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Histomorphometric Evaluation of Extraction Sockets
and Deficient Alveolar Ridges Treated with Allograft
and Barrier Membrane: A Pilot Study
Hyman Smukler, BDS, DMD, HDD*/Luca Landi, DDS**/Reza Setayesh, DMD, DMSc***
The aim of the study was to determine the fate of demineralized freeze-dried bone allograft (DFDBA)used in conjunction with a barrier membrane in the management of extraction sockets and deficientalveolar ridges, and to compare the amount of bone formed with that found in untreated sites. Tenbiopsies were obtained from 8 grafted patients. Five biopsies were harvested from untreated sites dur-ing routine implant placement and analyzed for comparison. In the socket management procedure,DFDBA was packed tightly into the socket and covered with an expanded polytetrafluoroethylene (e-PTFE) membrane. Primary closure was achieved in all cases. In the ridge regeneration procedure, corti-cal columns were placed in the ridge projecting outward approximately 3 mm to create and maintainspace for DFDBA particles packed between them; the columns were then covered by an e-PTFE mem-brane. Healing time ranged from 8 to 23 months. At the time of implant placement, bone cores (7 mmϫ 2 mm) were harvested, fixed in 10% formalin solution, and prepared for histologic examination. Atthe light microscopic level, no inflammation or fibrous encapsulation was observed. New bone forma-tion on and around DFDBA particles was widespread. Histomorphometric analysis of the grafted speci-mens and untreated sites was carried out using the trabecular bone volume (TBV) index. The TBV in themaxillary test specimens was 55.03%, as compared to 57.33% of control cores. Unaltered DFDBAmade up 8.7% of the test specimens. In the mandibular biopsies, the TBV was 56.6%, while for thecontrols it was 40.9%. The volume of DFDBA still present was 2.45%. The results tended to indicatethat treatment with DFDBA in conjunction with cell occlusive membranes will result in new bone for-mation, predominantly by the process of conduction, which appears to be similar in amount andnature to that found in cores harvested from healed nonfunctional edentulous areas.
(INT J ORAL MAXILLOFAC IMPLANTS 1999;14:407–416) Key words: deficient ridges, demineralized freeze-dried bone allograft, extraction sockets, guided bone
regeneration, histomorphometry, osteoconduction
According to Amler et al,1 uncomplicated heal- events, beginning with clot formation and culmi- ing of human extraction sockets takes place in nating in a bone-filled socket with a connective tis- approximately 40 days in an organized sequence of sue and epithelial tissue covering. However, diseaseof periodontic and endodontic origin or surgicaltrauma can adversely affect this normal pattern andresult in extraction sites that have healed but have ***Professor, Boston University School of Dental Medicine, Department of Periodontology and Oral Biology, Boston, alveolar ridges that are quantitatively deficient.
These deformed alveolar ridges do not permit ***Periodontal Resident, Boston University School of Dental appropriate pontic fabrication when conventional Medicine, Department of Periodontology and Oral Biology, fixed prostheses are contemplated; nor do they per- Boston, Massachusetts; and Private Practice, Grosseto, Italy.
mit the placement of endosseous implants when ***Associate Professor, Boston University School of Dental Medicine, Department of Periodontology and Oral Biology, this form of tooth replacement is being considered.
Defective ridge formation can be prevented bygrafting the deficient or vulnerable sockets at the Reprint requests: Dr Hyman Smukler, Boston University School
time of tooth loss to ensure the formation of alveo- of Dental Medicine, Department of Periodontology and OralBiology, 100 East Newton Street, Boston, MA 02118. lar bone within the sites,2,3 and deficient alveolar ridges can be augmented or regenerated.4–7 COPYRIGHT 2000 BY QUINTESSENCE PUBLISHING CO, INC. PRINTINGOF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART OF The International Journal of Oral & Maxillofacial Implants THIS ARTICLE MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITH- OUT WRITTEN PERMISSION FROM THE PUBLISHER.
