Maxillary sinus floor augmentation with Bio-Oss or Bio-Oss mixed with autogenous bone as graft: a systematic review

Aims: The objective of the present systematic review was to test the hypothesis of no differences in the implant treatment outcome when Bio‐Oss or Bio‐Oss mixed with autogenous bone is used as graft for the maxillary sinus floor augmentation (MSFA) applying the lateral window technique. Material and methods: A MEDLINE (PubMed) search in combination with a hand search of relevant journals was conducted by including human studies published in English from January 1, 1990 to June 1, 2010. The search provided 879 titles and 35 studies fulfilled the inclusion criteria. Considerable variation in the included studies prevented meta‐analysis from being performed and no long‐term study comparing MSFA with the two treatment modalities was identified. Also, the survival of suprastructures after the two augmentation procedures was not compared within the same study. Results: The 1‐year implant survival was compared in one study demonstrating no statistically significant difference. The implant survival was 96% with Bio‐Oss and 94% with a mixture of 80% Bio‐Oss and 20% autogenous mandibular bone. Addition of a limited amount of autogenous bone to Bio‐Oss seemed not to increase the amount of new bone formation and bone‐to‐implant contact compared with Bio‐Oss. Conclusions: Therefore, the hypothesis of no differences between the use of Bio‐Oss or Bio‐Oss mixed with autogenous bone as graft for MSFA could neither be confirmed nor rejected. To cite this article : Jensen T, Schou S, Stavropoulos A, Terheyden H, Holmstrup P. Maxillary sinus floor augmentation with Bio‐Oss or Bio‐Oss mixed with autogenous bone as graft: a systematic review. Clin. Oral Impl. Res. 23, 2012; 263–273
doi: 10.1111/j.1600‐0501.2011.02168.x     

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     

Implant treatment in combination with lateral augmentation of the alveolar process: a 3-year prospective study

Background: In patients in whom the height of the alveolar process is adequate but the crest is too narrow to host an implant, lateral augmentation is required. Such augmentations have mostly been performed using autogenous bone blocks secured to the buccal surface. An alternative to autogenous bone may be bovine hydroxyapatite (Bio‐Oss, Geistlich Pharma AG, Wolhusen, Switzerland) or other bone substitutes. Purpose: The aim of this study was to evaluate the clinical and radiographic outcome of dental implants inserted after lateral augmentation of too narrow alveolar processes with a combination of bovine hydroxyapatite (Bio‐Oss) and autogenous bone. Methods: Thirty patients (14 males and 16 females) with a mean age of 41.6 years fulfilled the inclusion criteria. Twenty‐nine augmentation sites with a total of 74 implants could be followed for 3 years. Results: Three implants were lost; these were lost before loading (at the abutment operation). The survival rate was 95.9%. The mean marginal bone loss during the 3‐year observation period was 0.3 ± 0.2 mm. Conclusions: A 50/50 combination of Bio‐Oss and autogenous bone chips stabilized with Tisseel (Baxter AG/Duo Quick AG, Vienna, Austria) was useful for lateral augmentation of the alveolar crest. Lateral grafts with Bio‐Oss, autogenous bone, and Tisseel made it possible to achieve good implant stability and high implant survival results. The bone level changes adjacent to the implants were the same as in nongrafted cases.     

Apical and marginal bone alterations around implants in maxillary sinus augmentation grafted with autogenous bone or bovine bone material and simultaneous or delayed dental implant positioning

Objective: A re‐pneumatization phenomenon was recorded in sinuses grafted with different materials. The specific aims of this paper were to assess the dental implant survival rate and the behavior of marginal and apical bone remodeling around dental implants placed following sinus augmentation. Materials and methods: A retrospective study was conducted on consecutive patients treated in two surgical centers. Different surgical techniques were adopted for sinus augmentation: simultaneous or delayed dental implant insertion with bovine bone‐material augmentation or autologous bone grafting (chin and iliac crest). Survival rates were recorded for the overall number of implants (patients of group A). Apical and marginal bone levels (ABL and MBL, respectively) were radiographically measured, and statistical analysis was performed in implants of a subgroup of patients (group B). Results: A total of 282 dental implants were positioned. Recorded cumulative survival rates (CSRs) were 95.6% and 100% for autogenous and bovine bone material, respectively, while CSRs at 2‐year follow‐up for immediate and delayed procedures were 99.3% and 96.5%. For the subgroup B, 57 sinus augmentation procedures were performed in 39 patients, with the positioning of 154 implants. Generally, the apical‐ and marginal‐bone resorption of the bovine bone‐material group was less than that of the autogenous group. The differences between the ABL values of the bovine bone‐material and iliac‐crest groups were statistically significant at 1 year, whereas this significance disappeared at the 2‐year follow‐up; tests showed that a statistical difference was recorded in the bovine bone‐material group between the 1‐ and 2‐year follow‐ups. With regard to MBL comparisons between simultaneous and delayed implantation, the differences maintained their significance at the 2‐year follow‐up also. Conclusions: Differences regarding apical bone alteration between autogenous bone from the iliac crest and bovine bone material at the 1‐ and 2‐year follow‐ups, as well as in the bovine bone‐material group between the 1‐ and 2‐year follow‐ups, attested to slower but more prolonged physiologic bone remodeling in the bovine‐graft‐material group than in the autogenous‐bone group. The MBL analysis showed that remodeling in the delayed implant group demonstrated a greater resorption in the cervical portion than was seen in the simultaneous implant group. To cite this article:
Sbordone L, Levin L, Guidetti F, Sbordone C, Glikman A, Schwartz‐Arad D. Apical and marginal bone alterations around implants in maxillary sinus augmentation grafted with autogenous bone or bovine bone material and simultaneous or delayed dental implant positioning.
Clin. Oral Impl. Res 22 , 2011; 485–491
doi: 10.1111/j.1600‐0501.2010.02030.x     

