Injectable calcium phosphate cement as a filler for bone defects around oral implants: an experimental study in goats

The aim of this study was to evaluate the clinical applicability and biological behavior of a newly developed injectable calcium phosphate (Ca-P) cement as bone filler for gaps around oral implants. Twenty-four step-like implants, creating gaps of 1 and 2 mm, were inserted into the trabecular bone of the medial femoral condyles of six goats. Four different situations were tested: (1) implant + gaps; (2) implant + gaps, but covered with a polylactic acid membrane; (3) implant + gaps that were filled with Ca-P cement; and (4) implant + gaps that were filled with Ca-P cement and covered with a membrane. All implants were left in place for 12 weeks. Histological and quantitative histomorphometrical measurements demonstrated that implants + gaps had generally poor bone contact at the implant base. Furthermore, fibrous encapsulation was observed in the gap part. In contrast, the presence of a membrane promoted bone ingrowth into the gap and also the bone contact at the implant base. Injection of Ca-P cement resulted in an almost complete filling of the gaps around the implant. The cement surface was completely covered by bone. Active resorption and remodeling of cement particles was observed, suggesting a pattern of slow resorption associated with full replacement with newly formed bone. Additional use of a membrane did not result in adjunctive benefits. Bone-to-implant contact at the implant base was comparable with the implants provided only with a membrane. In conclusion, the Ca-P cement used here showed excellent clinical handling properties combined with a superior bone behavior. On the other hand, the degradation rate of the material was still very slow. This current characteristic can hamper the final clinical applicability of the material as gap filler for periimplant or periodontal defects.     

Ridge augmentation and maxillary sinus grafting with a biphasic calcium phosphate: histologic and histomorphometric observations

Objectives: This retrospective study reports on histologic and histomorphometric observations performed on human biopsies harvested from sites augmented exclusively by biphasic calcium phosphate [BCP: hydroxyapatite (HA)/ tricalcium phosphate (TCP) 60/40] and healed for a minimum of 6 months.
Materials and methods: Five patients benefited from three augmentation regimens (i.e.: one-stage lateral augmentation; two-stage lateral augmentation; and two-stage sinus grafting). In all patients, a degradable collagen membrane served as a cell-occlusive barrier. Core biopsies were obtained from lateral as from crestal aspects 6–10 months after augmentation surgeries. For histologic and histomorphometric evaluations, the non-decalcified tissue processing was performed.
Results: The histological examination of 11 biopsies showed graft particles frequently being bridged by the new bone, and a close contact between the graft particles and newly formed bone was seen in all samples. The mean percentages of newly formed bone, soft tissue compartment, and graft material were 38.8% (±5.89%), 41.75% (±6.08%), and 19.63% (±4.85%), respectively. Regarding bone-to-graft contact values, the percentage of bone coverage of graft particles for all biopsies ranged from 27.83% to 80.17%. The mean percentage of bone coverage was 55.39% (±13.03%).
Conclusions: Data from the present study demonstrated osteoconductivity scores for the BCP material (HA/TCP 60/40) in patients resembling those previously shown for grafting materials of xenogenic and alloplastic origin.     

Bioactive glass granules as a bone adjunctive material in maxillary sinus floor augmentation