Smukler et al
Requirements for successful alveolar regenera- There is a paucity of human histologic and his- tion were first presented by Melcher and Dreyer in tomorphometric data pertaining to the amounts of 1962.8 Later, Nyman and coworkers9 proposed new bone formed in extraction sockets and on guidelines for guided tissue regeneration in the deficient alveolar ridges augmented with DFDBA repair of defects associated with teeth and edentu- particles and barrier membranes. This study was lous ridges.10 These included creation and mainte- undertaken to evaluate the potential of this type of nance of space; protection of the blood clot treatment to produce new bone in these situations.
formed; trephining of cortical plates to enhance the An additional aim was to compare the amounts of ingress of vascular, cellular, and molecular elements newly formed bone with that found in untreated needed in the regenerative process; and the use of a cell occlusive barrier membrane to prevent inva-sion of the site by tissues that could impede regen- Materials and Methods
eration. These criteria have since been successfullyapplied in endeavors to generate bone in extraction Patient Selection. Six patients, all requiring
sockets2,3 and to regenerate alveolar bone in defec- extraction of 1 or more teeth for traumatic or tive ridges.4,5,6,11 Human demineralized freeze- endodontic reasons (these were to be replaced by dried bone allografts (DFDBA) have been used in endosseous implants), were included in the socket conjunction with the principles of guided bone treatment portion of the study. Two patients regeneration to reconstitute and maintain bone requiring ridge augmentation procedures prior to during the placement of endosseous implants.6,12–18 implant placement participated in this part of the In these instances, DFDBA has been considered a study, while 5 patients requiring routine endosse- space maintaining device and osteopromotive, and ous implant placement provided cores for the new bone formation takes place predominantly by untreated areas (Table 1). The patients, 4 males a process of osteoconduction.3,16,18 The role of and 4 females ranging in age from 30 to 65 years DFDBA as an osteoinductive element has been (mean 58.33), were all treated in Department of both questioned19–24 and affirmed.2,25–27 Periodontology and Oral Biology Implant Center COPYRIGHT 2000 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING 408 Volume 14, Number 3, 1999
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Smukler et al
at Boston University School of Dental Medicine.
ing the membranes from the soft tissue and under- All patients were in good health as determined by lying bone. Primary closure of the wounds was medical history screening, had no contraindica- obtained using suturing methods previously tions to treatment, exhibited good oral hygiene, described. Those membranes that were retained and were informed of the nature of this investiga- until implant placement were removed in the same tion. All gave their informed consent according to manner at the time of stage 2 surgery (Fig 3).
the guidelines of the Internal Review Board, which Ridge Regeneration. Appropriate local anesthesia was administered, and a distal-to-mesial incision Surgical Technique. Socket Management. Fol-
was made on the crest of the edentulous ridge lowing administration of appropriate local anes- between the teeth adjacent to the edentulous space, thesia, intrasulcular incisions were made around from the mesiolingual line angle of the distal tooth the teeth to be extracted. Vertical releasing inci- to the distolingual line angle of the mesial tooth.
sions were made both palatally and facially, either Vertical releasing incisions were made at the distal at the mesial and distal line angles of teeth adjacent line angle of the distal and the mesial line angle of to the tooth being removed or one tooth distal and the mesial adjacent teeth, both buccally and lin- mesial to it, and mucoperiosteal flaps were care- gually, and carried around the teeth to join the cre- fully elevated. The tooth in question was atraumat- stal incision. Mucoperiosteal flaps were elevated, ically extracted and the socket was thoroughly and the buccal alveolar surface was penetrated in debrided (Fig 1). Intramarrow penetration with a multiple areas to expose the endosseum. Wider fine, round bur promoted appropriate bleeding.