Primary implant stability after maxillary sinus augmentation with autogenous mesenchymal stem cells: a biomechanical evaluation in rabbits

Objectives: To mechanically evaluate the effect of transplantation of precultured preosteoblasts derived from autogenic adult mesenchymal stem cells (aMSC) for experimental sinus floor augmentation on primary dental implant stability in comparison with conventional augmentation procedures in rabbits. Material and methods: After experimental sinus floor augmentation with a synthetic bone substitute, autogenous bone transplantation or osteoblast precursor cells, the primary stability of implants inserted in the edentulous part of the upper jaw of New Zealand White Rabbits was examined. Mechanical evaluation was performed by determination of insertion torque values (Osseocare^?), percussion testing (Periotest^?), resonance frequency analysis (Osstell^? and scanning laser Doppler vibrometer) and measurement of extraction forces. Results: Evaluation of mechanical properties with percussion testing and resonance frequency analysis with Osstell^? revealed slightly higher primary stability of the stem cell group whereas the scanning laser Doppler vibrometer and measurement of pull‐out forces showed no significant difference to the bone substitute group. Transplantation of autogenous bone graft resulted in the highest primary implant stability. Conclusions: The three examination modalities proved suitable for the determination of primary implant stability. The experimental maxillary sinus floor augmentation with precultured osteoblast precursor cells from autogenic stems cells clearly enhanced the primary stability of implants compared with the unaugmented sinus and lead to comparable primary mechanical properties to bone substitutes in rabbits. In comparison with the autogenous bone graft stability enhancement by stem cell transplantation declined. To cite this article:
Riecke B, Heiland M, Hothan A, Morlock M, Amling M, Blake FAS. Primary implant stability after maxillary sinus augmentation with autogenous mesenchymal stem cells – biomechanical evaluation in rabbits.
Clin. Oral Impl. Res. 22 , 2011; 1242–1246.doi: 10.1111/j.1600‐0501.2010.02043.x     

Maxillary sinus floor elevation with bovine bone mineral combined with either autogenous bone or autogenous stem cells: a prospective randomized clinical trial

Aim: To assess whether differences occur in bone formation after maxillary sinus floor elevation surgery with bovine bone mineral (BioOss^®) mixed with autogenous bone or autogenous stem cells. The primary endpoint was the percentage of new bone three months after the elevation procedure. Material and methods: In a randomized, controlled split‐mouth design, in 12 consecutive patients (age 60.8 ± 5.9 years, range 48–69 years) needing reconstruction of their atrophic maxilla, a bilateral sinus floor augmentation procedure was performed. Randomly, on one side the augmentation procedure was performed with bovine bone mineral (BioOss^®) seeded with mononuclear stem cells harvested from the posterior iliac crest (test group) while BioOss^® mixed with autogenous bone (harvested from the retromolar area) was applied on the contra‐lateral side (control group). On 14.8 ± 0.7 weeks after the sinus floor elevation, biopsies from the reconstructed areas were taken at the spots where subsequently the endosseous implants were placed. The biopsies were histomorphometrically analyzed. Results: Significantly more bone formation was observed in the test group (17.7 ± 7.3%) when compared with the control group (12.0%± 6.6; P=0.026). In both the test and control group, all implants could be placed with primary stability. In one patient, not all biopsies contained BioOss^®. This patient was excluded from analysis. Conclusion: Mesenchymal stem cells seeded on BioOss^® particles can induce the formation of a sufficient volume of new bone to enable the reliable placement of implants within a time frame comparable with that of applying either solely autogenous bone or a mixture of autogenous bone and BioOss^®. This technique could be an alternative to using autografts. To cite this article: Rickert D, Sauerbier S, Nagursky H, Menne D, Vissink A, Raghoebar GM. Maxillary sinus floor elevation with bovine bone mineral combined with either autogenous bone or autogenous stem cells: a prospective randomized clinical trial.
Clin. Oral Impl. Res. 22 , 2011; 251–258.
doi: 10.1111/j.1600‐0501.2010.01981.x     