OBJECTIVES: Bilateral sinus floor augmentation procedure was performed in 17 patients to study the effect of bioactive glass (BG) granules mixed with autologous bone (AB) chips on bone regeneration. The posterior part of 17 maxillary sinus was augmented with a 1:1 mixture of BG granules (phi 800-1000 microm) and AB chips harvested from the iliac crest (BG-AB group). The anterior parts of the same sinus and the contralateral sinus, serving as a control (AB group), were filled with AB chips alone. Trephine biopsies for histological, scanning electron microscopy (SEM), and energy dispersive X-ray (EDX) analyses were taken from the posterior part of the sinus after 21-34 weeks at the time of insertion of dental implants. Additionally, six biopsies were taken from the BG-AB group and four biopsies were taken from the AB group in connection with abutment operation at 49-62 weeks. RESULTS: Histological evaluation revealed lamellar bone growth in all the specimens. Although most of the BG granules were without bone contact in the majority of the patients in the BG-AB group, the bone lamellae were thicker than observed in the AB group. In the contact areas, bone was growing along the glass surface connecting the particles together. Histomorphometrical analysis carried out from the SEM images at 21-34 weeks revealed 26% and 25% bone in the BG-AB and the AB group, respectively. Corresponding figures for 49-62 weeks were 29% for the BG-AB group and 25% for the AB group. Bone-BG complex, i.e. the granules with intimate contact with bone, occupied 34% of the area measured at 21-34 weeks and 31% at 49-62 weeks. EDX analysis showed a tight contact and chemical bonding between the glass and bone. As a sign of dissolution, a few small Si-depleted areas were present in some BG granules at 21-34 weeks, while more and larger Si-free areas were observed in the granules at 49-62 weeks. CONCLUSION: The results indicate that BG granules (S53P4) can be used together with AB chips for sinus floor augmentation procedure, thus decreasing the amount of bone needed. Further studies concerning especially the biomechanical properties of the BG-AB complex with dental implants are needed.     

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.     

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.     

Back‐scattered electron imaging and elemental analysis of retrieved bone tissue following sinus augmentation with deproteinized bovine bone or biphasic calcium phosphate

Objectives: To compare resorption of a synthetic biphasic calcium phosphate (BCP) bone–graft substitute with deproteinized bovine bone (DBB) used for human maxillary sinus augmentation. Materials and methods: Eleven patients underwent bilateral maxillary sinus floor augmentation with DBB in one side and a BCP (40%β‐tricalcium phosphate (β‐TCP) and 60% hydroxyapatite) in the contralateral side. Simultaneously, with the augmentation on each side a microimplant was placed vertically from the top of the alveolar crest penetrating the residual bone and the grafting material. Eight months after initial surgery the microimplants were retrieved with a surrounding bone core. The composition of residual graft material and surrounding bone was analysed by scanning electron microscopy and energy dispersive X‐ray spectroscopy. Results: Residual graft material of both types was present as 10–500 μm particles in direct contact with, or completely surrounded by, newly formed bone; smaller particles were also present in non‐mineralized tissue. In the case of BCP the bone–graft substitute interface showed evidence of superficial disintegration of particles into individual grains. Median Ca/P ratios (at.%), determined from >200 discreet sites within residual graft particles and adjacent bone, were: DBB: 1.61 (confidence interval [CI] 1.59–1.64); BCP: 1.5 (CI 1.45–1.52); DBB‐augmented bone: 1.62 (CI 1.59–1.66); BCP‐augmented bone: 1.52 (CI 1.47–1.55); P=0.028 for DBB vs. BCP and DBB‐ vs. BCP‐augmented bone. The reduction in Ca/P ratio for BCP over the healing period is consistent with the dissolution of β‐TCP and reprecipitation on the surface of calcium‐deficient hydroxyapatite. Conclusion: The β‐TCP component of BCP may be gradually substituted by calcium‐deficient hydroxyapatite over the healing period. This process and superficial degranulation of BCP particles may influence the progress of resorption and healing. To cite this article:
Lindgren C, Hallman M, Sennerby L, Sammons R. Back‐scattered electron imaging and elemental analysis of retrieved bone tissue following sinus augmentation with deproteinized bovine bone or biphasic calcium phosphate.
Clin. Oral Impl. Res. 21 , 2010; 924–930.
doi: 10.1111/j.1600‐0501.2010.01933.x     

Porous titanium granules used as osteoconductive material for sinus floor augmentation: a clinical pilot study

