A.

Barone
M. Ricci
J. L. Calvo-Guirado
U. Covani

Bone remodelling after regenerative

procedures around implants placed in
fresh extraction sockets: an experimental
study in Beagle dogs

Authors affiliations:
A. Barone, U. Covani, Istituto Stomatologico Tirreno,
Versilia Hospital, Lido di Camaiore (LU), Italy
A. Barone, Department Oral Pathology, University of
Genova, Genova, Italy
M. Ricci, Nanoworld Institute, University of Genova,
Genova, Italy
J. L. Calvo-Guirado, Department of Implantology,
University of Murcia, Murcia, Spain
U. Covani, Department of Surgery, University of Pisa,
Pisa, Italy

Key words: bone remodelling, guided bone regeneration

Corresponding author:
Massimiliano Ricci
Istituto Stomatologico Tirreno
Ospedale della Versilia
Via Aurelia 335
Lido di Camaiore (Lucca)
Italy
Tel./Fax: 39 0584 6059 888
e-mail: ricci.massimiliano@yahoo.it

selected. The experimental teeth (fourth pre-molar and first molar) were hemi-sected removing the

Abstract
Introduction: After a tooth extraction, the height of the buccal wall tends to decrease. The literature
indicates that regenerative techniques (guided bone regenerative [GBR] techniques) have succeeded
in improving the bone levels. Therefore, this experiment set out to compare the physiological bone
remodelling in Beagle dog models after implant placement in a fresh extraction socket, with and
without the application of regenerative procedure.
Materials and methods: Five dogs were used in this study. Test and control sites were randomly
distal roots and placing implants. Porcine bone was placed to fill the gap around the implant on the
test sites and a reabsorbable membrane was used to cover the area. The dogs were put down at
different times (2 weeks, 1 month and 3 months). The measurements were taken immediately and at 2,
4, 12 weeks after implant placement. Students test for paired data was used to compare the means of
the clinical measurements.
Results: At 2 weeks: On the control sites, few signs of resorption were detected at the first molar only,
while at the test sites bone levels were placed at the implant shoulder or above.
At 4 weeks: On the control site, slight bone remodelling was observed, while on the test site minor
signs of resorption or an increase of bone levels were detected.
At 12 weeks: The alveolar crest on the control sites showed various degrees of remodelling. On the
test sites stable bone levels or an increase of bone crest was observed.
Conclusion: With the limits of this study, the findings showed that GBR techniques were able to limit
resorption of the alveolar crest after tooth extraction. A pattern of bone remodelling after tooth
extraction and implant placement was observed in the control sites (no GBR) as well as in test sites
(GBR), and although the exact cause of this is unclear, surgical trauma could play a role. Further studies
are necessary to confirm these results and to clarify the precise causes of bone remodelling in fresh
extraction sockets.

Date:
Accepted 15 September 2010
To cite this article:
Barone A, Ricci M, Calvo-Guirado JL, Covani U. Bone
remodelling after regenerative procedures around implants
placed in fresh extraction sockets: an experimental study in
the Beagle dogs.
Clin. Oral Impl. Res. 22, 2011; 11311137.
doi: 10.1111/j.1600-0501.2010.02084.x


c 2011 John Wiley & Sons A/S

A large number of studies have clearly shown

that tooth extraction brings about changes to
residual alveolar bone (Johnson 1969; Cardaropoli et al. 2003; Schropp et al. 2003; Araujo &
Lindhe 2005). As a consequence of extraction,
the height of the buccal wall tends to decrease
and bundle bone disappears (Cardaropoli et al.
2003; Schropp et al. 2003; Araujo & Lindhe
2005; Araujo et al. 2008). Although these
changes were noted as anecdotal information,
Johnson and colleagues had first demonstrated
40 years ago that a reduction from 2.5 to 7 mm in
height and up to 30 mm in width could follow a
tooth extraction. Moreover, they observed that
most changes occurred during the first month,
while a minor additional decrease in the ridge

continued over periods ranging between 10 and

20 weeks (Johnson 1969). Pietrokovski & Massler (1967) came to a similar conclusion, although
they underlined that a greater amount of tissue
attenuation occurs in the buccal wall of the molar
area rather than the frontal zone (Pietrokovski &
Massler 1967). More recently, Schropp et al.
(2003) have described that a reduction in residual
alveolar ridge up to 50% in width may occur
during the first 3 months of healing (Schropp
et al. 2003). It is worth underlining that multiple
adjacent extractions induce greater apico coronal
alterations compared with single extractions
(Lam 1960; Johnson 1969).
The exact causes of these phenomena are still
under discussion. On the one hand, Araujo &

