Extraction Sockets and Implantation of

Hydroxyapatites With Membrane Barriers

A Histologic Study
Stuart Froum, DDS,* Sang-Choon Cho, DDS,† Nicolas Elian, DDS,‡ Edwin Rosenberg, DDS,§
Michael Rohrer, DDS,储 Dennis Tarnow, DDS¶

The purpose of this pilot study was percentage of the total core. The mean
s a result of the bone resorption

A and soft tissue shrinkage that

occurs after routine atraumatic
tooth extraction, ideal implant place-
ment 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 pa-
tients 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 im-
plant prosthesis. The use of xenografts
(bovine bone)7,8 and alloplasts (includ-
ing bioactive glass9,10 and calcified co-
polymer11–13) have been shown both
clinically and histologically to im-
prove bone quality and quantity of the
healed extraction socket before im-
plant placement. Use of membrane
*Clinical Professor and Director of Clinical Research, Ashman
Department of Implant Dentistry, New York University, Kriser
Dental Center, New York, NY.
†Clinical Assistant Professor and Research Scientist, Ashman
Department of Implant Dentistry, New York University, Kriser
Dental Center, New York, NY.
‡Director of International Program, Assistant Professor, Ashman
Department of Implant Dentistry, New York University, Kriser
Dental Center, New York, NY.
§Professor Periodontics and Implant Dentistry University of
Pennsylvania, Philadelphia, Pennsylvania.
储Professor and Director, Division of Oral and Maxillofacial Pathol-
ogy, University of Minnesota, School of Dentistry, Minneapolis,
Minnesota.
¶Professor and Chair, Ashman Department of Implant Dentistry,
New York University, Kriser Dental Center, New York, NY.
ISSN 1056-6163/04/01302-153
Implant Dentistry
Volume 13 • Number 2
Copyright © 2004 by Lippincott Williams & Wilkins
DOI: 10.1097/01.ID.0000127524.98819.FF
to investigate the effect on extraction
socket healing when an absorbable hy-
droxyapatite (AH) and a nonabsorbable
anorganic bovine bone mineral (ABB)
covered with either an acellular dermal
matrix allograft (ADMA) or expanded
polytetrafluoroethylene (ePTFE) mem-
brane barrier were left exposed to the
oral cavity. Following tooth extraction,
a total of 16 sockets in 15 patients with
deficient buccal plates of ⱖ5 mm were
randomly divided into 4 treatment
groups: 1) AH covered with ADMA, 2)
AH covered with an ePTFE membrane,
3) ABB covered with ADMA, and 4)
ABB covered with an ePTFE mem-
brane. Primary coverage was not at-
tempted or obtained in any of the 16
treated sockets. Six to 8 months postex-
traction at the time of implant place-
ment, histologic cores of the treatment
sites were obtained. These cores were
processed, stained with Stevenel’s blue/
van Gieson’s picro fuchsin, and histo-
morphometrically analyzed. Vital bone,
connective tissue and marrow, and re-
sidual graft particles were reported as a
barriers with allografts,14 with bone
replacement materials (BRM),15,16 and
BRM or bone grafts combined with
calcium sulfate17,18 have also been ad-
vocated as immediate socket treatment
to minimize bone resorption and aug-
ment existing bone for implant
placement.
The use of nonabsorbable and ab-
sorbable membrane barriers at the
time of tooth extraction have also
vital bone was 34.5% (AH with ADMA),
41.7% (ABB with ADMA), 27.6%
(ePTFE and AH), and 17.8% (ePTFE
and ABB). The average percentage of
vital bone in the 8 sockets covered with
ADAMA was 38% compared with an
average percentage vital bone of 22% in
the 8 sockets covered with ePTFE mem-
brane barriers. Because of the small
number of specimens in the 4 groups,
statistical analysis was not possible.
However, in this pilot study, ADMA-
covered sites resulted in more vital bone
present 6 to 8 months postsocket treat-
ment than obtained in the ePTFE-
covered sites regardless of bone re-
placement materials used. Further
research is warranted to see if these
results show a similar difference in
bone-to-implant contact after implant
placement. (Implant Dent 2004;13:153–
164)
Key Words: extraction socket, barrier
membrane, histomorphometric analy-
sis, absorbable hydroxyapatite, acellu-
lar dermal matrix allograft
demonstrated the ability to reduce
hard tissue resorption.1,2 However, the
concept of socket preservation with
grafts, bone substitutes, and/or mem-
brane barriers is not without contro-
versy. 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

