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The International Journal of Periodontics & Restorative Dentistry

© 2013 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.

Volume 33, Number 6, 2013

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Following tooth removal, the sur-rounding alveolar bone naturally resorbs and a reduction of both the horizontal and vertical dimen-sions of the socket ridges occurs within the first 6 months,1 causing an inadequacy of available bone volume for subsequent endosse-ous implant treatment. During the process of socket wound healing, blood clot stabilization combined with bundle bone resorption con-tribute to dimensional changes of soft and hard tissues, measuring about 50% of the original width during the first year with most bone lost at the buccal side.1–3 Com-puted tomographic scans of pre-operative and postextraction sites with buccal wall defects provide quantitative evidence for trans-forming bone volume as well as for identifying locations of cortical and trabecular bone.2,4 A system-atic review analyzing dimensional changes to alveolar ridges follow-ing tooth extraction found the loss of horizontal dimension to be 32% at 3 months, and at 6 months the loss was between 29% and 63%.5

Alveolar ridge loss at extraction sites can be a significant problem for implant dentistry, adversely

1 Professor, Department of Surgery, University of Pisa, Camaiore (LU), Italy.2 Private Practice, Desenzano Del Garda, Italy.3 Private Practice, Padova (PD), Italy.4 Private Practice, Bergamo, Italy.5 Private Practice, Munich, Germany.6 Professor, Facultad de Odontología, University of Seville, Seville, Spain.7 Professor and Director, Hard Tissue Research Laboratory, University of Minnesota, Minneapolis, Minnesota, USA.

8 Senior Research Scientist and Assistant Director, Hard Tissue Research Laboratory, University of Minnesota, Minneapolis, Minnesota, USA.

9 Clinical Research Department, Biomet 3i, Palm Beach Gardens, Florida, USA. Correspondence to: Dr Antonio Barone, Department of Surgery, University of Pisa, Piazza Diaz 10, 55041 Camaiore (LU), Italy; fax: +39 (0)584- 6058716; email: [email protected]. ©2013 by Quintessence Publishing Co Inc.

Antonio Barone, DDS, PhD, MSc1/Marzio Todisco, DDS2 Maurizio Ludovichetti, MD, DDS3/Federico Gualini, MD, DDS, MSc4 Hans Aggstaller, PhD5/Daniel Torrés-Lagares, DDS, PhD6 Michael D. Rohrer, DDS, MS7/Hari S. Prasad, BS, MS, MDT8 James N. Kenealy, PharmD9

The aim of this prospective, randomized, controlled, multicenter study was to evaluate and compare the histologic and histomorphometric aspects of extraction sockets grafted with two commercially available bovine bone xenografts: Endobon (test group) and Bio-Oss (control group). The study was designed to ensure that baseline variables between groups were as similar as possible to allow for a direct comparison of graft healing characteristics. Thirty-eight patients contributed 62 augmented extraction sites to the study. All sites were grafted with one type of bovine bone mineral and covered with a resorbable collagen membrane for 6 months of healing prior to implant placement surgery. The histologic outcomes between the two treatment groups are similar, with de novo bone (mean ± SD) for the test group at 28.5% ± 20% and for the control group, 31.4% ± 18%. Histologic specimens also include membrane remnants. All but two implants integrated successfully after 1 year of follow-up. This investigation provides support for the efficacy of bovine bone xenograft for socket preservation when subsequent implant placement is planned. (Int J Periodontics Restorative Dent 2013;33:795–802. doi: 10.11607/prd.1690)

A Prospective, Randomized, Controlled, Multicenter Evaluation of Extraction Socket Preservation Comparing Two Bovine Xenografts: Clinical and Histologic Outcomes



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affecting implant placement, func-tion, and esthetics.6 Guided bone regeneration at the time of tooth extraction is advantageous for pre-serving alveolar bone and restoring bone height to diminished socket walls such that sufficient bone vol-ume is available for ideal implant placement at a later date.7,8 Socket grafting may be assisted with the use of collagen membranes to cov-er grafted sites and limit migration of graft material.8,9

