Stefan Fickl Hard tissue alterations after socket

Otto Zuhr
Hannes Wachtel
preservation: an experimental study
Wolfgang Bolz in the beagle dog
Markus B. Huerzeler

Authors’ affiliations:
Stefan Fickl, Otto Zuhr, Wolfang Bolz, Private
Institute for Periodontology and Implantology,
Munich, Germany
Hannes Wachtel, Department of Restorative
Dentistry, University School of Dental Medicine,
Charite-Berlin, Germany and Private Institute for
Periodontology and Implantology, Munich,
Germany
Markus B. Huerzeler, Department of Operative
Dentistry and Periodontology, Albert Ludwig
University of Freiburg, Freiburg, Germany and
Key words: experimental study, extraction socket, socket preservation
Abstract
Objectives: The aim of the following experimental study was to assess bone changes in the
horizontal and vertical dimension when using different socket preservation procedures.
Material and methods: In five beagle dogs the distal roots of the 3rd and 4th premolar
were extracted without elevation of a mucoperiosteal flap and the following treatments
were assigned:
s

Dental Branch, University of Texas, Houston, TX,

Tx 1: The extraction socket was filled with BioOss Collagen (Geistlich Biomaterials,
USA and Private Institute for Periodontology and Wolhusen, Switzerland) and interrupted sutures were applied.
Implantology, Munich, Germany s
Tx 2: The extraction socket was filled with BioOss Collagen (Geistlich Biomaterials,
Correspondence to: Wolhusen, Switzerland) and a free gingival graft was sutured to cover the socket.
Dr Stefan Fickl Tx 3: The extraction socket was left with its blood clot and interrupted sututes were
Institute for Periodontology and Implantology
Rosenkavalierplatz 18 applied.
Munich 81925 Four month after surgery the dogs were sacrificed and from each extraction site two
Germany
histological sections were selected for histometric analysis. The following parameters were
Tel.: þ 0049 89 9287840
Fax: þ 0049 89 915475 evaluated: (1) the vertical dimension was determined by placing a horizontal line on the
e-mail: fickl@ipi-muc.de lingual bone wall. Then, the distance from this line to the buccal bone wall was measured.
(2) The horizontal dimension was assessed at three different areas measured from the top
of the lingual crest: 1 mm (Value 1), 3 mm (Value 3) and 5 mm (Value 5).
Results: The mean vertical loss of the buccal bone plate for the Tx 1 group was
2.8
0.2 mm. The Tx 2 group showed vertical loss of 3.3
0.2 mm. The Tx 3 group
demonstrated 3.2
0.2 mm of mean vertical loss.
The horizontal dimension of the alveolar process was 4.4
0.3/6.1
0.2/7.2
0.1 mm at
the three different levels for the Tx 1 group. The Tx 2 group depicted bone dimensions of
4.8
0.2/6.0
0.2/7.1
0.1 mm. The horizontal dimension of the Tx 3 group was
3.7
0.3/6.2
0.2/7.0
0.1 mm. When the results from the horizontal measurements
were tested with the analysis of variance (ANOVA), a clear significance could be found in
particular for Value 1 mm between the test groups Tx 1 and Tx 2 and the control group
(Tx 3) (Po0.001). Furthermore the mean of treatment 1 (Tx 1) was slightly significantly
lower than of treatment 2 (Tx 2) (Po0.05).
Conclusion: The findings from the present study disclose that incorporation of BioOss
s
Date: Collagen into the extraction socket has only limited impact on the subsequent biologic
Accepted 12 December 2007
process with particular respect to the buccal bone plate. The horizontal measurement of the
To cite this article: alveolar ridge depicted that the loss of the buccal bone plate was replaced to a certain
Fickl S, Zuhr O, Wachtel H, Bolz W, Huerzeler MB. s

Hard tissue alterations after socket preservation: an
experimental study in the beagle dog.
Clin. Oral Impl. Res. 19, 2008; 1111–1118
doi: 10.1111/j.1600-0501.2008.01575.x
amount by newly generated bone guided by the BioOss Collagen scaffold. It seems that
s
the mechanical stability provided by BioOss Collagen and furthermore by a free gingival
graft could act as a placeholder preventing the soft tissue from collapsing.

