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Extraction Sockets and Implantation of Hydroxyapatites With Membrane Barriers A Histologic Study

Froum, Stuart DDS*; Cho, Sang-Choon DDS; Elian, Nicolas DDS; Rosenberg, Edwin DDS§; Rohrer, Michael DDS||; Tarnow, Dennis DDS

Author Information
doi: 10.1097/01.ID.0000127524.98819.FF
  • Free


As a result of the bone resorption and soft tissue shrinkage that occurs after routine atraumatic tooth extraction, ideal implant placement and implant esthetics are often compromised. Controlled clinical studies have documented an average of 4.4 mm of horizontal and 1.2 mm of vertical bone resorption 6 months after tooth extraction. 1,2 Other studies have documented significant dimensional changes in the surrounding alveolar bone after extraction procedures. 3–5 In 1 study, the incidence of anterior ridge deformities in partially edentulous patients was reported to be 91%. 6

Various materials have been used to prevent or minimize ridge collapse after tooth extraction in an attempt to improve implant placement and the subsequent esthetics of the final implant prosthesis. The use of xenografts (bovine bone) 7,8 and alloplasts (including bioactive glass 9,10 and calcified copolymer 11–13) have been shown both clinically and histologically to improve bone quality and quantity of the healed extraction socket before implant placement. Use of membrane barriers with allografts, 14 with bone replacement materials (BRM), 15,16 and BRM or bone grafts combined with calcium sulfate 17,18 have also been advocated as immediate socket treatment to minimize bone resorption and augment existing bone for implant placement.

The use of nonabsorbable and absorbable membrane barriers at the time of tooth extraction have also demonstrated the ability to reduce hard tissue resorption. 1,2 However, the concept of socket preservation with grafts, bone substitutes, and/or membrane barriers is not without controversy. Two separate studies reported that decalcified freeze-dried bone, with and without barrier membranes, bovine bone, and autogenous bone when implanted in healing extraction sockets interfered with normal healing and did not result in any increased bone-to-implant contact. 19,20

Recently, an acellular dermal matrix allograft (ADMA) was introduced as a substitute for autogenous connective tissue grafts for various periodontal, peri-implant, and extraction socket treatments. Although the cellular components of the allograft are removed, the ultrastructural integrity of the extracellular matrix is maintained. 21–23 Therefore, the use of ADMA to increase the zone of attached gingiva around teeth and dental implants, 24–27 treat gingival recession defects, 28–33 cover submerged implants that have been immediately inserted into fresh extraction sockets, 34 and in socket preservation treatment to decrease loss of ridge height and width after tooth extraction 35,36 has been described.

The use of guided bone regeneration with nonabsorbable ePTFE membranes 1 and absorbable membranes 2 immediately after tooth extraction have demonstrated superior clinical results in 2 separate studies, both using a nonfilled extraction socket as the healing control. Both studies attempted primary closure of the wound over the membrane barrier. However, in 3 test patients using expanded polytetrafluoroethylene (ePTFE) membranes, exposure of the membrane produced results with “similar dimensional changes as controls.” 1 A surgical technique has been described using a high-density PTFE membrane and particulate bone replacement material without primary closure to enhance socket healing. The author noted that this technique facilitates the preservation of keratinized mucosa and gingival architecture. 15 It is therefore of interest to see if ADMA and/or ePTFE barriers are able to produce an improved healing result in fresh extraction sockets when primary coverage is purposely not attempted.

The purpose of this pilot study was to compare, and histologically evaluate, the healing of extraction sockets implanted with either an absorbable or nonabsorbable hydroxyapatite and covered by an ADMA or an ePTFE membrane.

Materials and Methods

Sixteen 16 teeth scheduled for extraction, for periodontal or prosthetic reasons, and replacement with an implant were selected in 15 patients (9 males, 6 females) with an age range of 26 to 71 years (average, 48.1 years) who presented to the Ashman Department of Implant Dentistry at New York University Kriser Dental Center. The diagnosis of these teeth for extraction was confirmed by 2 separate instructors on faculty who were not part of the study.

All patients met the established physical and psychologic criteria for implant treatment in the Department of Implant Dentistry. In addition, patients did not have any medical conditions and were not taking any medications that were associated with a compromised bone healing response (ie, diabetes, autoimmune dysfunction, prolonged cortisone therapy, or chemotherapy). Pregnant women, or women intending to become pregnant within 1 year of the start of the study, were excluded from consideration. All patients were nonsmokers or previous smokers who had not smoked for at least 6 months. All patients had no known allergy to tetracycline and had not received any antibiotic over the previous 6 months. Patients were given an explanation of the nature of the study and, after expressing a wish to participate, they signed a written consent form before their participation. The informed consent and instruction to patient forms as well as the study protocol were approved by the University Committee on Activities Involving Human Subjects.

Participating patients were told that if they decided to discontinue their participation in the study at any time, they could continue being treated at New York University Dental Center as a regular clinic patient.