The efficacy of socket pres-ervation techniques and grafting materials can be evaluated clini-cally by measuring changes to al-veolar dimensions after healing intervals. A comprehensive review of the effect of socket grafting on alveolar dimension changes found a horizontal preservation of 59% and a vertical preservation of 109%.10 No consensus has been reached regarding the superior-ity of any one specific graft mate-rial for socket preservation.11 One commercial brand of graft mate-rial with evidence-based data on various regenerative applications is Bio-Oss (Geistlich), a bovine-derived hydroxyapatite xenograft that is biocompatible, osteocon-ductive, and integrates with the surrounding bone on a long-term basis.12,13 Endobon (Biomet 3i) is also a nonantigenic xenograft of bovine origin with over 20 years of documentation as a proven graft material for orthopedic and dental applications. Processing at high temperatures converts the bovine bone and its amorphous inorganic components into a hy-droxyapatite material, eliminating

all organic and protenaceous com-ponents.14 During sintering, the natural bovine bone trabecular microstructure is preserved, as evi-denced by the traces of osteocyte lacunae network; pores of a submi-cron range (mesioporoisity, 0.01 to 1 µm) are subsumed into the miner-alized matrix.14,15 The overall struc-ture and pore morphology (size, percentage, and interconnectivity of the individual pores) are similar to mineralized human bone and serve as a scaffold allowing ingress of osteogenic cells and accelera-tion of bone ingrowth.14,15 The rate of bone ingrowth has an impact on stabilization of the graft material, with the majority of bone ingrowth occurring between 10 days and 5 weeks after implantation.16

The following prospective, mul-ticenter, randomized, controlled study evaluates and compares Endobon and Bio-Oss when used for socket preservation on a clinical and histologic basis after 6 months of healing. The study design allows for a split-mouth histologic quan-tification of the rate and extent of de novo bone formation for each of the two bovine bone xenografts. Clinical and dental implant out-comes will be described in detail in a subsequent publication.

Method and materials

Patients

This study included adult patients in need of at least two premolar or molar tooth extractions on the same date. Extraction procedures

were indicated due to either se-vere decay, periodontal disease, tooth fracture, or failed endodontic treatment. Patients were excluded for reporting a smoking habit of ≥ 10 cigarettes per day, for the presence of uncontrolled diabetes mellitus or metabolic bone dis-ease, for having received thera-peutic radiation to the head within the past 12 months, or for being known to be pregnant at the time of enrollment. At the screening visit, patients were enrolled after satisfying admission criteria, com-pleting a medical history, and pro-viding informed consent.

Methods

Atraumatic tooth extraction tech-niques were used to preserve the remaining alveolar bone and sur-rounding tissues. For molar ex-tractions, crowns were sectioned and then the roots were individu-ally removed. Efforts were made to ensure removal of all remaining root fragments, fibers, and soft tis-sue from the sockets, including the use of curettes and/or burs for de-granulation of extraction sockets. Following completion of extrac-tion procedures, the sites were as-sessed and scored for remaining soft and hard tissues as follows.17 Type I socket: the facial soft tis-sue and buccal plate of bone are at normal levels in relation to the cementoenamel junction of the pre-extracted tooth and remain in-tact postextraction. Type II socket: facial soft tissue is present but the buccal plate is partially missing



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following extraction of the tooth. Type III socket: the facial soft tis-sue and the buccal plate of bone are both markedly reduced after tooth extraction. Cases scored as Type III were to be excluded from the study due to the uncertainty of graft retention. A periodontal probe was used to measure the greatest mesial–distal and buccal–lingual distances of the extraction alveolus.

Qualified extraction sites were randomly assigned to receive ei-ther Endobon or Bio-Oss bovine xenograft granules. Randomiza-tion was accomplished using pre-numbered cards prepared for each participating center that assigned treatment groups to four tooth sites. The randomization cards were kept in opaque security en-velopes and opened at the time of surgery. Both xenograft materi-als were composed of irregular hy-droxyapatite granules with various granule sizes (250 to 1,000 µm), which were hydrated prior to place-ment with either saline or blood. Operators were instructed not to overpack or compress the graft material into the fresh extraction socket. To promote graft retention and reduce the possibility of graft movement, the sites were covered with a resorbable OsseoGuard collagen membrane (Biomet 3i), which were secured in place under the mucosal margins without use of releasing incisions or other meth-ods to gain marginal closure. Pho-tographs and radiographs of each of the treated sites were obtained to document the condition of the sites immediately after the study

surgery. Patients were instruct-ed not to rinse the surgical sites with warm fluids or with alcohol- containing mouth rinses. Patients were also instructed to avoid chew-ing at the treated sites, manipulat-ing the sites with their tongue, or probing the site with objects.