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Barone et al  Bone remodelling after regenerative procedures around implants placed in fresh extraction sockets

Lindhe (2005) stated that, because the buccal

bone of the socket is made up of bundle bone,
and bundle bone is part of the periodontium, the
removal of a tooth renders this bone useless, and
its resorption is a natural consequence. Conversely, other authors have emphasized that surgical
trauma during extraction may imply the separation of the periostium and its disconnection from
the underlying bone surface. This might be the
cause of vascular damage and an acute inflammatory response, which in turn, will mediate the
resorption of the bone tissue (Wilderman 1963;
Staffileno et al. 1966; Wood 1972; Bragger et al.
1988).
However, in order to modify bone remodelling
after extraction various techniques have been
proposed.
First of all, Paolantonio (2001) suggested that
the placement of an implant in a fresh socket
could prevent bone remodelling. Other authors
have put the hypothesis to rest demonstrating
that implant placement does not interfere with
alveolar crest remodelling. Indeed, the reduction
in buccolingual width occurred normally after 4
6 months independent of the implant insertion
(Covani et al. 2004). Nevertheless, Araujo and
colleagues carried out a study to evaluate the
relationships between immediate implant placement and bone remodelling. They revealed that
the placement of implants in fresh extraction
sockets gave rise to marked alterations of the
buccal and lingual walls, both in terms of height
and width (Araujo & Lindhe 2005). Although the
exact cause of the buccal bone loss around immediate implants is still not clear, many studies
have evaluated the role of factors such as the
sockets location, the thickness of the buccal
bone crest, the marginal gap between implant
and alveolar wall, or the implant surface nanotopography (Araujo et al. 2006; Vignoletti et al.
2009).
In order to prevent bone resorption after tooth
extraction, different regenerative techniques have
been used. It was recently observed in experimental studies that grafting extraction sockets
with bovine de-proteinzed bone might preserve
the ridge dimensions (Araujo et al. 2008; Fickl et
al. 2008). However, although another study demonstrated that socket preservation with bovine
bone outperfomed the control group, and loss of
the buccal bone plate was reported in most of the
cases (Nevins et al. 2006). Thus, nowadays
complete preservation of the alveolar socket
seems to be an unpredictable treatment goal.
On the other hand, a large number of studies
underlined that guided bone regenerative (GBR)
techniques have succeeded in improving the bone
levels in humans, when different types of biomaterials are placed under membranes (Simion et al.
1994; Piattelli et al. 1996; Tinti et al. 1996,

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Clin. Oral Impl. Res. 22, 2011 / 11311137

1997; Tinti & Parma-Benfenati 1998; ParmaBenfenati & Tinti 1998; Simion et al. 1998;
Canullo et al. 2006; Simion et al. 2007). In
fact, some authors demonstrated that the marginal bone level changes were higher in those
patients treated with GBR procedures (mean:
2.2 mm), using both non-reabsorbable and reabsorbable membranes, compared with the control
implants (mean 1.7 mm) after a 2-year follow-up
(Zitzmann et al. 2001).
The present study was designed with these
considerations in mind: to compare the physiological bone remodelling in dog models after the
implant placement in a fresh extraction socket,
with or without the application of regenerative
procedures.

Material and methods

The ethical committee of the University of
Murcia, Spain, approved the research protocol.
Five Beagle dogs, about 1-year old and weighing
approximately 1013 kg, were used in this study.
During surgical procedures, the animals were
anaesthetized with intravenously administered
s
Pentothal Natrium (30 mg/ml; Abbot Laboratories, Chicago, IL, USA). Throughout the experiment, the animals were fed a pellet diet and
subjected to regular mechanical tooth and implant cleaning.
The fourth pre-molar and first molar (4P4, 1M1)
were selected as experimental teeth. A test and a
control site for each dog were randomly selected.
Specific software was used to obtain a randomization list (Random Allocation Software version
1.0, downloadable on http:// mahmoodsaghaei.
tripod.com/Softwares/randalloc.html). Then, five
sealed envelopes describing test and control sites
for each dog were prepared by the same investigator. At the time of surgery, each envelope
indicated to a blinded surgeon the test and the
control side according to the randomization list.