Effect of anorganic bovine bone to autogenous cortical bone ratio upon bone remodeling patterns following maxillary sinus augmentation

Introduction: Maxillary sinus augmentation is a predictable implant site development technique, although several local and systemic factors may influence outcomes. The aim of this study was to evaluate healing patterns and bone remodeling activity following the use of two different graft mixtures for maxillary sinus augmentation. Materials and methods: Patients in need of maxillary sinus augmentation were randomly assigned to two different groups. A graft mixture using a 50% autologous bone (AB) to 50% anorganic bovine bone (ABB) ratio was used in group 1, while a 20% AB to 80% ABB ratio was utilized for group 2. After a 6‐month healing period, bone core biopsies were harvested for histological, histomorphometrical, and immunohistochemical analyses. Results: Twenty‐eight subjects participated in this study. No statistically significant differences were found between groups in regards to vital bone and non‐mineralized tissue proportions. Higher number of osteoid lines (18.05 ± 10.06 in group 1 vs. 9.01 ± 7.53 in group 2; P=0.023) and higher cellularity, particularly regarding the number of osteocytes (631.85 ± 607.98 in group 1 vs. 219.08 ± 103.26 in group 2; P=0.002), were observed in specimens from group 1. Differences in expression patterns of osteopontin and tartrate‐resistant acid phosphatase were also detected between groups. Conclusion: AB to ABB ratio appears to influence bone remodeling patterns and cell content following maxillary sinus augmentation procedures. Similar proportion of vital bone was found in specimens obtained from both groups. More cellular presence was observed in samples containing higher proportions of AB. To cite this article:
Galindo‐Moreno P, Moreno‐Riestra I, Avila G, Padial‐Molina M, Paya JA, Wang H‐L, O'Valle F. Effect of anorganic bovine bone to autogenous cortical bone ratio upon bone remodeling patterns following maxillary sinus augmentation.
Clin. Oral Impl. Res. 22 , 2011; 857–864.
doi: 10.1111/j.1600‐0501.2010.02073.x     

Maxillary sinus augmentation with microstructured tricalcium phosphate ceramic in sheep

Objective: The objective of this study was to evaluate the biological performance of osteoinductive microstructured tricalcium phosphate (MSTCP) particles in maxillary sinus floor augmentation surgery in sheep. Material and methods: Sinus floor augmentation was performed in eight Swifter sheep. In each animal, the maxillary sinus floor was unilaterally augmented with MSTCP particles. Computed tomography (CT) imaging and histological analyses were performed after 12 weeks of implantation. Results: Maxillofacial CT, histology, histomorphometrical analysis and sequential polychrome fluorescent labeling indicated that MSTCP particles provided a scaffold for cell ingrowth and bone formation. After a 12‐week implantation period, the sinuses grafted with MSTCP showed an increased bone height of 6 mm and a mean total bone volume of 43%, with significant degradation of MSTCP particles. Conclusion: MSTCP particles represent a suitable bone substitute material for maxillary sinus floor augmentation surgery. To cite this article:
Klijn RJ, Hoekstra JWM, Van Den Beucken JJJP, Meijer GJ, Jansen JA. Maxillary sinus augmentation with microstructured tricalcium phosphate ceramic in sheep.
Clin. Oral Impl. Res. 23 , 2012; 274–280.
doi: 10.1111/j.1600‐0501.2011.02190.x     

Maxillary sinus augmentation with autologous bone harvested from the lateral maxillary wall combined with bovine‐derived hydroxyapatite: clinical and histologic observations