c 2008 The Authors. Journal compilation 

 c 2008 Blackwell Munksgaard 1111
Fickl et al . Hard tissue alterations after socket preservation
The healing of an extraction socket in-
cludes a series of events consisting of for-
mation and maturation of a blood
coagulum (Huebsch et al. 1952; Amler
1969; Cardaropoli et al. 2003). Araújo &
Lindhe (2005) demonstrated in an experi-
mental study that while the blood coagu-
lum becomes replaced by a provisional
matrix and woven bone the socket walls
are resorbed and gradually remodelled. In
particular the buccal bone plate demon-
strated marked osteoclastic resorption.
The authors stated that the crest of the
buccal bone wall of the extraction socket
was comprised solely of bundle bone (Ara-
újo & Lindhe 2005). As the bundle bone is
part of the periodontium, it loses its func-
tion after tooth removal and is resorbed.
The resulting dimensional changes have
been evaluated by volumetric analysis in a
clinical study by (Schropp et al. 2003). The
loss of bone volume in the horizontal
dimension amounts 5–7 mm within the
first 10 months (Schropp et al. 2003).
This corresponds with approximately
50% of the original width of the alveolar
bone (Schropp et al. 2003). An apico-cor-
onal height reduction of 1 mm accompa-
nies the horizontal change (Schropp et al.
2003). Multiple adjacent extraction sites
demonstrate greater apico-coronal altera-
tions compared with single extraction sites
(Lam 1960; Johnson 1969).
It was suggested that the immediate
placement of implants may avoid the re-
sorption process of the buccal bone plate
and maintain the original shape of the ridge
(Paolantonio et al. 2001). Findings reported
from an experimental trial by Araújo et al.
(2005) failed to support this hypothesis.
The authors reported that when implants
were placed immediately after tooth extrac-
tion, in particular the buccal bone plate
underwent a major remodelling process
(Araújo et al. 2005). The authors concluded
that ‘the placement of an implant in the
fresh extraction site . . . failed to prevent
the re-modelling that occurred in the walls
of the socket’ (Araújo et al. 2005). As
implant installation does not alter the
occurring biologic procedures after tooth
extraction, it was suggested that the appli-
cation of biomaterials could be able to
interfere with the resorption process. A
s
deproteinized bovine bone (Bio-Oss , Geis-
tlich Pharma AG, Wolhusen, Switzerland)
mineral has been used to graft bone defects
1112 | Clin. Oral Impl. Res. 19, 2008 / 1111–1118
and extraction sockets both in experimen-
tal and clinical studies (Berglundh &
Lindhe 1997; Araújo et al. 2001; Carmag-
nola et al. 2002; Cardaropoli et al. 2005).
Authors from experimental studies report
positive findings and conclude that the
biomaterial can act as a scaffold for new
bone formation (Berglundh & Lindhe 1997;
Araújo et al. 2001; Carmagnola et al. 2002;
Cardaropoli et al. 2005). Conflicting data
s
exist on the outcome of placing BioOss
into human extraction sockets. Studies
conducted in humans concluded, that
when using a xenogenous bone substitute
for grafting extraction sockets, the augmen-
ted bone was mainly occupied by connec-
s
tive tissue and BioOss particles (Artzi &
Nemcovsky 1998; Becker et al. 1998; Artzi
et al. 2000; Carmagnola et al. 2002; Jung
et al. 2004). To date no experimental study
has histologically compared various socket
preservation techniques with respect to the
preservation of the buccal bone plate. The