Background: Resorption of grafting material may lead to unpredictable long‐term results when rehabilitating the resorbed posterior maxilla. Nonresorbable, osteoconductive bone substitutes may therefore be an advantage over autogenous bone grafts. Purpose: The aim of the present pilot study was to test titanium granules as bone substitute in patients planned for augmentation of the sinus floor prior to or in conjunction with placement of dental implants. Materials and Methods: Sixteen patients with uni‐ or bilateral edentulism and need for augmentation of the sinus floor were included in the study. Residual bone height was 2 to 5 mm. Grafting and installation of the dental implants (18 fixtures) was carried out in the same session if primary stability of the implants could be achieved (12 patients). A staged protocol with implant placement 3 to 7 months after the augmentation procedure was used when primary implant stability was impossible to achieve (four patients). In all, 23 TiOblast? (Astra Tech AB, Mölndal, Sweden) implants were installed. Results: The patients have been followed 12 to 36 months after prosthetic loading. Three implants were found mobile and were removed (13.0%). Two of these were in patients where grafting and implant installation were carried out in separate procedures. The implants were found mobile at abutment connection and were removed. One patient in the single‐stage group had a postoperative sinus infection, which was successfully treated with antibiotics. However, one out of two implants in this patient was found mobile and was removed after 1 year in function. Conclusions: In the present study, titanium granules seem to function as augmentation material in the sinus floor. It is, however, not clear if the material can be safely used for two‐stage procedures. Further investigations with longer healing time before implant installation are required. Also, the possible risk of granule displacement during preparation of the fixture site should be further investigated. Additionally, biopsies from patients are requested to confirm any bone ingrowth between the granules.     

Influence of platelet-rich plasma on a bioglass and autogenous bone in sinus augmentation. An explorative study

Platelet-rich plasma (PRP) has been introduced to the field of oral and maxillofacial surgery for a decade, but its beneficial effects on maxillary sinus augmentation remain unclear. The aim of this study was to evaluate the short- and long-term effects of PRP on osseointegration following single-stage sinus augmentation in a randomized prospective animal study. The maxillary premolars of 24 minipigs were extracted bilaterally and allowed to heal for 2 months. Consecutively all animals underwent bilateral sinus floor elevation using autogenous bone, Biogran as well as a combination of the materials with PRP. Three dental implants (Ankylos, Dentsply Co., Mannheim, Germany) were installed in each sinus simultaneously. Four animals were sacrificed at each period of observation (1, 2, 8 and 12 months). Microradiographic images of the specimens were made for quantitative evaluation of the bone-implant contact (BIC) and light microscopic images were made for qualitative analysis. An increment of the BIC during the observation time could be seen over the observation time in all groups. Autogenous bone exhibited a level of BIC from 25.1 +/- 9.96% at 1 month to 55.1 +/- 13.10% at 12 months; on adding PRP, the BIC ranged from 28.4 +/- 4.64% to 52.5 +/- 17.06%. Biogran with and without PRP led to BIC levels from 16.3 +/- 4.64% to 37.6 +/- 16.40% and 21.7 +/- 4.33% to 46.6 +/- 19.37%, respectively. The results of this study did not show a significantly positive effect of PRP on the BIC following sinus augmentation in both groups.     

The use of autologous venous blood for maxillary sinus floor augmentation in conjunction with sinus membrane elevation: an experimental study