Postoperatively, patients were seen at approximately 10 days for healing assessment and were in-terviewed for postsurgical events such as swelling or release of graft material. Membrane outcomes in-cluded a visual assessment of the site to document the extent of wound closure. The condition of the membrane was documented, and, after suture removal, the sites were inspected to ensure the prop-er seating of the membrane and that no spillage of graft material was observed. A similar evaluation took place 2 weeks thereafter spe-cifically to document membrane status and to score the patient’s gingival and plaque indices.

After 6 months of healing, the sites were prepared for implant placement first using a tissue punch or mucoperiostal flap to access the cortical bone. A trephine drill was then used in the osteotomy prepa-ration, and the contents of the drill and tissue punch were preserved for histologic analysis to include examination of soft tissue for pres-ence of membrane collagen and trephine contents for proportion of vital (de novo) bone formation. Implants used in the study were NanoTite Tapered Certain implants (Biomet 3i) and associated restor-ative components. The acid-etched surface is present from the apex to

the bottom of the machined-sur-faced collar with the NanoTite sur-face treatment of nanometer-scale discrete crystalline depositions of calcium phosphate added to all the etched surfaces. Bone density was assessed as well as fit of the implant at final seating. The final drill unit torque was recorded and a healing abutment was placed at this implant placement surgery.

A healing period of at least 4 months was to be provided for im-plants placed in the maxilla and of at least 2 months for mandibular implants before prosthesis inser-tion. About 10 days after implant placement surgery, all patients returned to the study center for a clinical evaluation and suture re-moval. The definitive prosthesis was to be inserted at the discretion of the investigator and according to the treatment plan design within 12 months of the implant place-ment surgery.

Histologic preparation

The specimens were harvested and placed in 10% neutral buffered formalin. Upon receipt in the Hard Tissue Research Laboratory at The University of Minnesota School of Dentistry, they were sectioned in half through the area of interest and immediately dehydrated with a graded series of alcohols for 9 days. Following dehydration, the speci-mens were infiltrated with a light-curing embedding resin (Technovit 7200 VLC). Following 20 days of infiltration with constant shaking at normal atmospheric pressure, the



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specimens were embedded and polymerized by 450-nm light with the temperature of the specimens never exceeding 40°C. The speci-mens were then prepared accord-ing to the cutting/grinding method of Donath.18,19 The specimens were cut to a thickness of 150 µm on an EXAKT cutting/grinding sys-tem (EXAKT Technologies). Cores were then polished to a thickness of 45 to 60 µm using a series of polishing sandpaper disks from 800 to 2,400 grit using an EXAKT microgrinding system followed by a final polish with 0.3 µm alumina polishing paste. The slides were stained with Stevenel blue and Van Gieson picro fuchsin.

Histomorphometry

Following histologic prepara-tion, the specimens were evalu-ated histomorphometrically. All the specimens were digitized at the same magnification using a

NIKON ECLIPSE 50i microscope (Nikon) and a Spot Insight 2 mega sample digital camera (Diagnostic Instruments). Histomorphometric measurements were completed us-ing a combination of spot insight program and Adobe PhotoShop (Adobe Systems). At least two slides of each specimen were evaluated. Digitized images were scored with regard to areas of new (vital) bone, residual xenograft, and soft tissue. The following qual-itative assessments were done: (1) nature of the newly formed tis-sues in the extraction sites, (2) re-sorption pattern of any observed graft particles, and (3) bone rela-tionship to the residual grafting material. The five most central sec-tions in each specimen were se-lected for quantitative assessment of different tissue components: mineralized bone, osteoid, and fi-brous tissue. These measurements are expressed as a percentage of the total surface area of the bone core section.

Results

The study was conducted at six clinical and university centers in Italy, Germany, and Spain. A total of 38 patients were enrolled over a 9-month period with 78 treat-ed extraction sites. Not all sites produced histologic specimens that yielded data. Qualified sites were those with successful tooth extractions, grafting, and oste-otomy preparation that produced an intact bone core for histologic assessment. A total of 62 quali-fied sites were included, with 24 patients contributing 2 qualified sites and 14 patients providing 1 qualified extraction site each to the study dataset and these were evenly divided between the test and control grafting materials.