aims of the present investigation were the
following:
1. Is it possible to preserve the buccal
bone plate by incorporation of bioma-
terials?
2. Is it beneficial concerning the resorption
process to incorporate biomaterials?
3. Is the additional use of a free gingival
graft advantageous with respect to the
resorption process?
Material and methods
The study protocol was approved by the
ethical committee of Biomatech (BIOMA-
TECH NAMSA, Lyon, France). Five beagle
dogs (1-year old and weighting 17–19 kg)
were used for this experiment. Supragingival
scaling was performed on all dogs 5 days
prior to tooth extraction. Anaesthesia was
s
induced by injecting atropine (Atropine ,
Aguettant, France; 0.05 mg/kg intramuscu-
s s
lar) and tiletamine-zolazepam (Zoletil 100,
Virbac, France; 5–10 mg/kg intramuscular).
Subsequently an injection of thiopental so-
dium was given (NesdonalND, Merial, Lyon,
France; 10–15 mg/kg/intravenous) and the
animals were placed on an O2–N2O isoflur-
ane (1–4%) mixture. In both quadrants of the
mandible the third and fourth premolars (3P3
and 4P4) were used as experimental sites.
The third and fourth mandibular premo-
lars were hemisected with the use of a
c 2008 The Authors. Journal compilation 
 c 2008 Blackwell Munksgaard
fissure bur. The distal roots were carefully
extracted using a forceps without elevating
a muco-periosteal flap or compromising
the marginal gingiva. The pulp tissues of
the mesial roots were extirpated and en-
gaged with a Gates–Glidden bur. After
obturating the root canals with gutta-
percha, the coronal part of the pulp cham-
ber was sealed with an auto-polymerizing
s
resin material (Clearfil Core , Kuraray,
Tokyo, Japan). The extraction sites were
randomly assigned to one of the following
treatments:
Tx 1: The extraction socket was filled
s
with BioOss Collagen (Geistlich Bioma-
terials, Wolhusen, Switzerland) and se-
cured with a non-resorbable suture
s
material (Gore-Tex CV5, W.L. Gore &
Associates, Putzbrunn, Germany) (Fig. 1).
Tx 2: The extraction socket was filled
s
with BioOss Collagen (Geistlich Bioma-
terials) and a free gingival graft was utilized
to superficially cover the extraction socket
according to the technique of Jung et al.
(2004) and Landsberg & Bichacho (1994).
The free gingival graft with a thickness of
3–4 mm was harvested from the palate.
Several interrupted sutures (Seralene 7–
s
0 , Serag Wiesner, Naila, Germany) were
applied to fix the transplant to the marginal
gingiva of the extraction socket (Fig. 2).
Tx 3: The extraction socket was left with
its blood clot and secured with a non-
s
resorbable suture material (Gore-Tex )
(Fig. 3).
Tx 4: The internal buccal aspect of the
extraction socket was covered with an
experimental porcine cross-linked collagen
membrane, afterwards, the extraction
s
socket was filled with BioOss Collagen
(Geistlich Biomaterials) and then the
membrane was folded on top of the graft.
Consecutively, a prefabricated resin bonded
bridge with a subgingival pontic design was
bonded to the adjacent teeth with an auto-
polymerizing resin material (Clearfil
Core ). The Tx 4 group showed major
infections with membrane exposure and
marked tissue recession in the postopera-
tive phase. Consequently no qualitative or
quantitative evaluation of this group could
be assessed.
After surgery the following regimen was
administered:
- Antimicrobial prophylaxis: spiramycine
750,000 IU and metronidazole 125 mg
 Fickl et al . Hard tissue alterations after socket preservation