IMPLANT DENTISTRY / VOLUME 13, NUMBER 2 2004 153

and did not result in any increased
bone-to-implant contact.19,20
Recently, an acellular dermal ma-
trix allograft (ADMA) was introduced
as a substitute for autogenous connec-
tive tissue grafts for various periodon-
tal, peri-implant, and extraction socket
treatments. Although the cellular com-
ponents of the allograft are removed,
the ultrastructural integrity of the ex-
tracellular matrix is maintained.21–23
Therefore, the use of ADMA to in-
crease 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
extraction35,36 has been described.
The use of guided bone regenera-
tion with nonabsorbable ePTFE mem-
branes1 and absorbable membranes2 im-
mediately 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 bar-
rier. However, in 3 test patients using
expanded polytetrafluoroethylene
(ePTFE) membranes, exposure of the
membrane produced results with “simi-
lar dimensional changes as controls.”1 A
surgical technique has been described
using a high-density PTFE membrane
and particulate bone replacement mate-
rial without primary closure to enhance
socket healing. The author noted that
this technique facilitates the preserva-
tion 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 ab-
sorbable or nonabsorbable hydroxyap-
atite and covered by an ADMA or an
ePTFE membrane.
MATERIALS AND METHODS
16
Sixteen teeth scheduled for ex-
traction, for periodontal or prosthetic
154 EXTRACTION SOCKETS AND IMPLANTATION
reasons, and replacement with an im-
plant 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 Depart-
ment of Implant Dentistry at New
York University Kriser Dental Center.
The diagnosis of these teeth for extrac-
tion was confirmed by 2 separate in-
structors 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, pa-
tients did not have any medical condi-
tions and were not taking any medica-
tions that were associated with a
compromised bone healing response
(ie, diabetes, autoimmune dysfunc-
tion, 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 participa-
tion. The informed consent and in-
struction to patient forms as well as
the study protocol were approved by
the University Committee on Activi-
ties 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.
Measurements
The measurement techniques used
have been previously described.9 To
briefly review, before extraction, ra-
diographs, impressions, and diagnos-
tic 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
OF HYDROXYAPATITES
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 sur-
gery (6 – 8 months after extraction),
the template was again positioned to
obtain a histologic core from the iden-
tical site.
Surgical Protocol
After administration of local anes-
thesia, 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 at-
tempted or obtained). After extraction
of the tooth, the sockets were de-
brided, measured, and decorticated
with a half-round burr under copious
irrigation. After tooth extraction, those
sockets with buccal plate bone loss ⱖ5
mm were included in the study. Thus,
each of the sockets treated had a com-
bined 3- to 4-wall configuration.
Treatment selection was then made
randomly from sealed envelopes pre-
pared by a statistician. Of the 16 sock-
ets treated, 8 sockets received absorb-
able 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 mem-
branes (Fig. 1– 8). Four treatment
groups were therefore established as
follows:
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 hydroxy-

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. The ADMA was then secured buccally under the periosteum.
Fig. 3. The flap was sutured with no attempt at primary closure.
Fig. 4. Six weeks postsurgery, the ADMA membrane remains in place with surface sloughing
observed.
Fig. 5. Three months postsurgery, the flap margins have migrated over the ADMA.
apatite with a particle size ranging
from 250 to 420 ␮ m (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 ␮m (Os-
teoGraf R/N300; Dentsply). These
bone substitute particles were placed
into the socket to the level of the in-
terproximal bone and covered with ei-
ther ADMA or ePTFE membranes.
The ADMA was obtained from tissue
bank skin and was processed before
freeze-drying to remove the entire epi-
dermal layer superficial to the base-
ment 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 sepa-
rated from the bone with a small peri-
osteal elevator. The ADMA barriers
were placed with the connective tissue
side facing the socket and the base-
ment 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
IMPLANT DENTISTRY / VOLUME 13, NUMBER 2 2004
sutures; Ethicon, Inc., Somerville, NJ)
to the remaining periosteum at the api-
cal part of the flap. The mucoperios-
teal 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 chro-
mic gut; Ethicon, Inc.) using inter-
rupted and vertical mattress sutures.
However, no attempt was made to
cover the membrane barriers. The
temporary prosthesis was relieved be-
fore 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% chlorhexi-
dine rinses (Peridex; Zila Pharmaceu-
ticals, Inc., Phoenix, AZ) twice a day
beginning the day of surgery and con-
tinuing 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, infec-
tion (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).
Six to 8 months after extraction
socket surgery, an implant of appro-
priate size was placed in the healed
socket. At time of implant site prepa-
ration, 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 histomor-
phometrically analyzed for bone and
soft tissue. Processing and analysis of
the specimens using a nondecalcified
155