The measurement techniques used have been previously described. 9 To briefly review, before extraction, radiographs, impressions, and diagnostic casts were taken. A template was then fabricated on the study model, including at least 1 tooth anterior or posterior to the hopeless tooth. A light-cured resin material was used to fabricate the template. The crown of the hopeless tooth was cut off on the study model and a guide hole was drilled with a 3 × 10-mm drill through the template directly above the outline of the root on the model. A metal ring was placed in the hole and resin was added around the ring to stabilize its position. At the time of implant surgery (6–8 months after extraction), the template was again positioned to obtain a histologic core from the identical site.

Surgical Protocol

After administration of local anesthesia, crestal, intrasulcular, and where necessary, vertical incisions were made to expose the involved roots and alveolar crest. Full-thickness buccal and lingual flaps were raised and split apically with sharp dissection to adequately view the sockets and allow sufficient flap release to obtain closure (primary closure was not attempted or obtained). After extraction of the tooth, the sockets were debrided, measured, and decorticated with a half-round burr under copious irrigation. After tooth extraction, those sockets with buccal plate bone loss ≥5 mm were included in the study. Thus, each of the sockets treated had a combined 3- to 4-wall configuration. Treatment selection was then made randomly from sealed envelopes prepared by a statistician. Of the 16 sockets treated, 8 sockets received absorbable hydroxyapatite bone substitutes. Four of these sites were covered with ADMA membranes and the 4 others covered with ePTFE membranes. Eight additional sockets received non-absorbable anorganic bovine bone substitutes. Four of these sites were covered with ADMA membranes and the other 4 covered with ePTFE membranes (Fig. 1–8). Four treatment groups were therefore established as follows:

Fig. 1.
Fig. 1.:
After debridement of the extraction socket on tooth no. 9, the acellular dermatic matrix allograft was fitted and reflected to the lingual. The socket was filled with absorbable hydroxyapatite.
Fig. 2.
Fig. 2.:
The ADMA was then secured buccally under the periosteum.
Fig. 3.
Fig. 3.:
The flap was sutured with no attempt at primary closure.
Fig. 4.
Fig. 4.:
Six weeks postsurgery, the ADMA membrane remains in place with surface sloughing observed.
Fig. 5.
Fig. 5.:
Three months postsurgery, the flap margins have migrated over the ADMA.
Fig. 6.
Fig. 6.:
The extraction socket of tooth no. 13 after debridement.
Fig. 7.
Fig. 7.:
The socket is filled with anorganic bovine bone (ABB).
Fig. 8.
Fig. 8.:
The ePTFE membrane is secured over the ABB and the flap suture with absorbable vertical mattress sutures.
  1. Fill with absorbable hydroxyapatite (AH) and covered with ADMA;
  2. Fill with AH and covered with an ePTFE membrane;
  3. Fill with anorganic bovine bone (ABB) and covered with ADMA; and
  4. Fill with ABB and covered with an ePTFE membrane.

The AH consisted of a low-density 100% pure synthetic hydroxyapatite with a particle size ranging from 250 to 420 μm (OsteoGraf R/LD; Dentsply, Lakewood, CO). The ABB was a natural anorganic bovine-derived microporous hydroxyapatite (100% protein-free) with a particle size ranging from 250 to 420 μm (OsteoGraf R/N300; Dentsply). These bone substitute particles were placed into the socket to the level of the interproximal bone and covered with either ADMA or ePTFE membranes. The ADMA was obtained from tissue bank skin and was processed before freeze-drying to remove the entire epidermal layer superficial to the basement membrane, removing dermal cellular elements (Alloderm Life Cell Corp., The Woodlands, TX). The non-absorbable membrane was composed of ePTFE (Gore-Tex Regenerative material, oval 4 or 6; W.L. Gore & Associates, Inc., Flagstaff, AZ).

In all cases, the ADMA or ePTFE membranes were shaped to completely cover the socket, extend 4 to 5 mm apical to the buccal and lingual walls, and be located 1 to 2 mm from the adjacent teeth. The barriers were then stabilized by “tucking” them under the buccal and lingual periosteum and connective tissue that had been separated from the bone with a small periosteal elevator. The ADMA barriers were placed with the connective tissue side facing the socket and the basement membrane side (smooth side) facing the oral cavity.

In the cases in which the barriers were not stable after shaping and placement, they were sutured with 5-0 absorbable suture (5-0 coated Vicryl sutures; Ethicon, Inc., Somerville, NJ) to the remaining periosteum at the apical part of the flap. The mucoperiosteal flaps were sutured with 4-0 silk (Silk Black braided 4-0; Ethicon, Inc.), ePTFE (Gore-Tex suture CV-5, Gore-Tex; W.L. Gore & Associates, Inc.), or absorbable sutures (4-0 chromic gut; Ethicon, Inc.) using interrupted and vertical mattress sutures. However, no attempt was made to cover the membrane barriers. The temporary prosthesis was relieved before insertion. Patients were placed on 100 mg doxycycline beginning at least 1 hour before surgery and continuing for 13 days after surgery. Patients were also prescribed 0.12% chlorhexidine rinses (Peridex; Zila Pharmaceuticals, Inc., Phoenix, AZ) twice a day beginning the day of surgery and continuing until the time of membrane removal. Patients were seen weekly for 4 weeks and then once a month to monitor healing until the barrier was removed. At these visits, the tissue around the membrane was examined for evidence of inflammation, infection (exudate), or exfoliation of the membrane. The membranes and tissue were irrigated with a syringe filled with Betadine followed by 0.12% chlorhexidine and concluding with 0.9% saline. When inflammation was detected, patients were placed on 100 mg doxycycline once a day for 2 to 4 weeks. When infection or exudate was detected, the membrane barriers (ADMA or ePTFE) were removed and the time of removal recorded (Table 1).