tration of 0.2% chlorhexidine was perfor-

med three times per week for 4 weeks.

The sutures were removed 2 weeks post-

surgery.
The animals were terminated 4 months
after tooth extraction. After anaesthesia
s
with an intramuscular injection of Zoletil
(50 mg/kg), heparin was administered by
intravenous injection (100 IU/kg). The an-
imals were euthanized by a lethal dose
s
injection of Dolethal (Pentobarbital sodi-
que, Vetoquinol, Paris, France) before for-
malin injection. Tissue fixation was
s
Fig. 1. Treatment group 1: The extraction socket is filled with BioOss Collagen and interrupted sutures were achieved by injecting approximately
applied. 300 ml of 10% formalin in the common
carotid artery. Following this initial fixa-
tion each mandible was dissected behind
the first molar and resected. Each ramus
was separated by a frontal section and fixed
in 10% buffered formalin solution. The
experimental units, together with the me-
sial roots, were dissected using a diamond
saw (Exakt Apparatebau, Norderstedt,
Germany). The biopsies were processed
for ground sectioning according to the
methods described by Donath & Breuner
(1982) and Donath (1993). The samples
were dehydrated in increasing grades of
s
ethanol and infiltrated with Technovit
720 VLC-resin (Kulzer, Friedrichsdorf,
s
Fig. 2. Treatment group 2: After incorporation of BioOss Collagen into the extraction socket, a free gingival Germany). Serial sections were cut in the
graft was sutured into the orifice of the extraction socket. bucco-lingual plane and parallel to the axis
of the mesial root representing the central
part of the extraction socket (Exakt Appa-
ratebau). By micro grinding and polishing,
the sections were reduced to 20 mm and
stained with toluidine blue.