Muco-periosteal full-thickness flaps were elevated to disclose the buccal and lingual hard bone
wall of the ridge. The experimental teeth were
hemi-sected with the use of a fissure bur and the
distal roots were carefully removed using forceps.
The pulp tissue of the mesial roots of all experimental teeth was removed and the canals were
filled with an endodontic cement after placement
of a rubber dam (Fig. 2). The coronal portion of
the pulp chamber was filled with a composite
material. The buccallingual dimension of the
entrance of the experimental sites was measured
using a calliper. The control sites were prepared
for implant installation according to the guidelines provided by the manufacturer. Extreme care
was taken in the preparation of the implant site in
order to follow the lingual bone wall. Subsequently, two implants that were 3.25 mm wide
s
and 10/11.5 mm long (Nanotite Biomet, West
Palm Beach, FL, USA) were placed in the fresh
extraction sockets with the neck of the implant at
the level of the buccal bone crest. An identical
procedure was followed on the test side. Two
implants were placed both in test and control site
of each dog. However, porcine collagenated bone
s
(MP3 , Osteobiol, Tecnoss, Coazze, Italy) was
placed on test sites to fill the gap around the
s
implant. A collagen membrane (Evolution , Osteobiol, Tecnoss) was utilized to cover the area of
GBR (Fig. 3). The buccal and lingual flaps were
managed and secured to allow a submerged healing of the experimental sites.
The dogs were placed on a plaque control
regimen that included tooth cleaning three times
a week with the use of toothbrush and dentifrice.
During the first week after surgery, the animals
received Amoxicillin (500 mg, twice daily) via
the systemic route. A lethal dose of Pentothal
s
Natrium was administered to the dogs according
to the experimental protocol: one dog 2 weeks
after implant placement; 2 dogs after 1 month;
and the remaining 2 dogs after 3 months. The
mandibles were dissected and placed in fixative.

Fig. 1. The graph shows bone resorption at different times on the control and test sites both in the fourth premolar and in the
first molar.


c 2011 John Wiley & Sons A/S

Barone et al  Bone remodelling after regenerative procedures around implants placed in fresh extraction sockets

Fig. 4. Drawing of the measurements taken in the present

study: I, implant shoulder; C, crestal level.
Fig. 2. The figure shows the area of implant insertion on the control side. Implants were placed in the socket of the distal root
of the fourth premolar and in the first molar area immediately after tooth extraction.

periodontal probe both on lingual and vestibular

side. The assessments were made immediately
after root extractions and at 2, 4 and 12 weeks
after implant placement. The mean values and
standard deviations among the animals were
calculated for each parameter and time point of
the study. Students test for paired data was used
to compare the means of the clinical measurements. P value was considered as 0.05.

Results
Fig. 3. On the test side, after the insertion, implants were covered by a biomaterial consisting of collagenated porcine bone
s
s
(MP3 Osteobiol, Tecnoss) and a membrane (Evolution ,Osteobiol, Tecnoss).

Each implant site was removed using a diamond

saw.

Histologic methods

The specimens were immediately fixed in 10%

buffered formalin at pH 7.2 for 1 week, and
washed in a solution of 0.1 M sodium phosphate
solution before dehydration in a graded series of
alcohols. The specimens were then embedded in
LR White resin (London Resin, Berkshire, UK).
Before sectioning, radiographies were made to
determine both the direction and the position of
the cutting edges. Undecalcified cut and ground
sections were prepared by using the Precise
Automated System 1 (Assing, Roma, Italy).
One central section from each implant site was
collected and ground to a final thickness of
40 5 mm (mean SD) using a graded series
(2401200) of silicon carbide grit papers under
running water (Exakt Apparatebau GmbH, Norderstedt, Germany). The sections were then
mounted on glass microscope slides and double

c 2011 John Wiley & Sons A/S

stained with toluidine blue. The acid fuchsin

solutions were prepared in the following way: a
toluidine blue solution was prepared adding 0.5 g
of sodium carbonate and 1 g of toluidine blue to
100 ml of distilled water and the acid fuchsin
solution was prepared by adding 20 g of acid
fuchsin to 100 ml of distilled water. The samples
were investigated using an Axiolab microscope
(Carl Zeiss, Jena, Germany) that was connected
to a digital camera (FinePix S2 pro, Fuji Photo
Co. Ltd, Minato-ku, Tokyo, Japan) and interfaced to a monitor and PC (Intel Pentium IV HT).
This optical system was combined with a software package with image capturing capabilities
(Image-Pro Plus 4.5, Media Cybernetics Inc.,
Images & Computer, Milano, Italy). The digitized images were stored in the TIFF format with
an N  M 3024  2016 grid of 24 bit pixels.
The distance from implant shoulder to the bone
wall crest was measured at the buccal and lingual
sites, as reported in Fig. 4. The distance from
apex of the alveolar crest (C) and implant
shoulder (I) was measured using a standardized

