The International Journal of Periodontics & Restorative Dentistry

Histomorphometric Comparison of a Biphasic Bone Ceramic to Anorganic Bovine Bone for Sinus Augmentation: 6- to 8-Month Postsurgical Assessment 3f Vital Bone Formation. A Pilot Study.

Stuart J. Froum, DDS/Stephen S. Wallace, DDS Sang-Choon Cho, DDS/Nicolas Elian, DDS Dennis P. Tarnow, DDS

This blinded, randomized, controlled pilot investigation is the first to histomorphometrically compare vital bone formation following bilateral sinus grafting with a biphasic calcium phos­phate (BCP) (Straurnann Bone Ceramic) to an anoganic bovine bone matrix (ABBM) (Bio-Oss) 6 to 8 months following graft placement. Twelve patients were selected. Following elevation of the lateral sinus walls, one material was placed in the right sinus and the other material was laced in the left sinus, as determined by randomization. Six to 8 months after grafting (with me same time frame used for each patient), a trephine core was taken from the grafted area and sent for histomorphometric analysis. Cores were obtained from 21 healed sinuses in 12 patients. Nine patients provided bilateral cores. Histomorphometric analysis of 70 BCP cores and 7 7 ABBM cores revealed an average vital bone content of 28.35% and 22.2736, respec­tively. The average percentage of residual graft particles was 28.4% in the BCP cores and 26.0% in the ABBM cores. The difference in vital bone formation was not significantly differ­ent (n= 9 patients, paired t test) between bilateral sinuses treated with the BCP and those treated with the ABBM. Histologically, both materials appeared to be osteoconductive and ~pport new bone formation. Future studies are needed to confirm the ability of this regener­ted bone to support dental implant maintenance over time. (Int J Periodontics Restorative Dent 2008;28:273-281.)

-Clinical ,Professor, Department of Periodontology and lmplant Dentistry, College of Dentistry, New York University, New York.

-Associate Clinical Professor, Department of Periodontology and lmplant Dentistry, College of Dentistry, New York University, New York.

Assistant Clinical Professor, Department of Periodontology and lmplant Dentistry, College o)f Dentistry, New York University, New York.

Assistant Professor and Director, Department of Periodontology and lmplant Dentistry, College of Dentistry, New York University, New York.

Professor and Chair, Department of Periodontology and lmplant Dentistry, College of Dentistry, New York University, New York.

Correspondence to: Dr Stuart J. Froum, 17 West 54th Street, Suite 1C/D, New York, NY, 10019; fax: 212 246 7599;

The subantral augmentation (sinus lift) procedure has been shown to be a pre­dictable method for placing root-form implants in areas of the posterior max­illa with deficient bone quantity and/or quality. The original protocol uses autogenous bone from intraoral or extraoral sources.1 4 The need for a sec­ond surgical site to harvest autogenous bone increases the length of the surgi­cal intervention, surgical risk, and post-surgical morbidity, since healing is required in multiple sites.

Therefore, bone replacement graft materials have been used in the sinus lift procedure to avoid the drawbacks inherent in the harvesting of autogenous bone. These materials include allografts, xenografts, and alloplasts. The literature shows highly successful clinical results following the use of most of these materials in terms of implant survival. In fact, the implant survival rates reported for most bone replacement grafts are higher than those reported for 100% autogenous bone.

Straumann bone ceramic (Straumann) is a biphasic calcium phosphate (BCP) that has been widely used as a bone graft substitute in orthopedic; ear, nose, and throat; and dental surgery. This material is fully synthetic and consists of 60% hydroxyapatite and 40% beta-trical-cium phosphate. The granules are 90% porous with interconnected pores of 100 to 500 pm. BCP has been shown to be safe, nonallogenic, and effective as a scaffold for the for­mation of new bone.

Anorganic bovine bone matrix (ABBM) (Bio-Oss, Osteohealth) is a bone substitute manufactured from bovine bone mineral that has been processed and sterilized for use in intraoral grafting procedures. It is com­posed of only the mineral portion of bone. The safety of ABBM was previously established. Both grafting materials used in this study were approved by the Federal Drug Administration for use in sinus aug­mentation procedures.
The purpose of this proof-of-prin-ciple prospective, blinded, random­ized, controlled investigation was to compare the efficacy of BCP to ABBM in terms of vital bone formation 6 to 8 months after sinus augmentation surgery.

Method and materials
Patient selection
Fifteen subjects were selected from those presenting to the Department of Periodontics and Implant Dentistry at the New York University Kriser Dental Center who, after being presented with alternative treatment plans, chose a plan that included maxillary posterior implants but did not possess sufficient bone volume for the placement ot these implants.

There were no limitations to enrollment in terms of gender, race, or ethnicity. Patients who could not undergo standard oral surgical procedures for any reason, patients who smoked more than 10 cigarettes per day, and women who were pregnant or nursing a child were excluded.