Background: There have been reports of successful bone formation with sinus floor elevation induced by simply elevating the maxillary sinus membrane and filling the sinus cavity with a blood clot. Purpose: We investigated the feasibility of maxillary sinus floor augmentation using the patient's own venous blood in conjunction with a sinus membrane elevation procedure. Materials and methods: An implant that protruded 8 mm into the maxillary sinus after sinus membrane elevation was placed in the maxillary sinus of six adult female mongrel dogs. The resulting space between the membrane and the sinus floor was filled with autologous venous blood retrieved from each dog. The implants were left in place for 6 months. Results: During the experimental period, the created space collapsed and the sinus membrane fell down onto the implant. A small amount of new bone formation occurred in the space created by the collapsed membrane. The average height of newly formed bone around the implants in the sinus was 2.7±0.7 mm on the buccal side and 0.6±0.3 mm on the palatal side. Conclusion: The results of this pilot study indicate that blood clots do not have sufficient integrity to enable the sinus membrane to remain in an elevated position for therapeutically effective periods of time. Accordingly, it is recommended that this method be used only when a small aount of new bone formation is necessary around implants in the maxillary sinus cavity. To cite this article:
Kim H‐R, Choi B‐H, Xuan F, Jeong S‐M. The use of autologous venous blood for maxillary sinus floor augmentation in conjunction with sinus membrane elevation: an experimental study.
Clin. Oral Impl. Res. 21 , 2010; 346–349.
doi: 10.1111/j.1600‐0501.2009.01855.x     

Histological and histomorphometric analyses of calcium phosphate cement in rabbit calvaria

PURPOSE: To assess bone regeneration in critical sized defects in the rabbit calvarium, filled with the bone substitute calcium phosphate cement. MATERIAL AND METHODS: Circular bone defects (8mm) were made in both parietal bones of 10 rabbits. One of the defects was filled with the calcium phosphate cement, and the other received autogenous bone harvested from the calvaria. The animals were killed at 3 or 6 weeks (n=5). Data analysis included qualitative assessment of the calvarial specimens and histomorphometric analysis was used to quantify the amount of new bone within the defects. RESULTS: The microscopic analysis of the samples showed bone healing with both calcium phosphate cement and autogenous bone graft. Data obtained from the histomorphometric analysis were statistically analyzed using 2-way analysis of variance and the Tukey's test. Data analysis showed that the autogenous bone graft had significantly more new bone compared with calcium phosphate cement at 3 and 6 weeks. Calcium phosphate cement at 6 weeks presented similar results to autogenous bone at 3 weeks. Both treatments presented an increase in bone healing with time. CONCLUSION: Treatments allowed bone regeneration that increased with time, however surgical cavities treated with the autogenous graft had more bone formation than those with calcium phosphate cement.     

Parietal bone as graft material for maxillary sinus floor elevation: structure and remodeling of the donor and of recipient sites

Particulate parietal bone is used for maxillary sinus floor elevation procedure prior to dental implant placement. However, data on internal structure of the parietal bone and on graft remodeling and incorporation in the host bone are limited. We determined the structure and remodeling activities of 24 parietal bone specimens sampled at time of sinus grafting (T1 samples), and the amount and turnover of bone formed at the recipient site at time of implant placement (T2 samples, obtained 10 months after T1 samples, on average). In T1 samples, the outer cortex was 1.16+/-0.45 mm thick, had a typical haversian structure, and showed a low level of remodeling. In the cancellous portion of the samples, trabecular bone volume represented 52.8+/-10.3%. Bone remodeling was more active in the cancellous portion than in the cortical portion, but few osteoblasts and osteoclasts were seen. T2 samples consisted solely of trabecular bone, which occupied 49.4+/-18.4% of total sample volume. The boundary between new bone and the recipient bed was not discernible. Remnants of the graft particles were embedded within new bone, and showed signs of intense resorption. Bone remodeling was highly active, as shown by the presence of numerous osteoclasts resorbing new bone, together with thick osteoid seams and large osteoblasts. A loose cotton-like mineralized material was frequently observed in the marrow spaces; this acellular and non-collagenous material was strongly stained by toluidine blue, suggesting a glycoprotein nature. This study offers insights into cortical and trabecular bone structure and shows the low-level remodeling activity of parietal bone. About 10 months after grafting, the grafted chips were incorporated in new bone and almost completely resorbed. This high turnover may be beneficial for implant placement.     