Each site healed without complications and gingival mucosa covered all implants. The tissues
that covered implants were constituted by a
dense connectival layer devoid of inflammatory
cells as ascertained in each histological examination. The implants appeared osteo-integrated according to the clinical criteria with the exception
of implants placed 15 days before, which
although seemed stable showed some peri-implant defects. The healing process was observed
in intervals: after 2 weeks, 1 month and 3
months, respectively. Statistical analysis indicated that differences between test and control
sites were significant (t  2.37, SD 0.431,
degrees of freedom 22, the probability of this
result, assuming the null hypothesis, is
0.027o0.05) (Fig. 1).
Histological and Histomorphometrical
Evaluations
Implant sites at 2 weeks

At this time point, one dog only was put down.

Two weeks after implant placement, both sides
showed incomplete healing. On the control side,

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Clin. Oral Impl. Res. 22, 2011 / 11311137

Barone et al  Bone remodelling after regenerative procedures around implants placed in fresh extraction sockets

and 7). The gap around the implant was filled

with porcine bone particles and connective tissue. Occasionally, particles were surrounded by
woven bone and in certain areas particles were
close to bone remodelling units located in the
woven bone. Measurements of bone levels indicated that both buccal and lingual bone were
located at the implant neck level in the fourth
pre-molar (0  0.5 mm). Conversely, at the first
molar the lingual bone was placed 1  0.5 mm
above the implant platform, while bone crest was
located at the same level as the implant neck,
buccally.

there was a horizontal gap between the implant

shoulder and marginal bone crest, which was
filled with an amount of provisional connective
tissue and a small amount of new woven bone
(Fig. 5). A large number of bone multicellular
units was observed in the lingual area. From a
histomorphometric point of view, our clinical
evaluations revealed that the fourth pre-molar
bone was located at the same level of the implant
platform both in the lingual and buccal
area (0.1  0.24 mm on the buccal side;
0  0.24 mm on lingual side). Moreover, at the
first molar, the buccal crest was located
0.5  0.24 mm below the implant neck (Table
1). In this area, the defect showed a similar
amount of newly formed, provisional connective
bone and a large number of osteoclasts. On the
test side, the implant was covered by a membrane that showed few signs of resorption (Figs 6

completely remodelled. From the histological

analysis it was evident that on the control sites
woven and lamellar bone filled the gap (Fig. 10).
In contrast, test sides showed residual bone
particles, surrounded by woven and lamellar
bone (Fig. 11). Numerous areas of active osteoclast resorption were observed, whereas connective tissue close to biomaterial particles were
detected at the most coronal part (Fig. 12). The

Implant sites at 4 weeks

At this time point two dogs were put down. On

the control site, bone levels of the fourth premolar were located 0.5  0.43 mm under the
implant platform on the buccal side and
0.2  0.43 mm lingually. In the first molar
area, the buccal bone showed an average decrease
of 0.5  0.43 mm, while the lingual bone was
placed 0  0.43 mm on average from the implant
shoulder (Fig. 8). On the test sites, the residual
membrane covered the implant area showing
some signs of degradation. Connective tissues
and woven bone mixed with the porcine particles
surrounded the implant area (Fig. 9). Measurements indicated that at the fourth pre-molar area
the buccal bone was 0.1  047 mm on average
under the implant platform, while the lingual
crest was placed 0.5  0.47 mm on average above
the implant shoulder. At the first molar, buccal
bone measured 1  0.47 mm on average above
the implant platform, while the lingual crest was
at the same level as the implant (0  0.47 mm).

Fig. 6. Histological section (buccallingual) of an implant at

the test site after 2 weeks. Biomaterial fills the gap between
implant and buccal crest. Few signs of bone remodelling are
present around the graft. Haematoxilin eosin stain (original
magnification  50).