The mean patient age at time of enrollment was 51 ± 14 years with a sex distribution of 53% men and 47% women. In each group, approximately 26% admitted to a daily average of 11 cigarettes.

Fig 1 Mandibular molar site after tooth extraction.

Fig 2 Endobon granules hydrated using the patient’s blood as the preferred hydration material and placed directly into the debrided extraction socket, filling it to the height of the surrounding alveolar ridges.

Fig 3 An OsseoGuard membrane is trimmed and adapted over the grafted site with the borders placed underneath adjacent soft tissue. The mucosal margins were secured using mattress sutures, and the membrane was left exposed to the oral cavity.



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Reasons for tooth extractions in-cluded severe decay (65%), peri-odontal disease (15%), tooth fracture (15%), and endodontic failure (5%). Figures 1 through 5 are examples of the grafting pro-cedure. All but one extraction site are in the posterior region, with 60% in the maxilla. Both groups had similar rates of tooth section-ing and the extent of bone re-quired for tooth removal. Socket type outcomes were also similar between groups, with most hav-ing type 1 (60%) and type 2 (31%) conditions and with two cases scored as type 3 but included in the analysis. In 17% of cases, bone removal was required for tooth extraction. Mesial–distal socket dimensions (mean ± SD) were 9.2 ± 2.9 mm and 8.9 ± 2.4 mm, and the buccal–lingual socket di-mensions (mean ± SD) were 8.8 ± 1.5 mm and 9.0 ± 1.9 mm for the test and control groups, respec-tively. The amount of graft material placed in the sites (mean ± SD) was

0.54 ± 0.22 and 0.51 ± 0.19 g for the test and control groups, respec-tively. At the suture removal visit, 10 days postsurgery, both groups had similar rates of site opening (test, 39% and control, 46%) and membrane exposure (test, 43% and control, 42%), and patients in both groups (41% to 42%) re-ported some spillage or escape of graft material from the study sites. An example of an implant-treated study site is included in Fig 6.

Histologic outcomes from Bio-Oss- and Endobon-treated sites are included in Figs 7 to 13. Of the 62 sites with histologic and clinical data, the percent vital bone for the test (Endobon) group was 28.5% ± 20.0% and for the control (Bio-Oss) group, 31.4% ± 18.1%. Because both test and control cases were in the same patient, all baseline variables were similar, allowing for a comparison of per-formance and success rates be-tween treatment groups. Analysis of histologic outcomes based on

socket type showed no difference between Type I (n = 30, 30% vital bone) vs Type II (n = 30, 33% vital bone). All but one implant integrat-ed successfully and a total of two implant failures were recorded for an overall success rate of 97.3% at 1 year.

Discussion

This clinical report describes his-tologic outcomes for two com-mercially available preparations of bovine bone xenograft, Bio-Oss and Endobon, when used as intra-socket regenerative materials with subsequent implant placement. Im-mediately after tooth removal, the condition of the extraction socket was assessed based on remaining soft and hard tissues according to socket type classifications. There was no correlation with these base-line data and histologic outcomes for de novo bone formation after 6 months of healing. Histometric

Fig 4 Healed augmented extraction socket 6 months after grafting showing retention of alveolar ridge height.

Fig 5 The osteotomy has been surgically prepared for placement of an implant.

Fig 6 Peri-apical radiograph of grafted site taken 1 year after prosthetic loading shows uniformity of the bone matrix.



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results between the two bovine regenerative materials were also similar, with mean de novo bone of 31.4% ± 18% for the Bio-Oss group and 28.5% ± 20% for the Endobon group.