Histometric measurements
The histologic examination was performed
with a stereomicroscope (Leica Stereomik-
roskop MZ 16, Leica, Wetzlar, Germany)
and a digital image software (ImageAccess,
Imagic, Glatbrugg, Switzerland).

Vertical measurements
The vertical distance between the coronal
Fig. 3. Treatment group 3: After tooth extraction, the socket is left with its blood clot and two superficial
margins of the buccal and lingual bone
interrupted sutures.
walls was determined in the following
way (Fig. 4): a horizontal line (HL) was
s
per day per os for 7 days (Stomorgyl , - Each animal received an injection of placed on top of the lingual crest (LBC)
s
Merial, Lyon, France). butorphanol (0.3 mg/kg) (TorbuGesic , perpendicular to the long axis of the tooth
- Anti-inflammatory drug: carprofene Fort Dodge Animal Health, Southamp- (VL). Subsequently a perpendicular vertical
50 mg per os and per day for 6 days ton, UK) post-surgically and on the line was drawn reaching to the top of the
s
(Rimadyl , Pfizer Santé Animale, Orsay, following day. Tooth cleaning with former buccal bone crest (BBC). The verti-
France) toothbrush and dentifrice and adminis- cal distance between the horizontal line

c 2008 The Authors. Journal compilation 

 c 2008 Blackwell Munksgaard 1113 | Clin. Oral Impl. Res. 19, 2008 / 1111–1118
Fickl et al . Hard tissue alterations after socket preservation
and the buccal bone crest was measured
and expressed in millimetres. Mean values
and standard deviations were calculated for
each experimental unit.
Horizontal measurement
The bucco-lingual width of the ridge was
measured according to (Araújo & Lindhe
2005) (Fig. 5): Parallel lines to the horizontal
plane (LBC) were placed at 1 mm (Value 1),
Fig. 4. Vertical Measurements: HL, horizontal line; VL, vertical line (tooth axis); BBC, buccal bone crest; LBC,
lingual bone crest.
Fig. 5. Horizontal Measurements: HL, horizontal line; BBC, buccal bone crest; LBC, lingual bone crest;
Value1, bucco-lingual measurement 1 mm below the LBC; Value2, bucco-lingual measurement 3 mm below
the LBC; Value 3, bucco-lingual measurement 5 mm below the LBC.
1114 | Clin. Oral Impl. Res. 19, 2008 / 1111–1118
3 mm (Value 3) and 5 mm (Value 5) below
the lingual crest, representing three different
levels of the alveolar ridge. The horizon-
tal distance between the borders of the
alveolar ridge were measured and expressed
in millimetres. Mean values and standard
deviations were calculated for each experi-
mental unit.
For the horizontal and vertical measure-
ments the analysis of variance (ANOVA)
c 2008 The Authors. Journal compilation 
 c 2008 Blackwell Munksgaard
with the two factors ‘dog’ and ‘treatment
group’ were applied. Because the interac-
tions between the factors treatment and
dog were low and the mean differences
between dogs are not significant the factor
‘dog’ was deleted.
Results
Clinical observations
Healing of all experimental sites besides the
mentioned infections in Tx 4 presented
uneventful. The experimental as well as
the control groups depicted no sign of in-
flammation. The free gingival grafts were
fully integrated without any sign of necrosis.
Histological observations
After 4 months of healing the treatment
groups 1 and 2 histologically differed from
the control group. The control group was
characterized by the presence of a hard
tissue bridge that sealed the coronal part
of the extraction socket. The hard tissue
bridge was continuous with the buccal and
lingual bone plate. This marginal bridge
was mainly made of woven bone with areas
of lamellar bone. Apical of the bridge the
socket was comprised of cancellous bone
dominated by its bone marrow. The mar-
ginal portion of the original buccal bone
plate was located apical to its lingual coun-
terpart. Compared with the lingual region
the buccal soft tissue component exhibited
a concave appearance with an invagination
towards the extraction socket (Fig. 6). In
both experimental treatment groups the
biomaterial occupied a substantial portion
of the tissue volume. A hard tissue bridge
sealing the former extraction socket could
s
be detected with BioOss Collagen parti-
cles being incorporated. Most of the BioOss
s
Collagen particles in the coronal and api-
cal portion were in direct contact with
woven and lamellar bone (Fig. 7). A small
part of the biomaterial was surrounded by
connective tissue in particular at the most
coronal part of the former extraction socket.
Qualitatively, both treatment groups 1 and
2 depicted less invagination of the buccal
soft and hard tissue (Figs 8 and 9).
Histometric observations
Vertical measurements (Table 1, Fig. 10)
The mean distance between the buccal
bone plate and the lingual bone plate was