Inclusion criteria included the presence of less than 5 mm of residual crestal bone bilaterally as measured on computerized axial tomographic radiographs. There were no contra­indications for sinus/implant surgery or surgery in general. Each subject gave informed consent and signed a consent document approved by the New York University School of Medicine, Institutional Board of Research. 

Sinus elevation surgery
The lateral window sinus elevation pra­cedure used in this study was previ­ously described and so will be pre­sented only briefly here. Either a hinge or a complete osteotomy of the lateral sinus wall was performed as necessary. If the bony window was removed to facilitate elevation of the membrane, it was not added to the grafted bone. The sinus membrane was then elevated across the floor and up the medial wall. BCP was placed in one subantral compartment and ABBM was placed in the contralateral subantral compartment, as determined by a computer-generated randomized code. The mixture for each material was composed of 50% 0.25- to 1.O-mm-size particles and 50% I.0-to 2.0-mm-size particles. Depending on the sinus anatomy, 3 to 5 mg of material was grafted in each sinus. The decision to treat both sinuses either simultaneously or at separate visits was determined by patientxvaluation -and the complexity of surgery. A synthetic bioabsorbable collagen barrier membrane (BioMend Extend, Zimmer Dental) was hydrated for 1 to 5 minutes in sterile saline prior to insertion and placed over the lateral window, extending approximately 3 mm beyond the preparation. Primary closure was achieved with silk (Ethicon), ,)olyglactin 910 (Vicryl, Ethicon), or expanded polytetrafluoroethylene sutures (Gore-Tex), according to the operator's preference. Existing removable appliances were removed as necessary, and appropriate antibiotic coverage and analgesics were prescribed.

Implant surgery and bone core harvest
luring implant placement (following a 6- to 8-month healing phase), a trephine core sample (10 mm in length and 3 mm in diameter) was retrieved from within the borders of the original lateral window. The bone cores were taken from sites selected so as not to compromise implant placement. The cores were taken from both test and control sides by one of the principal investigators. Removal of the core completed the subjects' participation in the study.

Statistical analysis
The retrieved cores were sent for histomorphometric analysis to determine the vital bone content, connective tissue content, and residual graft material content of each core sample. The histologic and histomorphometric procedures have been previously described.

Statistical analysis consisted of determining the averages and ranges for the percent of bone, vital bone, and connective tissue and marrow. Thirty-six sections from the BCP (test) group and 36 sections from the ABBM (control) group were evaluated. Paired t tests were used to evaluate each of the aforementioned parameters in the nine bilateral cores, in which the grafts were allowed to heal for the same time period prior to core extraction.

Results
Twelve bilateral sinus augmentations were performed on 12 patients. Of the 15 subjects enrolled in the study, 3 were withdrawn. One withdrew for financial reasons, one because of an inability to obtain cores within the study time protocol, and one because of an infection that required re-entry and debridement prior to the time required for core harvesting.

Cores were obtained 24 to 32 weeks postsurgery from 21 healed sinuses in 12 patients. Nine patients provided bilateral cores. One patient had an intact BCP core but an inadequate ABBM core, while two patients had intact ABBM cores but inadequate BCP cores. In these patients, core retrieval was attempted but could not be carried out because the graft material broke into pieces when attempting to trephine the core. Small schneiderian membrane perforations, which occurred during surgery, were reported in 29% of the treated sinuses (three sinuses in the BCP group and four sinuses in the ABBM group). All perforations were repaired with collagen membranes (BioGide, Osteohealth; or BioMend, Zimmer Dental).

Histomorphometric analysis of the 10 BCP cores revealed a 28.35% average vital bone volume (range: 7.5% to 71%). A similar analysis of the 11 ABBM cores revealed an average vital bone volume of 22.27% (range: 11 % to 30%). Bone vitality was 100% in all cores harvested.

The average percentages of mar­row/connective tissue were 43.25% and 51.73% for the BCP and ABBM sinuses, respectively, and the average percentages of residual graft material were 28.4% and 26%, respectively (Table 1). A paired t test of the nine bilateral sinus lifts with each material (BCP and ABBM) revealed no statisti­cally significant differences in any of the parameters evaluated (P > .05).

From a histologic point of view, both BCP and ABBM particles appeared to be osteoconductive. New bone formation was observed adjacent to and surrounding the BCP particles (Figs Ia to Ic). The ABBM particles were surrounded by greater or lesser amounts of new bone and osteoid depending on the patient and sinus observed.

Discussion
The use of bone substitute materials to replace autogenous bone in sinus augmentation procedures has become more widespread in an attempt to avoid the drawbacks of harvesting and using autogenous bone. Two independent systematic reviews of survival rates for implants placed in grafted maxillary sinuses showed implant survival rates of 91.8% and 91.5%. l5il6 In the review by Del Fabbro et a1,16 sinuses grafted with 100% bone replacement graft had an implant survival rate of 96.2%, compared to 87.7% for sinuses grafted with 100% autogenous bone.