holes, approximately 2 ϫ 2 mm (Fig 4a), were Commercially obtained DFDBA (American Red drilled to receive the specially prepared DFDBA cor- Cross, St. Louis, MO) of 250 to 350 µm particle tical columns (Northwest Tissue Center, Seattle, size was hydrated with sterile normal saline for 30 WA), which, after being firmly placed in these holes, minutes prior to placement within the sockets. The projected out laterally approximately 3 mm like tent DFDBA was placed in the socket and compressed poles (Fig 4b) to support the e-PTFE membrane to using saline-saturated gauze, from which all excess be placed over the site.7 Particulate DFDBA with saline had been expressed, and firm pressure from the same properties as that used in the socket treat- a hand instrument to eliminate dead spaces within ment part of the study was similarly reconstituted the graft material. This was repeated until the and compressed onto the surface of the alveolar socket was slightly overfilled (Fig 2).
bone around and between the cortical columns (Fig A nonresorbable expanded polytetrafluoroeth- 4c). The membrane was then suitably trimmed, using the same precautions as previously described, Flagstaff, AZ) of appropriate dimension was and adapted well to sound bone surrounding the trimmed so that it extended approximately 3 mm augmentation site. The buccal flaps were further over the socket onto sound bone buccolingually released via periosteal separation to permit primary but did not engage adjacent tooth surfaces. The closure of the wounds without undue tension, and buccal flaps were further released by periosteal the flaps were sutured with e-PTFE vertical mattress separation to permit coronal positioning of the tis- alternating with interrupted sutures. Postoperative sues and primary closure. Suturing was accom- medications and membrane removal were the same plished with nonresorbable e-PTFE, vertical mat- tress, and interrupted sutures. The patients were Core Harvesting. At the time of implant place-
placed on doxycycline 100 mg/day for 2 weeks ment, which varied between 8 and 23 months after and nonsteroidal anti-inflammatory medication for grafting, the patients received appropriate local pain control for 5 days, and chlorhexidine glu- infiltration anesthesia and mucoperiosteal flaps conate mouthwash (twice daily) was prescribed were elevated. Utilizing the photographic records until mechanical plaque control could be recom- made at each surgical stage as a frame of reference, menced after 1 week. Sutures were removed after 1 the center of each augmented extraction site was week and the patients were seen weekly to monitor compared to the original, in an attempt to ensure that the core would be taken from the treated site.
Membranes were kept in place for a minimum The use of templates would have been more accu- of 5 weeks; they were removed at the time of rate, but since the study did not include measure- implant placement if they had not already become ment of the ridges, templates were not used. As the exposed and been removed. The membranes were first step in osteotomy site preparation, a 2-mm removed following administration of local anesthe- surgical trephine was used to remove a 7-mm-long sia by elevating mucoperiosteal flaps and separat- bone core from the center of the regenerated site.
COPYRIGHT 2000 BY QUINTESSENCE PUBLISHING CO, INC. PRINTINGOF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART OF The International Journal of Oral & Maxillofacial Implants THIS ARTICLE MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITH- OUT WRITTEN PERMISSION FROM THE PUBLISHER.
Smukler et al
Fig 3 At stage 2 surgery, the e-PTFE
site. Note the fracture of thin, vulnerable ridge, with holes trephined in the buccal plate. Some of the holes will have corti- extraction site. The width of the ridgehas been maintained.
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Smukler et al
This was immediately fixed in 10% formaldehyde; maturely and were removed at 5 weeks. Socket site preparation was then completed, the selected treatment and ridge augmentation both resulted in implants were placed (Fig 5), and the wounds were ridges of adequate dimension for implant place- closed with vertical and interrupted sutures.
ment. Microscopic examination of the extraction Sutures were removed in 7 days; healing generally site cores did not reveal any inflammatory progressed uneventfully. The same modus operandi response or fibrous encapsulation of particulate was utilized when cores were obtained in the ridge bone. Very little osteoclastic activity was noted augmentation part of the study. Similarly, the cores around the remaining nonvital DFDBA particles; from healed, untreated sites were procured at the rather, those particles still present were sur- rounded by and appeared to be coalesced with Histologic Preparation. Following fixation, the
newly formed bone (Fig 6a). Osteoblastic activity cores were decalcified in nitric acid for 2 weeks.