Fig. 6. Bucco-oral section of Tx 3. Note the marginal hard tissue bridge and the large amount of bone marrow.
Fig. 7. Histological view of the apical part of the extraction socket. Note that most of the biomaterial particles
are surrounded by woven bone.
2.8
0.2 mm for Tx 1. The treatment
group 2 (Tx 2) depicted a distance between
buccal and lingual bone plate of
3.3
0.2 mm. Tx 3 showed a correspond-
ing mean value of 3.2
0.2 mm. When
tested with an ANOVA the means with Tx 1
were clearly significantly lower than with
Tx 2 and Tx 3 (Po0.001). The treatment
means of Tx 2 and Tx 3 were not signifi-
cantly different (P40.1).
Horizontal measurements (Table 2, Fig. 11)
The horizontal dimension at the three
different levels of the alveolar process was
c 2008 The Authors. Journal compilation 
 c 2008 Blackwell Munksgaard
Fickl et al . Hard tissue alterations after socket preservation
4.4
0.3/6.1
0.2/7.2
0.1 mm for
the Tx 1 group. The Tx 2 group demon-
strated corresponding bone dimensions of
4.8
0.2/6.0
0.2/7.1
0.1 mm. The
horizontal dimension of the Tx 3 Group
was 3.7
0.3/6.2
0.2/7.0
0.1 mm.
When tested with an ANOVA the following
results could be obtained:
Value 1 mm: The means of treatment 3
(Tx 3) were clearly significantly lower than
the mean of treatment 1 (Tx 2) and 2 (Tx 3)
(Po0.001). The means of treatment 1 (Tx 1)
were slightly significantly lower than of
treatment 2 (Tx 2) (Po0.05).
1115 |
Value 3 mm: No significant mean differ-
ences could be shown between treatments
1 (Tx 1) to 3 (Tx 3) (P40.05).
Value 5 mm: The means of treatment 3
(Tx 3) were slightly significantly lower than
of treatment 1 (Tx 1) and 2 (Tx 2) (Po0.05)
(Fig. 12).
Discussion
The findings from the present study dis-
close, that incorporation of BioOss Col-
s
lagen into the extraction socket has only
limited influence on the subsequent biolo-
gic process with particular respect to the
buccal bone plate. The treatment groups
displayed major bone alteration predomi-
nantly at the buccal aspect. Araújo &
Lindhe (2005) demonstrated in an experi-
mental study that 1 week after tooth
extraction the crest of the buccal bone plate
is situated coronally to the lingual bone
plate. Using these data as a baseline refer-
ence for the present investigation, a
marked resorptive process occurred during
4 months of healing in particular at the
buccal bone plate. Assuming the buccal
and the lingual bone plate is at least at
the same height at baseline, a beneficial
effect of the various treatment sequences
must be questioned. The manifest resorp-
tion at the buccal aspect amounting 2.8–
3.3 mm after four months of healing is in
agreement with the findings from the
above cited experimental study of (Araújo
& Lindhe 2005). The authors demon-
strated that eight weeks after tooth extrac-
tion the buccal bone crest was located
1.9 mm apical of its lingual counterpart.
In the present investigation no mucoper-
iosteal flap was raised for tooth extraction.
By elevating the periosteum, the blood
supply of the exposed bone surface will be
compromised, leading to osteoclastic activ-
ity and bone resorption (Wilderman 1963;
Wood et al. 1972; Bragger et al. 1988).
Araújo & Lindhe (2005) demonstrated 1
and 2 weeks after tooth extraction using
minute mucoperiosteal flaps, that osteo-
clasts were present at the exposed alveolar
ridge showing signs of surface resorption.
The pronounced alterations occurring after
tooth extraction found in the present
investigation even without detaching
the periosteum convey that destroying the
Clin. Oral Impl. Res. 19, 2008 / 1111–1118
Fickl et al . Hard tissue alterations after socket preservation
Fig. 8. Histological view of the coronal part of the extraction socket. A major part of the biomaterial is
incorporated in connective tissue.
Fig. 9. Bucco-lingual section of Tx 2. Note that most of the BioOss collagen particles are in direct contact with
woven bone.
biologic unit of the periodontium (bundle
bone, Sharpey-fibres and root cementum)
is a determining factor for inducing the
resorption process of the extraction socket.
In particular the bundle bone – the area of
the marginal bone into which the perio-
dontal ligament fibres invest – will lose its
function and gradually disappear. Cardaro-
poli et al. (2003) showed, that already 2
weeks after tooth extraction most of the
bundle bone at the mesial and distal aspect
of the root has been replaced by woven
1116 | Clin. Oral Impl. Res. 19, 2008 / 1111–1118
bone. The crestal region of the buccal bone
plate is often exclusively made of bundle
bone, while the lingual bone plate consists
of a combination of bundle bone and
lamellar bone (Araújo & Lindhe 2005).
This may explain the marked reduction of
height in particular at the buccal aspect in
previous studies and in this present inves-
tigation. As no mucoperiosteal flap was
raised, no primary closure could be
obtained in treatment groups 1 and 3. It
cannot be ruled out, that a certain amount
c 2008 The Authors. Journal compilation 
 c 2008 Blackwell Munksgaard
Table 1. Mean vertical distance between
buccal and lingual bone crest
Tx Vertical
1 2.8 (0.2)
2 3.3 (0.2)
3 3.2 (0.2)
of the bone resorption may be due to
that fact.
The vertical loss of the buccal bone plate
seems to have a major consequence for the
horizontal soft tissue stability. It can be
assumed, that when the buccal bone plate
is resorbed, the soft tissue complex can no
longer be stabilized and will collapse into
the newly formed space. As the buccal soft
tissue occupies the place of the former
buccal bone plate, the room for bone
regeneration is reduced, leading to the
observed major bucco-lingual shrinkage. It
seems that the osteconductive effect of the
bone substitute is not able to preserve the
buccal bone plate.
The horizontal measurement of the
alveolar ridge after tooth extraction and
socket preservation techniques demon-
strated, that the test groups displayed a
greater width of the alveolar process than
the control group. It must be stated that
due to the limited amount of sites the
statistical results should be evaluated
with caution and only used as a trend.
But with particular respect to the coronal
part of the alveolar ridge (Value 1 mm), the
treatment group 1 (Tx1) depicted a statis-
tically significant greater dimension of the
alveolar ridge four months after tooth ex-
traction. In the histologic evaluation the
s
BioOss Collagen particles were well inte-
grated and continuous with the newly
formed network of woven and lamellar
bone. This is in agreement with Cardaro-
poli et al. (2005). They grafted surgically
s
produced defects with BioOss Collagen
and showed that the major part of the
s
BioOss Collagen particles were found to
be in direct contact with newly formed
mineralized bone. In the present study
the control group depicted a cortical bone
bridge at the coronal aspect of the former
extraction socket and in the central part
mainly bone marrow. This is also in agree-
ment with Cardaropoli et al. (2003), who
showed that after 180 days of healing a
large volume below the cortical bone bridge