Fig. 6. The extraction socket of tooth no. 13 after debridement.
Fig. 7. The socket is filled with anorganic bovine bone (ABB).
Fig. 8. The ePTFE membrane is secured over the ABB and the flap suture with absorbable
vertical mattress sutures.
technique has been described.37–39 Val-
ues were then reported using a grid
overlay for total bone material, per-
cent connective tissue (%CT), and
percent residual implant materials
(%RIM).
RESULTS
Histomorphometric results are
presented in Table 1of the 16 extrac-
tion sockets covered with either
ADMA or ePTFE barriers and filled
with an AH or a nonabsorbable ABB.
Clinically, all sockets exhibited a nor-
mal 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 re-
ported knowledge of the barrier exfo-
liating 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 re-
move the barriers at various times be-
fore implant placement because of in-
fection (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
156 EXTRACTION SOCKETS AND
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 sock-
ets 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 aver-
age 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 incorpo-
rated 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 aver-
age marrow and connective tissue of
45.5% (range, 34 – 63%), and an aver-
age residual graft material of 12.2%
IMPLANTATION OF HYDROXYAPATITES
(range, 1–30.6%). Particles of ABB
were surrounded by vital bone incor-
porating the particles into a well-
formed cancellous bone pattern (Figs.
11 and 12). Histology of sockets cov-
ered with ePTFE membranes and
filled with AH showed an average vi-
tal bone of 27.6% (range, 14 – 40.1%),
an average marrow and connective tis-
sue 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 par-
ticles of AH, most surrounded by con-
nective 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 av-
erage 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 bridg-
ing 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).
Because of the small number of
specimens in the 4 groups, statistical
analysis was not possible.
DISCUSSION
Attempts to prevent or minimize
postextraction bone resorption prob-
lems include:
1. Immediate placement of an implant
in the extraction socket.
2. Immediate implant placement and
use of a bone graft or bone substi-
tute in the extraction socket.
3. Placement of various materials im-
mediately 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
Table 1. Histomorphometric Results of the 16 Extraction Sockets
Early Healing Vital
Barrier Graft Age Removal Period Bone Marrow Remaining
Type Type Initials (yrs) Sites (months) (months) (%) (%) Graft (%)
ADMA AH LM 47 7 8 25 64 11
RZ 56 2 6 19 81 0
LW 63 3 7 37 62 2
WH 71 9 6 57 40 30
ABB PT 45 3 1.5 6 19.5 49.9 30.6
CL 26 18 6 62.4 34 3.6
YL 53 14 6 48.7 35 16.3
IR 57 3 6 36 63 1
ePTFE AH SL 36 11 2 6 32 62 6
LM 47 10 1 8 14 67 19
GH 43 19 4 8 40.1 43.5 16.4
VL 31 4 8 24.3 69.6 6.1
ABB SD 60 14 2 7 10.6 75.4 14
RK 51 8 4 7 12.9 65.4 21.7
WG 50 4 8 25 42 33
GS 33 13 2 7 23 60 17
This table lists histomorphometric results of 16 extraction sockets, 8 covered with the ADMA barrier with either AH or ABP as the socket fill material and 8 covered with the ePTFE barrier with the same
2 socket fill materials. The table shows the percent vital bone, percent marrow, and percent of remaining graft material in each of the 16 cores taken.