Table 1
Table 1:
Histomorphometric Results of the 16 Extraction Sockets

Six to 8 months after extraction socket surgery, an implant of appropriate size was placed in the healed socket. At time of implant site preparation, the template was again placed and a core of bone 2.0 mm × 7.0 mm long was obtained. The cores were coded and sent to the Hard Tissue Research Laboratory at the University of Minnesota School of Dentistry. The processing and histomorphometric measurements were performed by an investigator who had no knowledge of the treatment rendered. The cores were stained with Stevenel’s blue/van Gieson’s picro fuchsin and histomorphometrically analyzed for bone and soft tissue. Processing and analysis of the specimens using a nondecalcified technique has been described. 37–39 Values were then reported using a grid overlay for total bone material, percent connective tissue (%CT), and percent residual implant materials (%RIM).


Histomorphometric results are presented in Table 1 of the 16 extraction sockets covered with either ADMA or ePTFE barriers and filled with an AH or a nonabsorbable ABB. Clinically, all sockets exhibited a normal healing response at the time of implant placement and core removal. The ADMA barriers exhibited surface sloughing within 2 to 4 weeks post-placement. All at but one site, the ADMA was not evident by the 12-week follow-up period. No patient reported knowledge of the barrier exfoliating at those time periods (Figs. 4 and 5). However, at 1 site in the ADMA group and at 6 sites in the ePTFE group, it was necessary to remove the barriers at various times before implant placement because of infection (exudate) present at the surgical site. The ADMA barrier was removed 6 weeks postplacement and the 6 ePTFE barriers were removed from 4 to 16 weeks after placement. In all cases, removal was accomplished by deepithelialization of the inner layer of the overlying flap and lifting the barrier with a periosteal elevator and a hemostat. In all except 2 cases (ePTFE membranes), suturing of the overlying flap was not required. In these 2 cases, ePTFE sutures were used to suture the flap over the healing tissue. No attempt was made to de-bride or remove the tissue under the membrane barrier.

Histology of the cores from sockets covered with ADMA and filled with AH showed an average vital bone of 34.5% (range, 19–57%), an average marrow and connective tissue of 61.8% (range, 40–81%), and an average residual graft material of 4% (range, 0–11%). Bone present at these sites was 100% vital and ranged from 19% to 57%. Evidence of AH particles were still present in all sections but in most specimens appeared separate and distant from the vital bone. In other sections, these particles were incorporated into new bone as well as being separate from vital bone (Figs. 9 and 10). Histology of the sockets covered with ADMA and filled with ABB showed an average vital bone of 41.7% (range, 19.5–62.4%), an average marrow and connective tissue of 45.5% (range, 34–63%), and an average residual graft material of 12.2% (range, 1–30.6%). Particles of ABB were surrounded by vital bone incorporating the particles into a well-formed cancellous bone pattern (Figs. 11 and 12). Histology of sockets covered with ePTFE membranes and filled with AH showed an average vital bone of 27.6% (range, 14–40.1%), an average marrow and connective tissue of 60.5% (range, 43.5–69.6%), and an average residual graft material of 11.9% (range, 6–19%). Bone present at these sites was 100% vital. All sections contained remaining particles of AH, most surrounded by connective tissue and a few others in close proximity, even fusing with the bone (Figs. 13 and 14). Histology of the cores from sockets covered with ePTFE membranes and filled with ABB showed an average vital bone of 17.8% (range, 10.6–25%), an average marrow and connective tissue of 60.7% (range, 42–75.4%), and an average residual graft material of 21.4% (range, 14–33%). The bone present at these 4 sites was 46.2%, 88.2%, 100%, and 100% vital, respectively. Active new bone formation was seen around most of the remaining ABB particles with the beginning of bridging of particles by vital bone (Figs. 15 and 16). The average percentage vital bone in the 8 sockets covered with ADMA was 38% compared with an average percentage vital bone of 22.7% in the 8 sockets covered with ePTFE membrane barriers (Table 2).