Objective: The aim of this study was to determine the clinical efficacy of a mixture of autologous bone harvested from the lateral wall of the maxilla using bone shavers and bovine‐derived hydroxyapatite (HA) placed as a graft to elevate the maxillary sinus floor. The histological picture of tissue found in the sinus, the survival rate and the success of the implants were all evaluated. Material and methods: A total of 90 titanium implants were placed in 34 patients. In all of them, the lateral maxillary wall was harvested as a particulate bone graft, subsequently mixed with bovine‐derived HA and packed in the sinus cavity. The lateral access window was then covered with a bioresorbable porcine‐derived collagen membrane. In 32 sinuses, a two‐stage surgery was performed, while in the remaining 10 cases a one‐stage surgery was carried out. In the two‐stage approach, 14 randomly selected biopsies were obtained at the time of implant insertion after a healing period of 9 months. The histological specimens were histologically and histomorphometrically evaluated. Results: One implant was lost, leading to a survival rate of 98.9%. The new bone consisted of lamellae of living bone contained osteocytes and in close contact with bovine bone particles that were partly infiltrated by newly formed bone. Bovine bone particle resorption could not be found. The histomorphometric analysis showed the following averages: 29% of newly formed bone and 21% of anorganic bovine bone. The marrow spaces made up the remaining 50% of the specimens. Conclusion: Sinus lift graft with autologous bone harvested from the maxillary lateral wall combined with demineralized bovine bone leads to a predictable outcome regarding the amount of bone formation in sinus floor augmentation. To cite this article:
de Vicente JC, Hernández‐Vallejo G, Braña‐Abascal P, Peña I. Maxillary sinus augmentation with autologous bone harvested from the lateral maxillary wall combined with bovine‐derived hydroxyapatite: clinical and histologic observations.
Clin. Oral Impl. Res. 21 , 2010; 430–438
doi: 10.1111/j.1600‐0501.2009.01877.x     

Histologic analysis of clinical biopsies taken 6 months and 3 years after maxillary sinus floor augmentation with 80% bovine hydroxyapatite and 20% autogenous bone mixed with fibrin glue

Background: Bovine hydroxyapatite (Bio‐Oss®, Geistlich Pharmaceutical, Wollhausen, Switzerland) has been suggested to be used in maxillary sinus floor augmentation procedures prior to or in conjunction with implant placement. However, the long‐term histologic fate of this material is not well understood. Purpose: The aim with this study was to histologically evaluate the tissue response in patients to a mixture of bovine hydroxyapatite (BH), autogenous bone, and fibrin glue 6 months and 3 years after a maxillary sinus floor augmentation procedure. Materials and Method: Biopsies were taken from a group of 20 consecutive patients 6 months (n = 16) and 3 years (n = 12) after maxillary sinus floor augmentation with a mixture of BH (80%), autogenous bone (20%), and fibrin glue and prepared for histologic analysis. Results: Light microscopy and morphometry from biopsies taken after 6 months showed various amounts of mineralized bone tissue. The specimen area was occupied by 54.1 ± 12.6% nonmineralized tissue, followed by 21.2 ± 24.5% lamellar bone, 14.5 ± 10.3% BH particles, and 10.2 ± 13.4% woven bone. The nonmineralized tissue seen in bone‐forming areas consisted of a loose connective tissue, rich with vessels and cells. There were no signs of resorption of the BH particles. The lamellar bone appeared to have originated from the recipient site and was seldom in contact with the BH particles. After 3 years, the nonmineralized tissue area had decreased to 36.0 ± 19.0% (p > .05) and consisted mainly of bone marrow tissue. The surface area of lamellar bone had increased to 50.7 ± 22.8% (p > .05), and there was almost no immature bone. The mean specimen area occupied by BH particles, was 12.4 ± 8.7% and had not changed from 6 months (not significant). Moreover, the sizes of the particles were similar after 6 months and 3 years. The degree of BH particle–bone contact had increased from 28.8%± 19.9% after 6 months to 54.5 ± 28.8% after 3 years (p > .05). Conclusion: Histology of specimens from maxillary sinuses augmented with 80% BH particles, 20% autogenous bone, and fibrin glue showed a positive bone tissue response after 6 months and 3 years after augmentation of the maxillary sinus floor prior to implant placement in a group fo 20 patients. The bone surrounding and in contact with the BH particles after 6 months was mainly immature woven bone, which with time was replaced by mature lamellar bone filling the interparticle space as observed in the 3‐year specimens. Moreover, bone‐integrated BH particles seem to be resistant to resorption. The results indicate that the procedure may be considered when only small amounts of intraoral autogenous bone graft are available.     

Optimal microvessel density from composite graft of autogenous maxillary cortical bone and anorganic bovine bone in sinus augmentation: influence of clinical variables