rates after immediate implant place- evident that although treatment with terial seems a viable method of ridge
ment with a variety of implant types immediately placed implants with or preservation, there is a paucity of mea-
and variable follow-up periods.40 How- without additional augmentation ma- surement proof to substantiate this
ever, these studies did not address the
amount of vertical or horizontal
postimplant resorption of the buccal or
lingual plates of bone. Although 1 hu-
man study41 reported on bone implant
contact of immediately placed im-
plants, 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 in-
crease 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 probabil-
ity of measurement error.”42 Another
animal study43 evaluated bone healing
around implants placed into simulated Fig. 9. Seven-month low-power section of a core of bone from a socket treated with ABMA and
extraction defects of varying widths in 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).
10 mongrel dogs. Although clinically, Fig. 10. High-power view of an area in the previous figure showing particle of AH not com-
all test and control sites healed with pletely resorbed and totally incorporated to the vital bone (original magnification ⫻20:
complete bone fill in the defect, histo- Stevenel’s Blue/van Gieson’s picro fuchsin stain).
logically, as the gap around the im- Fig. 11. A low-power histologic section of a core of bone obtained 6 months postgrafting with
plants widened, bone-to-implant con- ABMA and ABB. Vital bone measures 48.7%. The bone and ABB form a cancellous bone
tact decreased, and the point of the pattern with vital bone bridging among the ABB particles (original magnification ⫻4: Stevenel’s
highest bone-to-implant contact Blue/van Gieson’s picro fuchsin stain).
Fig. 12. A high-power histologic view of an area of Figure 11 showing ABB particles com-
shifted apically. Again, there were no pletely surrounded by vital bone. The green-staining material in contact with the particles on
measurements made to determine if the right is osteoid, which is becoming vital bone (original magnification ⫻20: Stevenel’s
and how much bone resorption took Blue/van Gieson’s picro fuchsin stain).
place during the healing period. It is