Table 2
Table 2:
Average Percent of Vital Bone in Sockets Covered With Acellular Dermal Matrix Allograft (ADMA) or Expanded Polytetrafluoroethylene (ePTFE) Membranes and Filled With Absorbable Hydroxyapatite (AH) or Anorganic Bovine Bone (ABB)
Table 3
Table 3:
Average Percent of Vital Bone in Healed Single vs. Multirooted Sockets
Fig. 9.
Fig. 9.:
Seven-month low-power section of a core of bone from a socket treated with ABMA and AH. Vital bone measured 37%. Particles of AH remain and are seen within bone and surrounded by connective tissue (original magnification ×: Stevenel’s Blue/van Gieson’s picro fuchsin stain).
Fig. 10.
Fig. 10.:
High-power view of an area in the previous figure showing particle of AH not completely resorbed and totally incorporated to the vital bone (original magnification ×20: Stevenel’s Blue/van Gieson’s picro fuchsin stain).
Fig. 11.
Fig. 11.:
A low-power histologic section of a core of bone obtained 6 months postgrafting with ABMA and ABB. Vital bone measures 48.7%. The bone and ABB form a cancellous bone pattern with vital bone bridging among the ABB particles (original magnification ×4: Stevenel’s Blue/van Gieson’s picro fuchsin stain).
Fig. 12.
Fig. 12.:
A high-power histologic view of an area of Figure 11 showing ABB particles completely surrounded by vital bone. The green-staining material in contact with the particles on the right is osteoid, which is becoming vital bone (original magnification ×20: Stevenel’s Blue/van Gieson’s picro fuchsin stain).
Fig. 13.
Fig. 13.:
Low-power histologic section of a core of bone obtained 8 months postgrafting with ePTFE and AH. AH particles remain, most of which are separate from vital bone, although some are fused to bone. Vital bone measured 24.3% (original magnification ×4: Stevenel’s Blue/van Gieson’s picro fuchsin stain).
Fig. 14.
Fig. 14.:
A high-power histologic view of an area of Figure 13 showing unabsorbed particles of AHH. The particle on the left is separate from the new bone and the one on the right is fusing with vital bone (original magnification ×20: Stevenel’s Blue/van Gieson’s picro fuchsin stain).
Fig. 15.
Fig. 15.:
Low-power histologic section of a core of bone obtained 7 months postgrafting with ePTFE and ABB. Most of the particles of ABB are surrounded or in contact with osteoid or new vital bone. Vital bone measured 12.9% (original magnification ×4: Stevenel’s Blue/van Gieson’s picro fuchsin stain).
Fig. 16.
Fig. 16.:
A high-power histologic view of an area of Figure 15 showing particles of ABB surrounded by vital bone. New bone formation (green stain) is also evident (original magnification ×20: Stevenel’s Blue/van Gieson’s picro fuchsin stain).

Because of the small number of specimens in the 4 groups, statistical analysis was not possible.


Attempts to prevent or minimize postextraction bone resorption problems include:

  1. Immediate placement of an implant in the extraction socket.
  2. Immediate implant placement and use of a bone graft or bone substitute in the extraction socket.
  3. Placement of various materials immediately after tooth extraction to fill and/or cover the socket in an attempt to prevent resorption. The implant is then placed in a delayed protocol following socket healing.

An extensive literature review of human studies reported high survival rates after immediate implant placement with a variety of implant types and variable follow-up periods. 40 However, these studies did not address the amount of vertical or horizontal postimplant resorption of the buccal or lingual plates of bone. Although 1 human study 41 reported on bone implant contact of immediately placed implants, crestal bone resorption was not specifically studied. Another study evaluated the effect of membrane (ePTFE) placement on ridge width in a dog model comparing nonmembrane-treated implant sites as controls. The authors noted a trend of a greater increase in ridge width in sites treated with membranes than control sites. However, the authors also noted that “ridge width measurements were not taken from standardized points and consequently there is a high probability of measurement error.” 42 Another animal study 43 evaluated bone healing around implants placed into simulated extraction defects of varying widths in 10 mongrel dogs. Although clinically, all test and control sites healed with complete bone fill in the defect, histologically, as the gap around the implants widened, bone-to-implant contact decreased, and the point of the highest bone-to-implant contact shifted apically. Again, there were no measurements made to determine if and how much bone resorption took place during the healing period. It is evident that although treatment with immediately placed implants with or without additional augmentation material seems a viable method of ridge preservation, there is a paucity of measurement proof to substantiate this premise. Recently, a study was performed around 15 immediately placed implants into extraction sockets. 44 After implant placement, measurements were made of the distance from the coronal border of the buccal to the coronal border of the lingual plate of bone. No membranes or filling materials were used and primary closure was obtained in all cases. At the time of second-stage surgery, 6 months postimplantation, these measurement were repeated. The mean buccal to lingual distance decreased from an initial 10.5 mm ± 1.52 (after implant placement) to 6.8 mm ± 1.33 (6 months postimplantation). Thus, the average horizontal bone resorption after immediate implant placement was 3.7 mm (range, 2–5 mm). This is slightly less that what was reported for the healed extraction sockets in the control group (no membrane, no fill, primary closure) in a previous study. 1