Objectives: The objectives of this study were to assess the microvessel density (MVD) of intra‐sinus grafts after 6 months of wound healing and to study the relationship between revascularization processes and patient clinical variables and habits. Material and methods: We performed 45 maxillary sinus augmentations with different implant placements in 25 consecutive patients, obtaining bone cores of the grafted area for histological, histomorphometric and immunohistochemical study. Biopsies were also taken from pristine bone in the posterior maxilla (control). Results: All implants survived at 24 months. Biopsies of sinus augmentation areas showed significantly greater remodeling activity vs. pristine bone, with significantly more osteoid lines. The morphometry study revealed 34.88±15.2% vital bone, 32.02±15.1% non‐mineralized tissue and 33.08±25.4% remnant anorganic bovine bone particles. The number of CD34‐positive vessels was 86.28±55.52/mm² in graft tissue vs. 31.52±13.69/mm² in native tissue (P=0.002, Mann–Whitney U=46). The larger amount of non‐mineralized tissue in grafts was directly correlated with a higher MVD (r=0.482, P=0.0001, Pearson's test). MVD was affected by the presence of periodontitis or tobacco and alcohol consumption. Conclusion: The angiogenesis and revascularization obtained by this type of graft achieve adequate tissue remodeling for osseointegration and are influenced by periodontal disease and tobacco or alcohol consumption. To cite this article:
Galindo‐Moreno P, Padial‐Molina M, Fernández‐Barbero JE, Mesa F, Rodríguez‐Martínez D, O'Valle F. Optimal microvessel density from composite graft of autogenous maxillary cortical bone and anorganic bovine bone in sinus augmentation: influence of clinical variables.
Clin. Oral Impl. Res. 21 , 2010; 221–227
doi: 10.1111/j.1600‐0501.2009.01827.x     

Long‐term results after lateral and osteotome technique sinus floor elevation: a retrospective analysis of 2190 implants over a time period of 15 years

Background: During a time period of 15 years (1992–2007), 2190 implants were inserted in 983 patients after sinus floor elevation. Materials and methods: One thousand two hundred and seven implants (461 patients) were placed into sites, in which the sinus was augmented using the lateral approach (LSFE), and 983 implants (522 patients) in sites augmented with the osteotome technique. Bovine bone mineral (n=1217), β‐tricalcium phosphate (n=126), and in some cases, only autogenous bone were used for augmentation in the LSFE. Generally, bone chips that were collected during the preparation of the osteotomy were added to the bone substitutes. No additional augmentation materials were used for augmentation with the osteotome technique. A retrospective analysis of the treatment results was assessed by patients documentations that were recorded in the impDAT(R) – Program and by the evaluation of pre‐, and post‐surgical orthopantomograms. Results: The implant survival analysis according to Kaplan–Meier showed 97.1% after 176 months of loading for both sinus floor elevation techniques. Discussion and conclusion: The evaluation with respect to the augmentation material used did not reveal significant differences in the implant survival rate and in both cases remodelling processes could be observed in the augmented area. To cite this article:
Tetsch J, Tetsch P, Lysek DA. Long‐term results after lateral and osteotome technique sinus floor elevation: a retrospective analysis of 2190 implants over a time period of 15 years.
Clin. Oral Impl. Res. 21 , 2010; 497–503.
doi: 10.1111/j.1600‐0501.2008.01661.x     

Maxillary bone grafting for insertion of endosseous implants: results after 12-124 months

Abstract: Insertion of endosseous implants in the atrophic maxilla is often complicated because of lack of supporting bone. Augmentation of the floor of the maxillary sinus with autogenous bone graft has been proven to be a reliable treatment modality, at least in the short term. The long‐term clinical and radiographic outcome with regard to the grafts, the implants and satisfaction of the patients with their implant‐supported overdenture was studied in 99 patients. The sinus floor was augmented with bone grafts derived from the iliac crest (83 subjects, 162 sinuses, 353 implants), the mandibular symphysis (14, 18, 37), or the maxillary tuberosity (2, 2, 2). Before implant installation, the width and height of the alveolar crest were increased in a first stage procedure in 74 patients, while in the other 25 patients augmentation and implant installation could be performed simultaneously (width and height of the alveolar crest >5 mm). Perforation of the sinus membrane occurred in 47 cases, which did not predispose to the development of sinusitis. Loss of bone particles and sequestration were observed in one (diabetic) patient only, in whom a dehiscence of the oral mucosa occurred. A second augmentation procedure was successful in this patient. Symptoms of transient sinusitis were observed in 3 patients. These symptoms were successfully treated with decongestants and antibiotics. 2 other patients developed a purulent sinusitis which resolved after a nasal antrostomy. In all cases, the bone volume was sufficient for implant insertion. 32 of 392 inserted Brånemark implants (8.2%) were lost during the follow‐up. After the healing period of the bone grafts, no sinus pathology was observed. The patients received implant‐supported overdentures (72 patients) or fixed bridges (27 patients). Overall, the patients were very satisfied with the prosthetic construction. We conclude that bone grafting of the floor of the maxillary sinus floor with autogenous bone for the insertion of implants is a reliable treatment modality with good long‐term results.     

