiene, presenting edentulous posterior maxilla with a residual bone crest measuring ≤ 4 mm in vertical height and 3 to 5 mm in horizontal thickness at radiographic examination, were selected to receive sinus augmentation and delayed implant placement. Under randomized conditions, sinus augmentation procedures were carried out using mineralized solvent-dehydrated bone allograft (MCBA), freeze-dried mineralized bone allograft (FDBA), anorganic bovine bone (ABB), equine-derived bone (EB), synthetic micro-macroporous biphasic calcium-phosphate block consisting of 70% beta-tricalcium phosphate and 30% hydroxyapatite (HA-β-TCP 30/70), or bioapatite-collagen (BC). After 6 months, bone core biopsies were retrieved and 13 implants were placed. Bone samples were processed for histological and histomorphometric analysis. CT scans were taken before and after surgery. After 4 months of healing, patients were restored with a provisional fixed acrylic resin prosthesis, as well as after further 2-4 months with a definitive cemented zirconia or porcelain-fused-to-metal crowns.

Results: There were no postoperative complications or implant failures. The histological examination showed that all biomaterials were in close contact with newly formed bone, surrounding the graft granules with a bridge-like network. No signs of acute inflammation were observed. The histomorphometry revealed 20.1% newly formed bone for MCBA, 32.1% for FDBA, 16.1% for ABB, 22.8% for EB, 20.3% for HA-β-TCP 30/70, and 21.4% for BC.

Conclusions: Within the limitations of the present investigation, all the six tested biomaterials showed good biocompatibility and osteoconductive properties when used in sinus augmentation procedures, although the FDBA seemed to have a better histomorphometric result in terms of newly formed bone and residual graft material. This trial is registered with ClinicalTrials.gov Identifier (Registration Number): NCT03496688.

Figures

Figure 1

Intraoperative views of the sinus augmentation procedure: (a) mobilization of the mucoperiosteal flap; (b) oval-shaped bony window; (c) sinus membrane elevation; (d) graft material in place; (e) resorbable membrane over the lateral window; (f) suture; (g) bone core biopsy and implant placement; (h) trephine bur and harvested specimen; (i) suture.

Figure 2

Radiographic evaluation: (a) CT scan before surgery; (b) CT scan after 6 months of graft healing; (c) CT scan after implant placement.

Figure 3

Mineralized solvent-dehydrated bone (toluidine blue and acid fuchsin): (a) trabecular bone with large marrow spaces and biomaterial particles was observed (original magnification 12X); (b) the biomaterial particles showed different sizes and they were partially surrounded by newly formed bone that was characterized by large osteocyte lacunae (original magnification 40X).

Figure 4

Freeze-dried mineralized bone allograft (toluidine blue and acid fuchsin): (a) newly formed bone with marrow spaces and particles of residual biomaterial was present. In a marginal portion of the sample, preexisting bone with small remodeling areas could be observed (original magnification 12X); (b) the biomaterial particles, showing areas of bone neoformation in their inner part, could be observed. Some of the biomaterial particles showed irregular margins, typical of a resorption process (original magnification 40X).

Figure 5

Anorganic bovine bone (toluidine blue and acid fuchsin): (a) the specimen appeared to be constituted by two separate fragments, where several particles of residual biomaterial were evident (original magnification 12X); (b) the areas of bone neoformation in tight contact with the biomaterial surface were present. In some fields, new bone formation inside the biomaterial particles could be observed (original magnification 40X).

Figure 6

Equine-derived bone (toluidine blue and acid fuchsin): (a) trabecular bone with large marrow spaces and biomaterial particles was observed. The biomaterial particles were located in the apical portion of the biopsy and they were surrounded by new bone (original magnification 12X); (b) the bone was in close contact with the granules and in some areas osteoblasts were observed in the process of apposing bone directly on the particle surface (original magnification 40X).

Figure 7

Synthetic micro-macroporous biphasic calcium-phosphate (HA-β-TCP 30/70) (toluidine blue and acid fuchsin): (a) trabecular bone with marrow spaces and residual biomaterial, located in the apical portion of the sample, could be observed (original magnification 12X); (b) the residual biomaterial was surrounded by newly formed bone and no gaps were present at the bone biomaterial interface. In some fields, the graft seemed to undergo resorption. Many large blood vessels could be seen (original magnification 40X).

Figure 8

Bioapatite-collagen (toluidine blue and acid fuchsin): (a) trabecular bone with marrow spaces and residual biomaterial particles was observed (original magnification 12X); (b) osteoblasts were observed in the process of apposing bone directly on the particle surface. Marrow spaces were colonized by small and large blood vessels in close proximity to the new bone and to the particles (original magnification 40X); (c) moderate inflammatory infiltrate and multinucleated giant cells, probably osteoclasts, were observed directly on the biomaterial particles surface (original magnification 400X).