Membrane barriers have been successfully used in the treatment of periodontal defects and in ridge augmentation procedures before implant placement. 45–55 One study on 26 subjects with mandibular class II furcation defects treated with ePTFE barriers concluded that “similar improvement in all clinical and surgical parameters” occurred in both the prematurely exposed and the fully submerged groups. 46 A technique for immediate implant insertion was described that advocated placement of an ePTFE barrier over the implant without primary flap coverage “because the membrane is, in effect, taking the place of the flap closure.” 56 The membrane remained exposed and in place for “approximately 1 month” before removal. However, ePTFE membrane exposure in cases of ridge augmentation occurred in a number of studies requiring early removal of the barriers and resulting in a compromised result in many cases. 47–49 Buser, Jovanovic, and Mellonig reported membrane exposure requiring early removal in 6.3% to 51% of cases treated. 47–49

In an attempt to prevent membrane exposure vertical and periosteal-releasing incisions, coronal flap advancement, and tension-free primary closure are recommended. These procedures result in a compromised vestibule and reduce the amount of keratinized tissue which oftentimes requires additional soft tissue surgical correction. 14 In the current study, to avoid the secondary complications listed here, no attempt at primary closure of the tissue covering the extraction socket was attempted.

The results of this study show a trend toward greater vital bone present in the ADMA-covered sites compared with the ePTFE-covered sites (38% vs. 22.7%). This trend was consistent whether comparing ADMA covering absorbable hydroxyapatite versus ePTFE covering the same AH (34.5% vs. 27.6%) or ADMA covering anorganic bovine bone versus ePTFE covering the same ABB (41.7% vs. 17.8%). It also appears that better results were obtained, regardless of the barrier, when ABB was used as the fill material. This difference in results favoring ADMA barriers could be the result of the fact that exposure of this membrane is less critical to success than exposure of ePTFE membranes. In fact, many authors (Buser et al., 47 Simion et al., 55 Wachtel et al., 57 Jovanovic et al., 48,58 Becker et al., 59 Simion et al., 60 Buser et al., 61 Jovanovic and Nevins, 62 and Nowzari and Slots 63) stressed the importance of keeping the ePTFE barriers submerged to obtain optimum results. The latter article (Nowzari and Slots 63) reported colonization of bacteria on the ePTFE membranes that became exposed. This too could have compromised results of ePTFE-covered sockets in the current study. However, the strict recall program and the removal of the 1 ABMA and 6 ePTFE barriers when infection was evident could have allowed positive vital bone formation with the fill materials used in this study despite membrane exposure. However, the population in this study was too small to detect significant differences in results of the membranes retained for longer periods of time as was reported in an experimental study in dogs. 50

It is interesting that in a published case report on 2 successful cases of ridge preservation using ADMA in conjunction with decalcified freeze bone allograft in a fresh extraction socket, the exposed ADMA membranes exfoliated “atraumatically” 3 weeks postinsertion. In a published case report of ADMA used for ridge augmentation, the author noted the importance of completely covering “the acellular dermal matrix with a pedicle ”and keeping it “completely covered during the healing period.” 64 Although no attempt was made to do this in this study, except for 1 barrier, which was removed 6 weeks postplacement, all 7 of the other ADMA barriers showed surface sloughing 2 to 4 weeks postoperatively and then were not evident at 8 weeks, or in some cases by 12 weeks, postsurgery. Because the 7 patients with these ADMA barriers did not report being aware of barrier loss, we must assume the barriers were incorporated into the wound healing (covered by epithelium) or exfoliated without patient knowledge. This contrasts to the 6 of 8 ePTFE barriers, which had to be removed prematurely during the study. This could reflect a better resistance of the ADMA barriers to bacterial colonization with the regimen of postsurgical treatment used in this study. A factor that was not measured in this study was the distance that the flaps were separated after suturing or the amount of exposure of the membranes during the healing phase. There could be a “critical distance” beyond which membrane exposure adversely affects socket healing. However, these variables require more cases, additional measurement parameters, and further investigation.

Although the combination of ADMA and ABB appears to result in the highest percentage of vital bone in this investigation, additional clinical and histologic studies are necessary before any speculation or conclusions are made. Certainly, the advantages of materials that result in significant bone fill of a healing extraction socket without the compromises caused by obtaining primary soft tissue closure warrant further investigation.

It is also evident that this study did not include a negative (no fill) control group. Using the same measurement technique in a previous study, the “no filled” and “no membrane” controls showed an average vital bone fill of 32.4% 6 to 8 months postsocket treatment. 9 One must be cautious with these comparisons because the methodology was different (in the previous study, primary closure was achieved) and the type of tooth (incisor, premolar, molar) and jaw location represent factors that could influence healing and vital bone counts because of differences in the type of bone native to that site.

When analyzing the data on all 16 sites in this study and comparing the results of multirooted (N = 8) with that of single-rooted teeth (N = 8), it is interesting to note that the average vital bone of the former was 34.16% (range, 10.6–62.4%), whereas that of single-rooted teeth was 37.03% (range, 12.9–67%). Although no statistically significant data can be drawn because of the limited sample size, these findings tend to demonstrate the variability of bone fill in human extraction sockets. For example, one might expect to have significantly more dense bone present after extraction socket healing in the anterior area (single-rooted teeth) because the bone is usually denser in nature. However, the healed sockets in this study show similar percentages of vital bone in single- and multirooted healed sockets. This pilot study demonstrates the need for a much larger sample size to more accurately follow the trends in healing responses. Confounding factors, including socket location, use of different graft materials, use of membranes, type of flap closure (or non-closure), and the presence and thickness of the bony walls of the sockets, prevent clear conclusions from being drawn from human socket studies. Therefore, at this point, based on the results of the present pilot study as well as the referenced literature, the operator must make clinical decisions based on the individual situations presented. Clearly, further research with a much larger sample size is indicated to isolate the previously mentioned variables to determine the best course of treatment after tooth extraction.