Fig. 10. Bucco-lingual section of Tx 1.
Fig. 11. Histogram describing the mean vertical distance between LBC and BBC.
was occupied by bone marrow. It can be
assumed the healed ridge is a non-load
carrying tissue with obviously no demand
for mineralized tissue. The xenogenous
bone substitute seems to replace the buccal
bone plate to a certain extent and minimize
the collapse of the soft tissue. It seems that
during the healing process of the buccal
bone plate the bone substitute is able to
stabilize the buccal soft tissue from invagi-
nation and may act as a scaffold for bone
regeneration. Concerning the use of depro-
teinized bovine bone material the present
data are in agreement with the experimen-
c 2008 The Authors. Journal compilation 
 c 2008 Blackwell Munksgaard
Fickl et al . Hard tissue alterations after socket preservation
tal studies of Berglundh & Lindhe (1997)
and Araújo et al. (2001), who concluded
that the biomaterial acted as a scaffold for
new bone formation. However data from
clinical trials fail to demonstrate a consis-
tent beneficial effect compared with spon-
taneous socket healing with respect to bone
regeneration. Most of the studies con-
cluded, that when using a xenogenous
bone substitute for grafting human extrac-
tion sockets, the augmented bone was
mainly occupied by connective tissue and
s
BioOss particles (Artzi & Nemcovsky
1998; Becker et al. 1998; Artzi et al.
1117 |
Table 2. Mean horizontal width at the dif-
ferent levels below the lingual bone crest
Tx Horizontal
Value Value Value
1 mm 3 mm 5 mm
1 4.4 (0.3) 6.1 (0.2) 7.2 (0.1)
2 4.8 (0.2) 6.0 (0.2) 7.1 (0.1)
3 3.7 (0.3) 6.2 (0.2) 7.0 (0.1)
2000; Carmagnola et al. 2002; Jung et al.
2004). Carmagnola et al. (2002) grafted
s
human extraction sockets with BioOss
and stated that seven months after augmen-
tation the sockets comprised mainly of
connective tissue and small amounts of
newly formed bone surrounding the graft
particles. It must be assumed that augment-
ing the human extraction socket with the
ultimate goal of bone regeneration is hardly
predictable and difficult to assess in an
animal model.
However, the findings from the present
study show that it might be reasonable to
use deproteinized bovine bone material to
stabilize the buccal soft tissue and prevent
it from collapsing into the socket. Further-
more due to the importance of the soft
tissue collapse, the adjuvant support of the
marginal gingiva with a free gingival graft
according to Landsberg & Bichacho (1994)
and Jung et al. (2004) seems to be bene-
ficial. The present investigation shows that
the additional use a free gingival graft to
stabilize and to seal the extraction socket
might be beneficial. It must be concluded
that stabilizing the extraction socket with a
s
combination of BioOss Collagen and a free
gingival graft has the potential to limit the
volume shrinkage occurring after tooth ex-
traction. Yet the biologic process after tooth
extraction cannot be altered.
The present investigation shows that the
used animal model is suitable to investi-
gate the biologic process occurring after
socket preservation techniques. The statis-
tical power is weak due to the limited
amount of sites. Therefore the results of
this present investigation should be used as
a trend for further investigations: it seems
that incorporation of biomaterials does not
preserve the buccal bone plate. Yet it may
be possible to limit the bucco-lingual
resorption process after tooth extraction to
a certain amount and the adjunctive use of
a soft tissue punch could be helpful to
stabilize the buccal soft tissue and prevent
Clin. Oral Impl. Res. 19, 2008 / 1111–1118
Fickl et al . Hard tissue alterations after socket preservation
Fig. 12. Histogram describing the mean horizontal width at Values 1, 2 and 3 for the different treatment
groups.
References
Amler, M.H. (1969) The time sequence of tissue rege-
neration in human extraction wounds. Oral Surgery,
Oral Medicine and Oral Pathology 27: 309–318.
Araújo, M., Sukekava, F., Wennstrom, J. & Lindhe,
J. (2005) Ridge alterations following implant pla-
cement in fresh extraction sockets: an experimen-
tal study in the dog. Journal of Clinical
Periodontology 32: 645–652.
Araújo, M.G., Carmagnola, D., Berglundh, T.,
Thilander, B. & Lindhe, J. (2001) Orthodontic
movement in bone defects augmented with
bio-oss. An experimental study in dogs. Journal
of Clinical Periodontology 28: 73–80.
Araújo, M.G. & Lindhe, J. (2005) Dimensional
ridge alterations following tooth extraction. An
experimental study in the dog. Journal of Clinical
Periodontology 32: 212–218.
Artzi, Z. & Nemcovsky, C.E. (1998) The applica-
tion of deproteinized bovine bone mineral for ridge