IMPLANT DENTISTRY / VOLUME 13, NUMBER 2 2004 157

 In an attempt to prevent mem-
brane exposure vertical and periosteal-
releasing incisions, coronal flap ad-
vancement, and tension-free primary
closure are recommended. These pro-
cedures result in a compromised ves-
tibule and reduce the amount of kera-
tinized 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 clo-
sure of the tissue covering the extrac-
tion 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
Fig. 13. Low-power histologic section of a core of bone obtained 8 months postgrafting with absorbable hydroxyapatite versus
ePTFE and AH. AH particles remain, most of which are separate from vital bone, although ePTFE covering the same AH (34.5%
some are fused to bone. Vital bone measured 24.3% (original magnification ⫻4: Stevenel’s vs. 27.6%) or ADMA covering anor-
Blue/van Gieson’s picro fuchsin stain).
Fig. 14. A high-power histologic view of an area of Figure 13 showing unabsorbed particles of
ganic bovine bone versus ePTFE cov-
AHH. The particle on the left is separate from the new bone and the one on the right is fusing ering the same ABB (41.7% vs.
with vital bone (original magnification ⫻20: Stevenel’s Blue/van Gieson’s picro fuchsin stain). 17.8%). It also appears that better re-
Fig. 15. Low-power histologic section of a core of bone obtained 7 months postgrafting with sults were obtained, regardless of the
ePTFE and ABB. Most of the particles of ABB are surrounded or in contact with osteoid or new barrier, when ABB was used as the fill
vital bone. Vital bone measured 12.9% (original magnification ⫻4: Stevenel’s Blue/van Gie- material. This difference in results fa-
son’s picro fuchsin stain). voring ADMA barriers could be the
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 magnifi-
result of the fact that exposure of this
cation ⫻20: Stevenel’s Blue/van Gieson’s picro fuchsin stain). membrane is less critical to success
than exposure of ePTFE membranes.
In fact, many authors (Buser et al.,47
premise. Recently, a study was per- odontal defects and in ridge augmenta- Simion et al.,55 Wachtel et al.,57 Jo-
formed around 15 immediately placed tion procedures before implant vanovic et al.,48,58 Becker et al.,59
implants into extraction sockets.44 Af- placement.45–55 One study on 26 subjects Simion et al.,60 Buser et al.,61 Jo-
ter implant placement, measurements with mandibular class II furcation de- vanovic and Nevins,62 and Nowzari
were made of the distance from the fects treated with ePTFE barriers con- and Slots63) stressed the importance of
coronal border of the buccal to the cluded that “similar improvement in all keeping the ePTFE barriers sub-
coronal border of the lingual plate of clinical and surgical parameters” oc- merged to obtain optimum results. The
bone. No membranes or filling mate- curred in both the prematurely exposed latter article (Nowzari and Slots63) re-
rials were used and primary closure and the fully submerged groups.46 A ported colonization of bacteria on the
was obtained in all cases. At the time technique for immediate implant inser- ePTFE membranes that became ex-
of second-stage surgery, 6 months tion was described that advocated place- posed. This too could have compro-
postimplantation, these measurement ment of an ePTFE barrier over the im- mised results of ePTFE-covered sock-
were repeated. The mean buccal to plant without primary flap coverage ets in the current study. However, the
lingual distance decreased from an ini- “because the membrane is, in effect, tak- strict recall program and the removal
tial 10.5 mm ⫾ 1.52 (after implant ing the place of the flap closure.”56 The of the 1 ABMA and 6 ePTFE barriers
placement) to 6.8 mm ⫾ 1.33 (6 membrane remained exposed and in when infection was evident could have
months postimplantation). Thus, the place for “approximately 1 month” be- allowed positive vital bone formation
average horizontal bone resorption af- fore removal. However, ePTFE mem- with the fill materials used in this
ter immediate implant placement was brane exposure in cases of ridge aug- study despite membrane exposure.
3.7 mm (range, 2–5 mm). This is mentation occurred in a number of However, the population in this study
slightly less that what was reported for studies requiring early removal of the was too small to detect significant dif-
the healed extraction sockets in the barriers and resulting in a compromised ferences in results of the membranes
control group (no membrane, no fill, result in many cases.47– 49 Buser, Jo- retained for longer periods of time as
primary closure) in a previous study.1 vanovic, and Mellonig reported mem- was reported in an experimental study
Membrane barriers have been suc- brane exposure requiring early removal in dogs.50
cessfully used in the treatment of peri- in 6.3% to 51% of cases treated.47– 49 It is interesting that in a published