In 1997, Wheeler reviewed the literature on the use of alloplastic materials alone in sinus augmentations and concluded that comparison studies indicated that sinuses augmented with pure alloplasts can support implants in function with results equal to or better than sinuses augmented with autogenous grafts or nongrafted sinuses. The author looked at combined study data on more than 165 successful sinus aug­mentations using a lloplasts without any allogenic or autogenous component.

Fugazzotto and Vlassis follwed 550 implants placed in 222 sinus augmentations using a variety of materials including xenografts (Bio-Oss) and tri-calcium phosphate and reported an overall success rate of 96.5% for the evaluation period of 73 months. Moreover, they reported no significant differences in terms of success between the types of material used.

More recent studies have supported the earlier favorable results reported for xenografts; however, this is not the case with studies of alloplasts. While the most recent evidence-based review showed a higher implant survival rate in sinuses grafted with 100% xenograft (95.6%) compared to sinuses grafted with 100% iliac crest (88.0%), it showed relatively poor results for sinuses grafted with 100% alloplast (81.O%).

The present study did not asseii implant survival rates; rather, it examined the percent of vital bone present after grafting bilateral sinuses with 100% BCP (alloplast) or 100% ABBM (xenograft). This is the first randomized, controlled clinical trial to directly compare BCP to ABBM in sinus augmentation.

While the amount of vital bone formed in the sinus after a given time period (6 to 8 months) may not correlate to survival of implants placed in these sinuses, it remains an accurate indicator to assess and compare the healing potential of graft or bone replacement graft materials. Bilateral sinus grafting in humans is an excellent model since it enables a direct comparison of two sinus augmentation materials while eliminating the host as a variable. Although the size of the two sinuses in the same individual may vary, studies using identical methods (eg, flap design, use of barrier membranes over the lateral window core sampling) and materials (eg, medications, membranes, sutures), such as this one, allow an accurate evaluation and comparison of the healing response of two bone graft or replacement graft materials. However, future studoes are needed to confirm and compare the ability of regenerated bone to support implants.

In the present study, vital bone formation was slightly higher in the BCP-grafted sinuses (28.35%) than in ABBM-treated sinuses (22.27%), but these differences were not statistically - significant. These values are similar to those obtained for vital bone formation in sinuses grafted with mineralized cancellous bone allograft (average: 28.25%) as documented in a previous study by the same authors.

However, unlike with mineralized cancellous bone allograft, where a percentage of the bone, surrounding the allograft particles was nonvital, all new bone in the present study showed 100% vitality in all cores examined in both the BCP and ABBM groups.

Several studies have shown a direct relationship between graft maturation time and vital bone formation. Froum et at7 used ABBM with and without autogenous bone in nine sinuses and reported 24% average vital bone volume at 6 to 9 months, compared to 33% vital bone volume at 12 to15 months. Valentini et aI8 examined sinuses grafted with 100% ABBM and showed a mean percentage of vital bone of 21.08% at 6 months and 27.55% at 12 months. A more recent study by Lee et aIz9 also showed a correlation between mean vital bone and time of healing. In 14 sinuses grafted with 100% ABBM ind covered with a collagen membrane, the average per­cent of vital bone was 18.3% at 6 months and 26.6% at 12 months.

In the present study, a similar trend may be noted with cores from sinuses grafted with BCP. In two cases in which core harvesting was attempted 6 months after grafting with BCP, the new bone and graft material had not fused sufficiently for a core to be taken. In another patient, a bmonth core taken from a sinus treated with BCP yielded 13% vital bone volume. Conversely, the best results with BCP-grafted sinuses were obtained with cores harvested 8 months postsurgety, with vital bone volumes of 55% and 71 %. This trend of increased vital bone volume with increased healing time was not seen in sinuses grafted with ABBM. In three patients, sinus cores harvested at 6 months postsurgery with ABBM showed vital bone values of 29%, 24%, and 27%, while cores obtained at 8 months showed vital bone values of 11%, 19%, and 21%. Although the number of patients and sinuses was limited, these trends seem to imply that a longer healing period is desirable prior to implant placement in sinuses grafted with BCP compared to those grafted with ABBM. However, the 6- to 8-month core retrieval time in the present study may be too short to see temporal differences in vital bone in the ABBM group.

This investigation should be considered a pilot study. Additional studies with greater numbers of patients are needed to determine whether longer healing times are necessary with BCP-grafted sinuses and whether the additional time results in greater avail­able bone. Moreover, studies assess­ing the survival of implants placed in sinuses grafted with these two materials are necessary to determine the advantages (if any) of using one material as opposed to the other.

Acknowledgments

The authors would like to thank Michael D. Rohrer, Professor and Director, Division of Oral and Maxillofacial Pathology and Hard Tissues Research Laboratory, University of Minnesota School of Dentistry, Minneapolis, and Hari S. Prasad, Senior Research Scientist, University of Minnesota School of Dentistry, Minneapolis, for their efforts and histomorphometric analy­sis of the specimens presented in the present study. This study was supported by Straumann, which donated the BCP.

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