Biodegradation Property of Beta‐Tricalcium Phosphate‐Collagen Composite in Accordance with Bone Formation: A Comparative Study with Bio‐Oss Collagen® in a Rat Critical‐Size Defect Model

Purpose: The objective of this study was to compare osteoconductivity and biodegradation properties of an in‐house fabricated beta‐tricalcium phosphate (b‐TCP)‐collagen composite with those of Bio‐Oss Collagen® (Osteohealth, Shirley, NY, USA) using a rat calvarial critical‐size defect model. Materials and Methods: b‐TCP–collagen composite material was fabricated by mixing b‐TCP granules having a particle size of 0.15 to 0.8 mm and 75% porosity, with bovine dermis‐derived soluble collagen sponge. The dry weight ratio of b‐TCP granules‐to‐collagen ratios was 4:1. Bio‐Oss Collagen or the b‐TCP–collagen composite was used to fill a 5.0 mm–diameter calvarial defect in rats. The defects were evaluated by histological and histomorphological analyses of decalcified histological sections with hematoxylin and eosin staining 6 and 10 weeks, respectively, after surgery. Results: The defect implanted with the b‐TCP composite contained immature bone structures with dense connective tissue in contrast to the abundant fibrous tissue, but no trabecular structure was observed within the defect implanted with Bio‐Oss Collagen at 6 weeks postoperatively. Eventually, the defect filled with the b‐TCP composite was covered with dense, continuous, mature bone tissue with complete replacement of the graft material. However, in defects filled with Bio‐Oss Collagen, only dense connective tissue, containing limited amounts of immature trabecular bone and abundant remnant Bio‐Oss particles, was observed. Histomorphological analysis revealed that the b‐TCP composite caused greater tissue augmentation with a larger volume of bone tissue observed in the defect and greater bioabsorption of remnant material than Bio‐Oss Collagen. Conclusion: These results indicated that the b‐TCP composite has greater osteoconductivity and better biodegradation properties than Bio‐Oss Collagen; these properties of the b‐TCP–collagen composite complimented bone formation and remodeling.     

Atrophic maxillary floor augmentation by mineralized human bone allograft in sinuses of different size: an histologic and histomorphometric analysis

Objective: The aims of this work were to histologically examine the healing of mineralized human bone allograft (MHBA) in sinus augmentation for elevating a severe maxillary atrophy ridge (≤2 mm residual ridge height) and to correlate the results to the sinus cavity size. Material and methods: A two‐stage protocol was conducted in 23 patients, all having crestal bone ≤2 mm. A mixture of 80/20 cortical/cancellous of MHBA particles was used to augment sinus using the lateral window approach in narrow (NS; <15 mm bucco‐palatal distance) and wide (WS; ≥15 mm bucco‐palatal distance) sinuses, based upon computerized tomography (CT) assessment. A bone core biopsy was taken at implant placement, 6 and 9 months after surgery. Microradiography, histology and histochemistry of methacrylate‐embedded sections were performed to analyze and to evaluate the bone and graft amount. Results: Newly formed bone around MBHA particles was found in all 28 biopsies. Bone showed a woven structure at 6 months after surgery and a lamellar structure 9 months after surgery. At 6 months after surgery, the 13 NS and 15 WS had 30.5±8.8% and 20.7±4.9% mean±SD bone formation, respectively. At 9 months after surgery, it was 38.8±7% (NS) and 30.7±3% (WS). Residual graft was about 16% (6 months) and 6% (9 months), in both NS and WS. The Mann–Whitney test showed a greater bone formation in NS than in WS (P<0.005). Conclusions: The used 80/20 MHBA mixture appears to promote, in the severe atrophic maxilla, a satisfactory bone formation. Our results prove that the larger the sinus, the longer the maturation time needed to achieve a suitable amount of new bone formation. To cite this article:
Maria Soardi C, Spinato S, Zaffe D, Wang H‐L. Atrophic maxillary floor augmentation by mineralized human bone allograft in sinuses of different size: an histologic and histomorphometric analysis.
Clin. Oral Impl. Res. 22 , 2011; 560–566
doi: 10.1111/j.1600‐0501.2010.02034.x     

Histological evaluation of healing after transalveolar maxillary sinus augmentation with bioglass and autogenous bone