was observed to still be occurring on some newly The bone specimens were embedded in paraffin; formed bone surfaces, indicating a persisting cut serially, in a longitudinal plane, to a thickness remodeling process (Fig 6b). The newly formed of 6 to 8 µm; and stained with hematoxylin and bone was woven, woven undergoing lamellation, eosin and toluidine blue in preparation for micro- or lamellar with secondary osteons being present scopic evaluation. Only the 6 central sections in the mineral phase (Fig 7a). In some sections, obtained from each core were used for compara- basophilic staining material was noted, sometimes tive study. This selection was made in an attempt eccentrically placed in lacunae, within the DFDBA to minimize the inclusion of artifacts related to the particles near their peripheries and adjacent to harvesting process, which were more likely to newly formed bone (Fig 7b). This material appear on the surfaces of the cores. In addition, it appeared to resemble the eccentrically placed was assumed that these sections would be more nuclei within newly formed vital bone.
The cores from the untreated, healed sites Histomorphometric Analysis. The 2 most cen-
exhibited the trabecular bone pattern typically tral sections of each core were evaluated histomor- seen in alveolar bone, with large marrow spaces phometrically by the same person, who was filled with adipose-type tissue usually seen at blinded. The microscopic slides were viewed on a maturity (Fig 8). The experimental histologic sec- Nikon FXA microscope with a digital analytic tions seemed to reveal a more compact picture, interface (MicroVideo Instruments, Avon, MA) with new bone formation on and about the endur- The microscope was attached to a video camera, which was linked to a computer, the software used appeared to be smaller and scarcer; some con- being Image Pro+ (North Reading, MA). The tained a mature adipose cellular arrangement, amounts of bone, marrow, and DFDBA particles while others exhibited an apparently more active within a given field were measured and expressed in pixels. The average number of fields for each section analyzed was 5.53 (SD 2.67). The magnifi- revealed essentially the same picture. The cortical cation used was 200 ϫ. The trabecular bone vol- columns were still recognizable histologically.
ume (TBV) index28 was used to establish the ratio They appeared to be virtually unchanged, with between trabecular bone and marrow spaces.
only early signs of cellular activity seen in isolated Photographic Data Collection. At strategic times
areas. Newly formed bone was present and in inti- during the treatment, 1-to-1 35-mm photographs mate contact with the surfaces of the cortical were taken to permit evaluation of clinical results and to help ensure that cores were always taken Histomorphometrically, the TBV for the maxil- from the center of a regenerated site (Figs 1, 4a, and lary test cores was 55.03% (SD = 15.02), while 5). Reference to pretreatment photographs permit- that for maxillary untreated sites was 57.33% (SD ted verification of ridge width maintenance in the = 11.37) (Fig 11, Table 2). In the mandible, the treated sites. Measurements were not made, as this TBV for the experimental areas was 56.60% (SD = 32.77) and 40.95% (SD = 2.76) for theuntreated areas (Fig 12, Table 3). The DFDBA still present in the specimens was 8.7% (SD =7.58) for the maxillary and 2.45% (SD = 1.04) for Primary closure was achieved in all surgical proce- dures, the postoperative period being generallyuneventful. Two membranes became exposed pre- COPYRIGHT 2000 BY QUINTESSENCE PUBLISHING CO, INC. PRINTINGOF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART OF The International Journal of Oral & Maxillofacial Implants THIS ARTICLE MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITH- OUT WRITTEN PERMISSION FROM THE PUBLISHER.
Smukler et al
Photomicrograph demonstrating a large amount of new High-power view (ϫ400) of outlined area in Fig 6a, bone (nb) formation surrounding DFDBA particles (d) in a 21- rotated 90 degrees counterclockwise. Note DFDBA particles (d) month postoperative maxillary extraction site specimen (tolui- surrounded and coalesced with new bone. Note cellular activ- dine blue stain, original magnification ϫ200).