Extraction socket treatment with ABMA barriers produced more vital bone 6 to 8 months postextraction than did ePTFE membranes, whether placed over AH or nonabsorbable ABB mineral.

The combination of ABMA covering ABB produced the greatest amount of vital bone at 6 to 8 months (41.7%) followed by ABMA covering AH (34.5%), ePTFE covering AH (27.6%), and ePTFE covering ABB 17.8%.

Without primary flap coverage over the extraction socket, 1 of 8 ABMA barriers and 6 of 8 ePTFE barriers had to be removed prematurely because of infection before the 6- to 8-month time period when implants were placed.

This pilot study demonstrates the need for a much larger sample size to more accurately follow the trends in healing responses.


The authors acknowledge the contributions of Hari Prasad, BS, MDT, Research Scientist, University of Minnesota Dental School, for his assistance with the histologic preparation and histomorphometric analysis. This study was supported by a grant from LifeCell, the Woodlands, TX.


The authors claim to have no financial interest in any company or any of the products mentioned in this article.


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Abstract Translations [German, Spanish, Portugese, Japanese]

AUTOR(EN): Stuart Froum, D.D.S.*, Sang-Choon Cho, D.D.S.**, Nicolas Elian, D.D.S.***, Edwin Rosenberg D.D.S.#, Michael Rohrer, D.D.S.##, und Dennis Tarnow, D.D.S.###. * Klinischer Professor und Direktor der klinischen Forschung, Ashman Abteilung für implantatgestützte Zahnheilkunde, Universität New York, Kriser Dentalzentrum, New York, NY. ** Klinischer Assistenzprofessor und Mitglied des wissenschaftlichen Forschungsteams, Ashman Abteilung für implantatgestützte Zahnheilkunde, Universität New York, Kriser Dentalzentrum, New York, NY. *** Leiter des internationalen Forschungsprogramms, Assistenzprofessor, Ashman Abteilung für implantatgestützte Zahnheilkunde, Universität New York, Kriser Dentalzentrum, New York, NY. # Professor für Orthodontie und implantatgestützte Zahnheilkunde, Universität von Pennsylvania, Philadelphia, PA. ## Professor und Leiter, Bereich für Oral und Kieferpathologie, Universität von Minnesota, zahnmedizinische Fakultät, Minneapolis, MN. ### Professor und Vorsitzender, Ashman Abteilung für implantatgestützte Zahnheilkunde, Universität New York, Kriser Dentalzentrum, New York, NY. Schriftverkehr:Stuart J. Froum, DDS, 17 West 54th Street, Suite 1 C/D, New York, New York 10019. Telefon: 212 - 586 - 4209, Fax: 212 - 246 - 7599. eMail:

Extraktionshöhlen und die Implantation von Hydroxylapatit mit Membranbarriere: eine histologische Studie

ZUSAMMENFASSUNG:Einführung: Zielsetzung dieser Pilotstudie war es, die Auswirkungen auf den Heilungsprozess bei Extraktionshöhlen zu untersuchen, wenn ein absorbierbares Hydroxylapatit (AH) und ein nicht absorbierbares anorganisches Rinder-knochenmineral (ARK) zur Reaktion in der Mundhöhle belassen werden. Eine Bedeckung dieser Materialien mit entweder einem azellulären, hautstrukturierten Allotransplantat (AHSA) oder einer erweiterten Polytetrafluoräthylmembranbarriere (ePTFÄ) war vorgesehen. Materialien und Methoden: Bei Zahnextraktionsbehandlungen an 15 Patienten mit mangelhaften Bukkalplatten von 5 mm entstanden insgesamt 16 Zahnhöhlen. Nach dem Zufallsprinzip erfolgte eine Aufteilung der Patienten in vier Behandlungsgruppen. 1. AH bedeckt mit AHSA, 2. AH bedeckt mit einer ePTFÄ-Membran, 3. ARK bedeckt mit AHSA, und 4. ARK bedeckt mit einer ePTFÄ-Membran. Ein Primärüberzug wurde in keinem der Fälle versucht bzw. erreicht. Sechs bis acht Monate nach Zahnex-traktion war die Implantatsetzung vorgesehen. Zu diesem Zeitpunkt wurden histologische Kerne der behandelten Bereiche entnommen. Diese Kernstücke wurden weiter verarbeitet, mit Stevenel-Blau /van Giesonschem Picrofuchsin eingefärbt und mittels histomorphologischen Messungen analysiert. Prozentuale Anteile von vitalem Knochen, Gewebe und Mark sowie verbleibenden Transplantatartikeln in den Gesamtkernen wurden ermittelt. Ergebnisse: Durchschnittlich betrug der Anteil an vitalem Knochengewebe 34,5 % (AH mit AHSA), 41,7 % (ARK mit AHSA), 27,6 % (ePTFÄ und AH) und 17,8 % (ePTFÄ und ARK). In den mit AHSA bedeckten acht Extraktionshöhlen fanden sich durchschnittlich 38 % an vitalem Knochen, während die weiteren acht, mit ePTFÄ-Membranbarrieren bedeckten Höhlen nur 22 % an vitalem Knochengewebe aufwiesen. Schlussfolgerungen: Augrund der geringen Anzahl an Untersuchungsproben innerhalb der vier Gruppen war keine statistische Analyse möglich. Als Ergebnisse dieser Pilotstudie können aber die nach sechs- bis achtmonatiger Nachbehandlung weitaus höheren Anteile an vitalem Knochen in den mit AHSA bedeckten Behandlungsbereichen gegenüber den mit ePTFÄ bedeckten Stellen festgehalten werden. Hierbei spielten die unterschiedlichen Knochenwiederher-stellungsmaterialien keine Rolle. Es empfiehlt sich, weiterführende Forschungen anzustellen, um die innerhalb dieser Pilotstudie ermittelten Ergebnisse auf eine eventuell ähnlich lautende Differenz bei Knochengewebe-zu-Implantat-Kontakt nach erfolgter Implantatsetzung zu untersuchen.