Histomorphometric comparison of maxillary pristine bone and composite bone graft biopsies obtained after sinus augmentation

Introduction: Sinus grafting is a technique oriented to facilitate implant placement in posterior atrophic maxillae. Several modifications of the original technique and a wide variety of materials have been proposed; most of them associated with implant survival rates. However, the quality of the bone obtained after the application of certain grafting materials has not been fully elucidated yet. The aims of this multicenter study were to analyse histomorphometrical samples obtained 6 months after sinus grafting using a composite graft consisting of anorganic bovine bone (ABB)+ autologous bone (AB), and to compare these samples with maxillary pristine bone biopsies. Material and methods: Ninety maxillary sinus augmentations were performed for delayed implant placement (N=90) in 45 consecutive patients (test group). Bone cores were harvested 6 months after grafting for histomorphometric and ultrastructural study. Control pristine bone biopsies were taken from the posterior maxilla of 10 patients (control). Bone radiographic changes were assessed up to 24 months after implant loading. Results: The total mean values after analysis of test cores revealed a proportion of 46.08±16.6% of vital bone, 42.27±15.1% of non‐mineralized connective tissue, and 37.02±25.1% of the remaining ABB particles. Significant bone remodeling activities were noticed in sinus grafting samples when compared with pristine bone. A statistically significant difference was observed in the number of osteoid lines between two groups, with higher values in the test one (15.1±11.48% vs. 2.5±2.2%, P=0.0005). Ultrastructural study showed that vital trabecular bone was in intimal contact with ABB particles. Radiographic analysis revealed that the higher the proportion of remaining ABB, the lower the total vertical resorption of the graft. Conclusion: Sinus grafting constitutes an excellent model for the study of de novo bone formation patterns and graft consolidation, when a combination of different bone substitutes is applied. The combination of ABB+AB yields highly satisfactory outcomes from both a clinical and a histologic perspective. To cite this article:
Galindo‐Moreno P, Moreno‐Riestra I, Ávila G, Fernández‐Barbero JE, Mesa F, Aguilar M, Wang H‐L, O'Valle F. Histomorphometric comparison of maxillary pristine bone and composite bone graft biopsies obtained after sinus augmentation.
Clin. Oral Impl. Res. 21 , 2009; 122–128.     

Development of a nonrigid, durable calcium phosphate cement for use in periodontal bone repair

BACKGROUND: Calcium phosphate cement (CPC) hardens in situ to form hydroxyapatite and has been used in dental and craniofacial restorative applications. However, when CPC was used in periodontal osseous repair, tooth mobility resulted in the fracture and exfoliation of the brittle CPC implant. The objective of the authors' study was to develop a strong and nonrigid CPC to provide compliance for tooth mobility without fracturing the implant. METHODS: The authors used tetracalcium phosphate, dicalcium phosphate anhydrous and biopolymer chitosan to develop a strong and nonrigid CPC. They used a powder:liquid ratio of 2:1, compared with the 1:1 ratio of a previously developed nonrigid CPC control. Specimens were characterized using a flexural test, scanning electron microscopy and powder X-ray diffraction. RESULTS: After 28 days of immersion, the new cement had a flexural strength (mean +/- standard deviation; n = 6) of 5.2 +/- 1.0 megapascals, higher than 1.8 +/- 1.5 MPa for the control (P < .05) and overlapping the reported strengths of sintered hydroxyapatite implants and cancellous bone. This cement showed a high ductility with a strain at peak load of 6.5 +/- 1.3 percent, compared with 4.4 +/- 1.9 percent for the control; both were 20-fold higher than the 0.2 percent of the conventional CPC. Nanosized hydroxyapatite crystals, similar to those in teeth and bones, were formed in the cements. CONCLUSIONS: The new nonrigid cement, containing nanohydroxyapatite crystals, possessed a high ductility and superior fracture resistance. This strong, tough and nonrigid CPC may be useful in periodontal repair to provide compliance for tooth mobility without fracture. CLINICAL IMPLICATIONS: The results of this study may yield the first self-hardening and nonrigid hydroxyapatite composite with high strength and durability and large deformation capability to be useful in the regeneration of periodontal osseous defects.