Photomicrograph representing newly formed bone of High-power view of area outlined in Fig 7a. Note woven and lamellar nature in a mandibular ridge augmentation woven and lamellar bone, primary osteons, and occurrence of at 8 months (hematoxylin and eosin, original magnification what could be nuclei in DFDBA particle (arrows) (hematoxylin and eosin, original magnification ϫ400).
core from a nonfunctional, untreatededentulous maxillary area. Compare therelative amounts of bone and marrowspace sizes with those in Fig 9 (hema-toxylin and eosin, original magnification mm core from a treated maxillary socketsite after 9 months of healing. Note thedenser appearance, scarcer and smallermarrow spaces, as compared to Fig 8(hematoxylin and eosin, original magnifi-cation ϫ40).
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Photomicrograph illustrating a cortical column (cc) surrounded by newly formed bone (nb) in an 8-monthmandibular ridge augmentation. The asterisk (*) indicates whatcould be an osteocyte surrounded by bone in the otherwiseunaltered cortical column (hematoxylin and eosin, originalmagnification ϫ400).
Bar graph comparing the TBV in test and untreated Bar graph comparing the TBV in test and untreated COPYRIGHT 2000 BY QUINTESSENCE PUBLISHING CO, INC. PRINTINGOF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART OF The International Journal of Oral & Maxillofacial Implants THIS ARTICLE MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITH- OUT WRITTEN PERMISSION FROM THE PUBLISHER.
Smukler et al
Discussion
genic” tissues from “undemineralized” allogeneicbone implants, Urist et al30 described some The present study appears to confirm that basophilic staining elements in some of the osteo- DFDBA can be used to successfully treat sockets cyte lacunae. These elements may merely be a fea- ture of nonvital bone implants. Urist et al30 also implants.2,3,16,18 It also corroborates the findings stated that all the treated and untreated allogeneic that utilization of particulate DFDBA, in conjunc- or autogenous implants used in their study exhib- tion with the principles of guided tissue regenera- ited empty lacunae within the same period after tion for the treatment of extraction sockets, will implantation. In addition, Urist in 198031 again result in the gradual replacement of the allograft stated that lacunae of implanted decalcified allo- by newly formed bone.3,18 The finding that bone grafts were predominantly empty and may remain formation takes place in an appositional manner so for extended periods of time. The findings of on and around the allograft particles verifies the empty lacunae in the remaining allograft particles findings of others and tends to substantiate a con- in the present study tend to agree with this.
ductive role for the DFDBA particles.3,7,17,18 The The observation that the experimental cores fact that osteoblastic activity was still occurring presented a more compact picture than the cores on the surfaces of the newly formed lamellar bone from the untreated healed areas is probably merely indicates that active remodeling of the DFDBA an aggregation of the new bone formation on and particles and bone formation continued to take around the remaining DFDBA particles and the place for up to 23 months in this study, a phe- sparser and smaller number of marrow spaces.
nomenon also noted by others.3,17,18 It is note- Whether this phenomenon would persist as the worthy that Simion et al18 were still able to iden- grafts mature or whether the new bone would tify, in human peri-implant tissue, apparently come to more closely resemble bone found in the unaltered DFDBA particles some 4 years after untreated sites still needs to be determined.
placement. In more apical portions of the same The histomorphometric analysis revealed that specimen, DFDBA particles could be seen com- the TBV for the maxillary cores was 55.03% in the pletely embedded in bone matrix and still show- experimental sites and 57.33% in the untreated ing signs of ongoing mineralization. This would sites. Similarly, the mean TBV for mandibular appear to indicate that allograft reconstitution or experimental cores and cores from untreated sites replacement may take many years to complete.