Objectives: The aim was to evaluate histologically the outcome of a bioglass and autogenous bone (at 1 : 1 ratio) composite implantation for transalveolar sinus augmentation. Methods: In 31 patients, during implant installation ca. 4 months after sinus augmentation, biopsies were harvested through the transalveolar osteotomy by means of a trephine bur and non‐decalcified sections through the long axis of the cylinder were produced. After a strict selection process, taking into account the presurgical residual bone height and biopsy length, 8 and 15 biopsies representing the new tissues formed inside the sinus and the transalveolar osteotomy, respectively, qualified for analysis. The tissue fractions occupied by newly formed bone (mineralized tissue+bone marrow), soft connective tissue, residual biomaterial+empty spaces, and debris inside the sinus cavity or the transalveolar osteotomy were estimated. Results: Bone and connective tissue fraction in the newly formed tissues inside the sinus cavity averaged 23.4 ± 13.2% and 54.1 ± 23.5%, respectively. Residual biomaterial, empty spaces, and debris averaged 1.9 ± 3.5%, 10.5 ± 6.3%, and 8.4 ± 14.5%, respectively. In the transalveolar osteotomy, bone and connective tissue fraction averaged 41.6 ± 14.3% and 46.1 ± 13%, respectively, while the amount of residual biomaterial, empty spaces, and debris was 2.8 ± 5%, 4.7 ± 1.9%, and 3.2 ± 2.6%, respectively. Statistically significant differences between the sinus cavity and the transalveolar osteotomy were found only for bone and empty spaces' values (P=0.02 and 0.04, respectively). Conclusion: Sinus augmentation with a bioglass and autogenous bone composite is compatible with bone formation that, in a short distance from the floor of the sinus, shows similar density as that reported previously for other commonly used bone substitutes. New bone fraction inside the transalveolar osteotomy was almost twice as much as in the sinus cavity, while the amount of residual biomaterial was much less than that inside the sinus. To cite this article :
Stavropoulos A, Sima C, Sima A, Nyengaard J, Karring T, Sculean A. Histological evaluation of healing after transalveolar maxillary sinus augmentation with bioglass and autogenous bone.
Clin. Oral Impl. Res. 23 , 2012; 125–131.
doi: 10.1111/j.1600‐0501.2011.02161.x     

Sinus augmentation analysis revised: the gradient of graft consolidation

Objective: Graft consolidation follows a gradient that reflects the properties of bone substitutes at sites of sinus augmentation. Here we present an analytical method to investigate the process of graft consolidation taking the distance from the maxillary host bone into account. Material and methods: We therefore evaluated histological specimens, 6 and 12 weeks after the sinus of minipigs was augmented with Bio‐Oss^®, a deproteinized bovine bone mineral, and Ostim^®, an aqueous paste of synthetic nanoparticular hydroxyapatite. A curve was drawn that represents the changes in histomorphometric parameters within a given distance from the maxillary host bone. Results: Based on this curve, three regions of interest were defined: R1 (0–1 mm) the bridging distance where new bone is laid onto the host bone, R2 (2–3 mm) a region of osteoconduction where new bone exclusively grows on the biomaterial, R3 (4–5 mm) and a region of osteoconduction where bone formation has reached its maximal extension. Qualitative and quantitative analysis of the three regions can reveal differences in graft consolidation, depending on the bone substitutes and the observation period [Bone volume (BV) per tissue volume after 6 weeks: R1: 19±8.4% for Bio‐Oss^® and 42.9±13.2% for Ostim^® (P=0.03), R2: 3±2.4% for Bio‐Oss^® and 14.7±9.5% for Ostim^® (P=0.03), R3: 5±4.1% for Bio‐Oss^® and 5.3±5.3% for Ostim^® (P=0.86). BV per tissue volume after 12 weeks: R1: 38.0±13.3% for Bio‐Oss^® and 53.3±6.6 for Ostim^® (P=0.04), R2: 14±12.2 for Bio‐Oss^® and 26.4±11 for Ostim^® (P=0.18), R3: 6.6±7 for Bio‐Oss^® and 10.7±5.8 for Ostim^® (P=0.32) after 12 weeks]. Conclusion: Based on the graft consolidation gradient, the impact of bone substitutes to modulate the process of bone formation and the kinetic of degradation within a distinct region of the augmented sinus can be investigated.     

Histological and histomorphometrical analyses of biopsies harvested 11 years after maxillary sinus floor augmentation with deproteinized bovine and autogenous bone

Objective: The purpose of the present study was to histologically and histomorphometrically evaluate the long‐term tissue response to deproteinized bovine bone (DPBB) particles used in association with autogenous bone and to compare particle size after 6 months and 11 years, in the same patients, in order to determine possible resorption. Material and methods: Twenty consecutive patients (14 women and six men) with a mean age of 62 years (range 48–69 years) with severe atrophy of the posterior maxilla were included in this study. Thirty maxillary sinuses with <5 mm subantral alveolar bone were augmented with a mixture of 80% DPBB and 20% autogenous bone. Eleven years (mean 11.5 years) after augmentation, biopsies were taken from the grafted areas of the 11 patients who volunteered to participate in this new surgical intervention. The following histomorphometrical measurements were performed in these specimens: total bone area in percentage, total area of the DPBB, total area of marrow space, the degree of DPBB–bone contact (percentage of the total surface length for each particle), the length of all DPBB particles and the area of all DPBB particles. The length and the area of the particles were compared with samples harvested from the same patients at 6 months (nine samples) and pristine particles from the manufacturer. Results: The biopsies consisted of 44.7±16.9% lamellar bone, 38±16.9% marrow space and 17.3±13.2% DPBB. The degree of DPBB to bone contact was 61.5±34%. There were no statistically significant differences between the length and area of the particles after 11 years compared with those measured after 6 months in the same patients or to pristine particles from the manufacturer. Conclusion: DPBB particles were found to be well integrated in lamellar bone, after sinus floor augmentation in humans, showing no significant changes in particle size after 11 years. To cite this article:
Mordenfeld A, Hallman M, Johansson CB, Albrektsson T. Histological and histomorphometrical analyses of biopsies harvested 11 years after maxillary sinus floor augmentation with deproteinized bovine and autogenous bone.
Clin. Oral Impl. Res. 21 , 2010; 961–970.
doi: 10.1111/j.1600‐0501.2010.01939.x     