SCHLÜSSELWÖRTER: Extraktionshöhle, Barrieremembran, histomorphologische Analyse, absorbierbares Hydroxylapatit, azelluläres, hautstrukturiertes Allotransplantat

AUTOR(ES): Stuart Froum, D.D.S.*, Sang-Choon Cho, D.D.S.**, Nicolas Elian, D.D.S.***, Edwin Rosenberg, D.D.S.#, Michael Rohrer, D.D.S.##, y Dennis Tarnow, D.D.S.###. *Profesor Clínico y Director de Investigación Clínica, Departamento Ashman de Odontología de Implantes, Universidad de Nueva York, Centro Dental Kriser, Nueva York, NY. **Profesor Asistente Clínico e Investigador Científico, Departamento Ashman de Odontología de Implantes, Universidad de Nueva York, Centro Dental Kriser, Nueva York, NY. ***Director del Programa Internacional, Profesor Asistente, Departamento Ashman de Odontología de Implantes, Universidad de Nueva York, Centro Dental Kriser, Nueva York, NY. # Profesor, Periodóntica y Odontología de Implantes, Universidad de Pennsylvania, Philadelphia, PA. ## Profesor y Director, División de Patología Oral y Maxilofacial, Universidad de Minnesota, Facultad de Odontología, Minneapolis, MN. ### Profesor y Jefe, Departamento Ashman de Odontología de Implantes, Universidad de Nueva York, Centro Dental Kriser, Nueva York, NY. Correspondencia a: Stuart J. Froum, DDS, 17 West 54th Street, Suite 1 C/D, New York, New York 10019. Teléfono: 212-586-4209, Fax: 212-246-7599. Correo electrónico:

Cavidades de extracción e implantación de hidroxiapatitas con barreras de membranas: Un estudio histológico

ABSTRACTO:Introducción: El propósito de este estudio piloto fue investigar el efecto en la curación de la cavidad de extracción, cuando un mineral de hueso bovino anorgánico (ABB por sus siglas en inglés) no absorbible y una hidroxiapatita absorbible (AH por sus siglas en inglés) recubiertas con una barrera de membrana de politetrafluoroetileno expandido (ePTFE) o aloinjerto de matriz dérmica acelular (ADMA por sus siglas en inglés) se dejaron expuestas en la cavidad oral. Materiales y métodos: Luego de la extracción del diente se dividieron aleatoriamente un total de 16 cavidades en 15 pacientes con placas bucales deficientes de 5 mm en 4 grupos de tratamiento: 1. AH cubierta con ADMA; 2. AH cubierta con una membrana de ePTFE; 3. ABB cubierta con ADMA; 4. ABB cubierta con una membrana de ePTFE. La cobertura primaria no se intentó ni se obtuvo en ninguna de las 16 cavidades tratadas. Seis a ocho meses luego de la extracción en el momento de la colocación del implante, se obtuvieron núcleos histológicos de los lugares de tratamiento. Estos núcleos fueron procesados, coloreadas con azul de Stevenel/picrofucsina de van Gieson y analizados histomorfométricamente. El hueso vivo, tejido conectivo y médula ósea, y partículas residuales del injerto se calcularon como porcentaje del núcleo total. Resultados: La mediana de hueso vivo fue de 34,5% (AH con ADMA), 41.7% (ABB con ADMA), 27,6% (ePTFE y AH) y 17,8% (ePTFE y ABB). El porcentaje promedio de hueso vivo en las 8 cavidades cubiertas con ADMA fue del 38% comparado con un porcentaje promedio de hueso vivo del 22% en las 8 cavidades cubiertas con barreras de membrana de ePTFE. Conclusiones: Debido al pequeño número de especimenes en los 4 grupos, no fue posible realizar un análisis estadístico. Sin embargo, en este estudio piloto, los sitios cubiertos con ADMA resultaron en una mayor presencia de hueso viso a los 6 a 8 meses luego del tratamiento de la cavidad que los obtenidos en los sitios cubiertos con ePTFE independientemente de los materiales de reemplazo del hueso usados. Se necesitan investigaciones adicionales para determinar si estos resultados muestran una diferencia similar en el contacto entre el hueso y los implantes luego de la colocación del implante.