Five clinical studies provide histomorphometric reference for immediate grafting of fresh extrac-tion sockets using Bio-Oss, with healing intervals ranging from 4 to 12 months prior to implant place-ment.20–24 Two of these studies in-clude the same 6-month healing interval as in the current study.20,21

In one report, a mean of 39.4% vital bone was observed for sites grafted in conjunction with acel-lular human dermal matrix.20 The other study reports histologic out-comes at increasing healing time intervals, with 4 months having 19.4% vital bone, 6 months having 34.5% vital bone, 9 months having 69.1% vital bone, and 12 months having 68.8% vital bone.21 For 9 months of healing specifically at nonmolar extraction sites grafted with Bio-Oss, mean new bone was 27.3% when collagen membranes

were placed22 and 46.3% for cases without membranes.23 Bio-Oss has also shown de novo bone of 23.6% after 4.6 months of healing, report-ed to be a better outcome in com-parison to allograft materials.24

Clinical studies with histomor-phometric outcomes for Endobon report use of the xenograft in si-nus augmentations with 27.5% new bone formation at 6 months25 and 25.1% at 9 months.26 Despite the difference in regenerative ap-proach, these outcomes for Endo-bon compare favorably with vital

NB NB

NB

BO

OSBO

BO

NB

NB

EBEB

M

M

E

Fig 7 (left) Histologic section of a tissue punch sample. The top specimen is a transverse section of a tissue punch where remnants of the OsseoGuard membrane (M) are visible in the green-colored stained regions immediate adjacent to the dermal layer (blue). The lower specimen is a cross section of a tissue punch showing a dermal layer under which remnants of the mem-brane (M) are visible along with an Endobon (E) particle directly under the membrane.

Fig 8 (right) Trephine core sample shows newly formed cancellous bone (NB) and particles of Bio-Oss (BO) within the vicinity of new bone formation. Bone stains red and Bio-Oss is straw-colored (Stevenel blue and Van Gieson picric fuchsin; original magnification ×25). OS = osteocyte.

Fig 9 Histologic section of a trephine core sample. On the left side of the image are Endobon particles (EB, dark gray) and de novo bone (NB) that stains orange. Endobon’s darker appearance is considered a result of higher density and lower microscopic translucency (Stevenel blue and Van Gieson’s fuchsin; original magnification ×25).



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bone outcomes for both bovine-derived xenografts in the present study.

Histology samples for both graft types also show similarities in presence of new bone forma-tion and the amount and patterns of graft particles in trephine core samples at higher magnifications. The darker appearance of Endo-bon granules on optical microsco-py, in contrast to the straw color of Bio-Oss, is one distinguishing char-acteristic in the current study. The lower translucency is considered

a result of Endobon’s lower sub-micron porosity, which has been shown in this and other studies to have no impact on biologic perfor-mance.

Conclusion

This prospective, randomized, con-trolled clinical study shows histo-morphometric outcome similarities between two bovine xenografts at 6 months of healing follow-ing immediate grafting of fresh

extraction sockets. The results also parallel those reported for bovine bone xenograft in other published clinical studies with de novo bone outcomes for intrasocket regenera-tive techniques.

Acknowledgments

This study was supported by a grant from Biomet 3i. The authors thank Dr Renée M. Stach for contributions to this article.

Fig 10 Histologic section of a Bio-Oss core sample. On the upper center portion of the core are Bio-Oss particles (BO, buff-colored) and de novo bone (NB) that stains orange. Native bone is darker than the xenograft and de novo bone in this section (Stevenel blue and Van Gieson picric fuchsin; original magnification ×40).

Fig 11 Histologic evaluation of bone samples at 24 weeks of extraction site healing. Bridging between Bio-Oss particles (BO) and vital bone (NB) is observed within the core (Stevenel blue and Van Gieson picric fuchsin; original magnification ×100). OS = osteocytes.

Fig 12 Formation of new bone (NB) dem-onstrating a cancellous bone pattern. At 24 weeks of extraction site healing, graft inte-gration and bone bridging with Endobon xenograft material (EB) is present. Picsene of osteocyte (OS) can be seen within the new bone (Stevenel blue and Van Gieson picric fuchsin; original magnification ×100).

Fig 13 Formation of new bone (NB) demonstrating a cancellous bone pattern. At 24 weeks of extraction site healing, graft integration and bone bridging with Bio-Oss xenograft material is present (Stevenel blue and Van Gieson picric fuchsin; original magnification ×200).

NB NB NB

NB

BOOS

BO

BO

NB

NBBO

BO

BO

OS

NB

NB

NBNB

NB

NB

NB

NB

EB EB

EB

EB

OSNB

NB



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