Anatomic and histological analysis in a goat model used for maxillary sinus floor augmentation with simultaneous implant placement

Objectives: The aim of the present study was to carry out an anatomic survey on the goat maxillary sinus in order to provide accurate and definite anatomic parameters for the design of sinus floor elevation and dental implantation studies in this valuable preclinic animal model. Material and methods: The anatomic topographic structure of the maxillary sinuses was studied bilaterally in 10 adult goats by a gross survey as well as a histological analysis with parasagittal or coronal sections. Then following parameters were defined and measured: (1) maxillary alveolar height (MAH): vertical height from the alveolar crest to the sinus floor; (2) sinus lateral floor width (SLFW): horizontal distance from the lateral border of the anteroposterior bone crest to the sinus lateral wall; (3) infraorbital canal diameter (ICD); and (4) maxillary sinus volume (MSV): the volume occupied by water injected into the sinus. The data were presented with mean±SD on both sides. Results: The goat has a maxillary sinus similar to humans, with a slender pyramidal shape that pneumatizes the entire maxilla, and a sinus wall covered with a mucosal lining. From the maxillary sinus floor, there is an anteroposterior bone crest protruding with the infraorbital canal enveloped. It divides the maxillary sinus floor into two parts. The SLFW of the lateral part of the maxillary sinus floor becomes broader, about 5.905±1.475 mm in the third premolar site, and the MAH increases towards the posterior area, where the maxillary sinus floor is close to the related teeth roots. According to original metrical data, we also proposed a possible operation procedure for sinus floor augmentation. Conclusions: There is enough space in the lateral floor of the maxillary sinus for dental implantation, and the third premolar area might be a suitable position suggested for maxillary sinus augmentation with simultaneous implant placement in a goat model. To cite this article:
Zou D, Guo L, Lu J, Zhang X, Zhang Z, Jiang X. Anatomic and histological analysis in a goat model used for maxillary sinus floor augmentation with simultaneous implant placement.
Clin. Oral Impl. Res. 21 , 2010; 65–70.     

Sinus floor augmentation with recombinant human growth and differentiation factor-5 (rhGDF-5): a pilot study in the Goettingen miniature pig comparing autogenous bone and rhGDF-5

Aim: The aim of this study was to test the hypothesis that recombinant human growth and differentiation factor-5 (rhGDF-5) in combination with a β-tricalcium phosphate (β-TCP) scaffold material results in superior bone formation in sinus floor augmentations in miniature pigs compared with a particulated autogenous bone graft combined with the scaffold material.
Material and methods: Six adult female Goettingen minipigs underwent a maxillary sinus floor augmentation procedure. In a split-mouth design, the sinus floors were augmented with β-TCP mixed with autogenous cortical bone chips, in a ratio of approximately 1 : 1, on one side. The contralateral test site was augmented using β-TCP coated with two concentrations of rhGDF-5 (400 μg rhGDF-5/g β-TCP or 800 μg rhGDF-5/g β-TCP; three animals in each case). Simultaneously, one dental implant was inserted into each sinus floor augmentation. After 12 weeks, a histological and histomorphometric assessment of non-decalcified histological specimens was made.
Results: There were significantly higher mean values of volume density of newly formed bone using β-TCP coated with two concentrations of rhGDF-5 (400 μg: 32.9%; 800 μg: 23.9%) than with the corresponding control (autogenous bone/β-TCP) (14.6%, 12.9%) ( P =0.012, P =0.049). The bone-to-implant contact rates (BIC) were significantly enhanced in test sites (400 μg: 84.2%; 800 μg: 69.8%) compared with the corresponding control sites (24.8%, 40.8%) ( P =.027, P =.045).
Conclusion: rhGDF-5 delivered on β-TCP significantly enhanced bone formation compared with β-TCP combined with autogenous bone in sinus lift procedures in miniature pigs.