158 EXTRACTION SOCKETS AND IMPLANTATION OF HYDROXYAPATITES

case report on 2 successful cases of during the study. This could reflect a control group. Using the same mea-
ridge preservation using ADMA in better resistance of the ADMA barri- surement technique in a previous
conjunction with decalcified freeze ers to bacterial colonization with the study, the “no filled” and “no mem-
bone allograft in a fresh extraction regimen of postsurgical treatment used brane” controls showed an average vi-
socket, the exposed ADMA mem- in this study. A factor that was not tal bone fill of 32.4% 6 to 8 months
branes exfoliated “atraumatically” 3 measured in this study was the dis- postsocket treatment.9 One must be
weeks postinsertion. In a published tance that the flaps were separated af- cautious with these comparisons be-
case report of ADMA used for ridge ter suturing or the amount of exposure cause the methodology was different
augmentation, the author noted the im- of the membranes during the healing (in the previous study, primary closure
portance of completely covering “the phase. There could be a “critical dis- was achieved) and the type of tooth
acellular dermal matrix with a pedicle tance” beyond which membrane expo- (incisor, premolar, molar) and jaw lo-
”and keeping it “completely covered sure adversely affects socket healing. cation represent factors that could in-
during the healing period.”64 Although However, these variables require more fluence healing and vital bone counts
no attempt was made to do this in this cases, additional measurement param-
because of differences in the type of
study, except for 1 barrier, which was eters, and further investigation.
bone native to that site.
removed 6 weeks postplacement, all 7 Although the combination of
When analyzing the data on all 16
of the other ADMA barriers showed ADMA and ABB appears to result in
surface sloughing 2 to 4 weeks post- the highest percentage of vital bone in sites in this study and comparing the
operatively and then were not evident this investigation, additional clinical results of multirooted (N ⫽ 8) with
at 8 weeks, or in some cases by 12 and histologic studies are necessary that of single-rooted teeth (N ⫽ 8), it
weeks, postsurgery. Because the 7 pa- before any speculation or conclusions is interesting to note that the average
tients with these ADMA barriers did are made. Certainly, the advantages of vital bone of the former was 34.16%
not report being aware of barrier loss, materials that result in significant bone (range, 10.6 – 62.4%), whereas that of
we must assume the barriers were in- fill of a healing extraction socket with- single-rooted teeth was 37.03%
corporated into the wound healing out the compromises caused by ob- (range, 12.9 – 67%). Although no sta-
(covered by epithelium) or exfoliated taining primary soft tissue closure tistically significant data can be drawn
without patient knowledge. This con- warrant further investigation. because of the limited sample size,
trasts to the 6 of 8 ePTFE barriers, It is also evident that this study these findings tend to demonstrate the
which had to be removed prematurely did not include a negative (no fill) variability of bone fill in human ex-
traction sockets. For example, one
might expect to have significantly
Table 2. Average Percent of Vital Bone in Sockets Covered With Acellular Dermal
Matrix Allograft (ADMA) or Expanded Polytetrafluoroethylene (ePTFE) Membranes and
more dense bone present after extrac-
Filled With Absorbable Hydroxyapatite (AH) or Anorganic Bovine Bone (ABB) tion socket healing in the anterior area
(single-rooted teeth) because the bone
Average Percent is usually denser in nature. However,
Barriers Vital Bone Grafts Vital Bone Percent (range)
the healed sockets in this study show
ADMA 38% AH 34.5 (19–57) similar percentages of vital bone in
ABB 41.7 (19.5–62.4) single- and multirooted healed sock-
ePTFE 22.7% AH 27.6 (14–40.1)
ets. This pilot study demonstrates the
ABB 17.8 (10–25)
need for a much larger sample size to
This table summarizes the average percent vital bone in sockets treated with ADMA compared with sockets treated with ePTFE
barriers. Average vital bone obtained from sockets filled with AH or ABB and covered with either ADMA or ePTFE barriers is also more accurately follow the trends in
recorded. healing responses. Confounding fac-
ADMA, acellular dermal matrix allograft; ePTFE, expanded polytetrafluoroethylene; AH, absorbable hydroxyapatite; ABB, anorganic tors, including socket location, use of
bovine bone mineral.
different graft materials, use of mem-
branes, type of flap closure (or non-
Table 3. Average Percent of Vital Bone in Healed Single vs. Multirooted Sockets
closure), and the presence and thick-
Anterior Single Rooted Posterior (multirooted) ness of the bony walls of the sockets,
Percent of prevent clear conclusions from being
Tooth No. Vital Bone Tooth No. Percent Vital Bone drawn from human socket studies.
Therefore, at this point, based on the
8 12.9 14 10.6
results of the present pilot study as
13 23 2 19
well as the referenced literature, the
4 24.3 3 19.5
4 25 3 36 operator must make clinical decisions
7 25 3 37 based on the individual situations pre-
9 57 19 40.1 sented. Clearly, further research with a
11 62 14 48.7 much larger sample size is indicated to
10 67 18 62.4 isolate the previously mentioned vari-
37.0% 34.2% ables to determine the best course of
This table presents the average percent of vital bone obtained in treated and healed sockets of either single and multirooted teeth. treatment after tooth extraction.