was 56.60% and 40.95%, respectively. It is appar- It was not possible to corroborate the presence ent that the amount of bone present in grafted of mineralization nodules within the DFDBA parti- areas is similar to that found in nongrafted, non- cles.16 However, the occasional appearance of functional edentulous ridge sites. The percentage of deeply stained basophilic material in osteocyte DFDBA particles still present in the maxillary test lacunae, in the most peripheral portions of the specimens was 8.70%, as opposed to 2.45% in demineralized particles nearest to adjacent new mandibular specimens. This difference may be the bone formation, which may be osteocyte nuclei, result of a more rapid reconstitution of the DFDBA was noteworthy. This may permit the assumption particles in the mandible, or there may also be indi- that some sort of ongoing creeping substitution of vidual biologic variations in response to allograft the graft with new bone may be occurring.
placement. The small sample size does not permit a How these events take place would be difficult to explain, but as Zhang et al29 suggest, they may The standard deviations for the maxillary test be related to the stimulating effect of residual cal- and untreated specimens were large (15.02 and cium levels in allografts, or the degradation of 11.37, respectively), but in the mandible the even organic matrix (collagen/proteoglycan), which may larger SD for the experimental core (32.77) was diffuse from the implant-stimulating cellular much greater than that of the untreated areas (SD = chemotaxis into the implant. Zhang et al further 1.25). It is noteworthy that among the 4 mandibu- suggest that the degraded matrix could also act as lar test specimens, 1 of the 2 sides with exposed a site to which cells attach and receive appropriate membrane became infected, resulting in very poor regulatory signals. Growth factor release may also bone formation (14.0%). If this site is excluded be involved in cellular infiltration, differentiation, from the analysis, the TBV for the mandibular test and establishment of a matrix that facilitates cores would be 70.80% (SD = 20.03), suggesting appropriate cell infiltration. However, it should be an even more marked difference from the untreated noted that in an investigation of chemical and sites. The large differences seen in both control and “autodigestive” methods to remove “alloanti- experimental data for most parameters examined COPYRIGHT 2000 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING 414 Volume 14, Number 3, 1999
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could well be a reflection of the small sample size Conclusions
or perhaps indicate a biologic variation that is com-mon in nonfunctioning alveolar bone.
Based on the findings and within the limits of this The value of DFDBA as an additive in bone histologic and histomorphometric study, it may be regeneration procedures has also been questioned by Becker et al.19,24,32 The same authors claim thatDFDBA has no inductive effect in promoting bone 1. In human extraction sockets, commercially formation in human extraction sockets, which available DFDBA, in conjunction with cell they found healed, with nonvital bone particles occlusive barrier membranes, appears to play a being surrounded by connective tissue. Sockets positive conductive role in new bone formation.
treated with autologous bone grafts, on the other 2. Histomorphometric analysis indicates similar hand, exhibited healing with vital woven bone.
trabecular bone volume in untreated sites and Other studies20–23 agree with these findings. Stud- extraction sockets grafted with DFDBA, when ies that investigated the properties of particulate guided bone regeneration principles are fol- human allografts have demonstrated, in ectopic lowed. The same applies to edentulous ridges sites or when gaps in bone are bridged, that the allografts do exhibit inductive properties.26,27 3. The new bone growth appears to be apposi- Zhang et al,33 in investigating the osteoconductiv- tional, and the DFDBA particles appear to undergo a creeping reconstitution that may take implanted into ectopic sites in athymic mice, more many months, if not years, to complete.
recently confirmed an inductive role for human 4. These results do not offer conclusive evidence particulate allograft. None of these studies used regarding the osteoinductive capacity of com- the principles of guided tissue regeneration, where mercially available particulate bone allografts.
cell occlusive membranes are used in conjunctionwith allograft placement as a basis for treatment.
The effect of this approach on induction needs to Acknowledgments
In addition, Schwartz and coworkers34 have The authors are indebted to Mr Tony Chin for the preparation shown that human particulate allografts obtained of the histology and to Dr Dana T. Graves for use of equipmentfor the histomorphometric analysis.
from different bone banks vary in biologic activitywhen placed in ectopic sites. This variation has References
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