PALABRAS CLAVES: Cavidad de extracción, barrera de membrana, análisis histomorfométrico, hidroxiapatita absorbible, aloinjerto de matriz dérmica acelular.

AUTOR(ES): Stuart Froum, Doutor em Ciência Dentária*, Sang-Choon Cho, Doutor em Ciência Dentária**, Nicolas Elian, Doutor em Ciência Dentária***, Edwin Rosenberg, Doutor em Ciência Dentária#, Michael Rohrer, Doutor em Ciência Dentária## e Dennis Tarnow, Doutor em Ciência Dentária###. *Professor Clínico e Diretor de Pesquisa Clínica, Departamento Ashman de Odontologia de Implantes, Universidade de Nova York, Centro Odontológico Kriser, Nova York, NY. **Professor Assistente Clínico e Cientista de Pesquisa, Departamento Ashman de Odontologia de Implantes, Universidade de Nova York, Centro Odontológico Kriser, Nova York, NY. ***Diretor de Programa Internacional, Professor Assistente, Departamento Ashman de Odontologia de Implantes, Universidade de Nova York, Centro Odontológico Kriser, Nova York, NY. #Professor de Periodontia e Odontologia de Implantes, Universidade da Pensilvânia, Filadélfia, PA. ##Professor e Diretor, Divisão de Patologia Oral e Maxilofacial, Universidade de Minnesota, Escola de Odontologia, Minneapolis, MN. ###Professor e Chefe, Departamento Ashman de Odontologia de Implantes, Universidade de Nova York, Centro Odontológico Kriser, Nova York, NY. Correspondência para: Stuart J. Froum, DDS. 17 West 54th Street, Suite 1 C/D, New York, New York 10019. Telefone: 212-586-4209, Fax: 212-246-7599. E-mail:

Cavidades de Extração e Implante de Hidroxiapatitas com Membranas Protetoras: um Estudo Histológico

RESUMO:Introdução: O objetivo deste estudopiloto era investigar o efeito na cura da cavidade de extração, quando uma hidroxiapatita absorvível (AH) e um mineral de osso bovino anorgânico não-absorvível (ABB) coberto ou com enxerto aloplástico de matriz dérmica acelular (ADMA) ou com uma membrana protetora de politetrafluoretileno expandido (cPTFE) eram deixados expostos à cavidade oral. Materiais e Métodos: Após a extração dentária, um total de 16 alvéolos em 15 pacientes com placas bucais deficientes de 5 mm era dividido aleatoriamente em 4 grupos de tratamento. 1. AH coberto com ADMA. 2. AH coberto com uma membrana cPTFE. 3. ABB coberto com ADMA. 4. ABB coberto com uma membrana cPTFE. A cobertura primária não foi tentada ou obtida em nenhum dos 16 alvéolos tratados. Seis a oito meses após a extração por ocasião da colocação do implante, núcleos histológicos dos locais do tratamento foram obtidos. Estes núcleos foram processados, manchados com azul de Stevenel/picrofucsina de van Gieson e analisados histomorfometricamente. Osso vital, tecido conjuntivo e medula, bem como partículas de enxerto residual foram relatados como porcentagem do núcleo total. Resultados: O osso vital médio era 34.5% (AH com ADMA), 41l7% (ABB com ADMA, 27.6% (ePTFE e AII) e 17.8% (ePTFE e ABB). A porcentagem média de osso vital nos 8 alvéolos cobertos com ADAMA era de 38%, em comparação com uma porcentagem média de osso vital de 22% nos 8 alvéolos cobertos com membranas protetoras cPTFE. Conclusões: Devido ao pequeno número de espécimes nos 4 grupos, a análise estatística não foi possível. Contudo, neste estudopiloto, locais cobertos com ADMA resultaram em mais osso vital presente 6 a 8 meses após o tratamento do alvéolo do que o obtido no locais cobertos com cPTFE, independente dos materiais para troca de osso usados. Justificase pesquisa adicional para verificar se estes resultados mostram diferença desse tipo no contato osso/implante após a colocação do implante.

PALAVRAS-CHAVE: Extraction socket, membrana protetora, análise histomorfométrica, hidroxiapatitas absovíveis, enxerto aloplástico de matriz dérmica acelular.



extraction socket; barrier membrane; histomorphometric analysis; absorbable hydroxyapatite; acellular dermal matrix allograft

© 2004 Lippincott Williams & Wilkins, Inc.