IMPLANT DENTISTRY / VOLUME 13, NUMBER 2 2004 159

CONCLUSIONS
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 cov-
ering 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 prema-
turely because of infection before the
6- to 8-month time period when im-
plants were placed.
This pilot study demonstrates the
need for a much larger sample size to
more accurately follow the trends in
healing responses.
ACKNOWLEDGMENTS
The authors acknowledge the con-
tributions of Hari Prasad, BS, MDT,
Research Scientist, University of Min-
nesota Dental School, for his assis-
tance with the histologic preparation
and histomorphometric analysis. This
study was supported by a grant from
LifeCell, the Woodlands, TX.
Disclosure
The authors claim to have no fi-
nancial interest in any company or any
of the products mentioned in this
article.
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Reprint requests and correspondence to:
Stuart J. Froum, DDS
17 West 54th Street
Suite 1 C/D
New York, NY 10019
Phone: (212) 586-4209
Fax: (212) 246-7599
E-mail: dr.froum@verizon.net
161
 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.###. * Kli-
nischer Professor und Direktor der klinischen For-
schung, Ashman Abteilung für implantatgestützte
Zahnheilkunde, Universität New York, Kriser Den-
talzentrum, New York, NY. ** Klinischer Assisten-
zprofessor und Mitglied des wissenschaftlichen
Forschungsteams, Ashman Abteilung für implan-
tatgestützte Zahnheilkunde, Universität New York,
Kriser Dentalzentrum, New York, NY. *** Leiter
des internationalen Forschungsprogramms, Assis-
tenzprofessor, Ashman Abteilung für implantat-
gestützte Zahnheilkunde, Universität New York,
Kriser Dentalzentrum, New York, NY. # Professor
für Orthodontie und implantatgestützte Zahnhei-
lkunde, Universität von Pennsylvania, Philadel-
phia, PA. ## Professor und Leiter, Bereich für
Oral- und Kieferpathologie, Universität von Min-
nesota, 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: dr.froum@verizon.net
162 EXTRACTION SOCKETS AND IMPLANTATION
Extraktionshöhlen und die Implantation von Hydroxylapatit mit Membranbarriere:
eine histologische Studie
ZUSAMMENFASSUNG: Einführung: Zielsetzung dieser Pilotstudie war es, die Aus-
wirkungen 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 Pati-
enten mit mangelhaften Bukkalplatten von 5 mm entstanden insgesamt 16 Zahnhöhlen.
Nach dem Zufallsprinzip erfolgte eine Aufteilung der Patienten in vier Behandlungsgrup-
pen. 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 histomorpholo-
gischen 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 an-
zustellen, um die innerhalb dieser Pilotstudie ermittelten Ergebnisse auf eine eventuell
ähnlich lautende Differenz bei Knochengewebe-zu-Implantat-Kontakt nach erfolgter Im-
plantatsetzung zu untersuchen.
SCHLÜSSELWÖRTER: Extraktionshöhle, Barrieremembran, histomorphologische Ana-
lyse, absorbierbares Hydroxylapatit, azelluläres, hautstrukturiertes Allotransplantat
OF HYDROXYAPATITES
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, Cen-
tro Dental Kriser, Nueva York, NY. **Profesor
Asistente Clínico e Investigador Científico, De-
partamento Ashman de Odontología de Implan-
tes, Universidad de Nueva York, Centro Dental
Kriser, Nueva York, NY. ***Director del Pro-
grama Internacional, Profesor Asistente, Depar-
tamento Ashman de Odontología de Implantes,
Universidad de Nueva York, Centro Dental
Kriser, Nueva York, NY. # Profesor, Periodón-
tica y Odontología de Implantes, Universidad de
Pennsylvania, Philadelphia, PA. ## Profesor y
Director, División de Patología Oral y Maxilo-
facial, 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. Corresponden-
cia 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: dr. froum@verizon.net
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 Ash-
man 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 Internacio-
nal, Professor Assistente, Departamento Ash-
man 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 Dire-
tor, Divisão de Patologia Oral e Maxilofacial,
Universidade de Minnesota, Escola de Odonto-
logia, Minneapolis, MN. ###Professor e Chefe,
Departamento Ashman de Odontologia de Im-
plantes, Universidade de Nova York, Centro Od-
ontológico Kriser, Nova York, NY. Corre-
spondência 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: dr.froum@verizon.net
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 especi-
menes 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 histomor-
fométrico, hidroxiapatita absorbible, aloinjerto de matriz dérmica acelular.
Cavidades de Extração e Implante de Hidroxiapatitas com Membranas Protetoras: um
Estudo Histológico
RESUMO: Introdução: O objetivo deste estudo-piloto 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. Re-
sultados: 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 estudo-piloto, 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. Justifica-se
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.
IMPLANT DENTISTRY / VOLUME 13, NUMBER 2 2004 163
164 EXTRACTION SOCKETS AND IMPLANTATION OF HYDROXYAPATITES