preservation prior to implantation. Clinical and
histologic observations in a case report. Journal of
Periodontology 69: 1062–1067.
Artzi, Z., Tal, H. & Dayan, D. (2000) Porous bovine
bone mineral in healing of human extraction
sockets. Part 1: histomorphometric evaluations
at 9 months. Journal of Periodontology 71: 1015–
1023.
Becker, W., Clokic, C., Sennerby, L., Urist, M.R. &
Becker, B.E. (1998) Histologic findings after im-
plantation and evaluation of different grafting
materials and titanium micro screws into extrac-
tion sockets: case reports. Journal of Perio-
dontology 69: 414–421.
Berglundh, T. & Lindhe, J. (1997) Healing around
implants placed in bone defects treated with bio-
oss. An experimental study in the dog. Clinical
Oral Implants Research 8: 117–124.
1118 | Clin. Oral Impl. Res. 19, 2008 / 1111–1118
Bragger, U., Pasqualli, L. & Kornman, K.S. (1988)
Remodelling of interdental alveolar bone after
periodontal flap procedure assessed by means of
computer-assisted densitometer image analysis
(cadia). Journal of Clinical Periodontology 15:
558–564.
Cardaropoli, G., Araújo, M., Hayacibara, R., Suke-
kava, F. & Lindhe, J. (2005) Healing of extraction
sockets and surgically produced - augmented and
non-augmented - defects in the alveolar ridge. An
experimental study in the dog. Journal of Clinical
Periodontology 32: 435–440.
Cardaropoli, G., Araújo, M. & Lindhe, J. (2003)
Dynamics of bone tissue formation in tooth
extraction sites. An experimental study in
dogs. Journal of Clinical Periodontology 30:
809–818.
Carmagnola, D., Adriaens, P. & Berglundh, T.
(2002) Healing of human extraction sockets filled
with bio-oss. Clinical Oral Implants Research
14: 137–143.
Donath, K. (1993) Preparation of Histological Sec-
tions (by the Cutting–Grinding Technique for
Hard Tissue and other Material Not Suitable for
Sectioned by Routine Methods) – Equipment and
Methodological Performance. Norderstedt: EX-
AKT - Kulzer Publication.
Donath, K. & Breuner, G. (1982) A method for the
study of undecalcified bones and teeth with at-
tached soft tissues. The sage-schliff (sawing and
grinding) technique. Journal of Oral Pathology
11: 318–326.
Huebsch, R.F., Coleman, R.D., Frandsen, A.M. &
Becks, H. (1952) The healing process following
molar extraction. I. Normal male rats (long-evans
strain). Oral Surgery Oral Medicine Oral Pathol-
ogy 5: 864–876.
c 2008 The Authors. Journal compilation 
 c 2008 Blackwell Munksgaard
the tissue from collapsing to a certain
amount.
The resorption process after tooth extrac-
tion has a major consequence on implant
dentistry in particular in the esthetic zone,
as in this area no tissue loss can be ac-
cepted. The present investigation shows
that augmenting the extraction socket
with biomaterials has no effect on the
resorption process, but may have the pos-
sibility to limit the bucco-lingual shrink-
age. For esthetic reasons the bucco-lingual
shrinkage should be completely avoided. In
this context the presented socket preserva-
tion techniques do not seem to be suffi-
cient to reach that particular goal. Further
investigations with the ultimate goal of
avoiding or compensating the resorption
process after tooth extraction should be
conducted.
Johnson, K.A. (1969) A study of the dimensional
change occurring in the maxilla following
tooth extraction. Australian Dental Journal 14:
241–244.
Jung, R.E., Siegenthaler, D.W. & Hammerle, C.H.
(2004) Postextraction tissue management: a soft
tissue punch technique. International Journal of
Periodontics and Restorative Dentistry 24: 545–
553.
Lam, R. (1960) Contour changes of the alveolar
process following extraction. Journal of Prosthetic
Dentistry 10: 25–32.
Landsberg, C.J. & Bichacho, N. (1994) A modified
surgical/prosthetic approach for optimal single
implant supported crowns - the socket seal sur-
gery. Practical Periodontics and Aesthetic Den-
tistry 6: 11–17.
Paolantonio, M., Dolci, M. & Scarano, A. (2001)
Immediate implant placement in fresh extraction
sockets. A controlled clinical and histological
study in man. Journal of Periodontology 7211:
1560–1571.
Schropp, L., Wenzel, A., Kostopoulos, L. & Karring,
T. (2003) Bone healing and soft tissue contour
changes following single-tooth extraction: a clin-
ical and radiographic 12-month prospective
study. International Journal of Perio-
dontics and Restorative Dentistry 23:
313–323.
Wilderman, M.N. (1963) Repair after a periosteal
retention procedure. Journal of Periodontology
34: 487–498.
Wood, D.L., Hoag, P.M., Donnenfeld, O.W. &
Rosenberg, D.L. (1972) Alveolar crest re-
duction following full and partial thickness
flaps. Journal of Periodontology 43:
141–144.