Implant sites at 12 weeks

At this time point two dogs were put down. Soft

tissue healing was definitively achieved, and a
thick layer of peri-implant mucosa covered both
test and control sites in each dog. Histological
analysis revealed the absence of any horizontal
gaps between the implant and the buccal/lingual
walls, indicating that hard tissues have been

Fig. 5. Histological section (buccallingual) of an implant at

the control site after 2 weeks. Buccal bone crest is reabsorbed
up to the first thread and connective tissue fills the area of
remodelling. Haematoxilin eosin stain (original magnification  50).

Table 1. Mean vertical distance in millimetres and standard deviation (SD) between the buccal and
the lingual crest of the fourth pre-molar and the first molar in test and control groups at different
time points
Time

Test sites GBR implant (SD)

Two weeks
(1 dog)
1 month
(2 dogs)
3 months
(2 dogs)

Fourth pre-molar

First molar

Fourth pre-molar

First molar

0
(0.5)
0.1
(0.47)
0.15
(0.5)

0
(0.5)
 0.5
0.47)
0.5
(0.5)

0
(0.5)
1
(0.47)
 0.5
(0.5)

1
(0.5)
0
(0.47)
 0.5
(0.5)

0.1
(0.24)
0.5
(0.43)
0.7
(0.6)

0
(0.24)
0.2
(0.43)
 0.75
(0.6)

0.5
(0.24)
0.5
(0.43)
0
(0.6)

0
(0.24)
0
(0.43)
0.5
(0.6)

b, buccal; l, lingual.

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Control sites implant (SD)

Clin. Oral Impl. Res. 22, 2011 / 11311137

Fig. 7. X-rays image of a section (buccallingual) of an

implant at the test site after 2 weeks. It is well recognizable
as the area of biomaterial graft zone around the implant neck.


c 2011 John Wiley & Sons A/S

Barone et al  Bone remodelling after regenerative procedures around implants placed in fresh extraction sockets

Fig. 8. Histological section (buccallingual) of an implant at

the control site after 4 weeks. Lingual crest shows a slight
remodelling, while the levels of bone at the buccal crest are
located lower. Haematoxilin eosin stain (original magnification  50).

Fig. 9. Histological section (buccallingual) of an implant at

the test site after 4 weeks. Both lingual and buccal crest
show few signs of remodelling. Biomaterial is still present
around the implant shoulder. However, a large number of
bone remodelling lacunae surround the grafting area. Haematoxilin eosin stain (original magnification  50).

Fig. 10. Histological section (buccallingual) of an implant

at the control site after 12 weeks. Buccal bone crest is
reabsorbed up to 0.75 mm and less bone-to-implant contact.
Haematoxilin eosin stain (original magnification  50).

on average under the implant shoulder. On the

other hand, the test side showed different results.
In the fourth pre-molar, the buccal crest was
stable (barely 0.15  0.5 mm on average under
implant platform), while lingual bone was placed
0.5  0.5 mm on average under the implant
shoulder. The results for the first molar showed
that the buccal and lingual wall were located
0.5  0.5 mm on average above the implant neck.

months) of the buccal and lingual bone crest after

placing an implant into fresh extraction sockets.
Furthermore, we aimed to assess whether regenerative procedures could influence bone remodelling around implants.
The findings from this study confirm that
dimensional alveolar ridge changes occur following an implant placement in fresh extraction
sockets (pre-molar and molar sites) regardless of
the application of regenerative procedures. The
marginal peri-implant gaps present at the time of
implant placement were completely filled after 3
months with ex novo bone formation. However,
a certain degree of bone resorption was evaluated
at the bone walls on the test as well as on the
control side. Dimensional changes of the socket
wall were mostly pronounced at the buccal aspect. Yet, the results of the test side indicated that
regenerative procedures might have limited the
remodelling of the alveolar crest. With regard to
the control side, the first signs of remodelling
were observed only after 2 weeks. Few signs of
resorption were detected on the buccal side of the
fourth pre-molar (0.1  0.24 mm) and on the
first molar (0.5  0.24 mm), where GBR procedures were missing. On the other hand, the test
sites showed the absence of any remodelling
either on the buccal or the lingual wall. On the
first molar, 1  0.5 mm of bone overtopped the
implant platform at the lingual wall. This was
probably due to the fact that the implants had
been inserted placing their shoulder at the level of
buccal bone using the lingual wall as a guide.

Discussion

Fig. 11. Histological section (buccallingual) of an implant

at the test site after 12 weeks. Lingual and palatal bone crest
are not reabsorbed and new bone formed overgrowth on the
cover screw implant. Haematoxilin eosin stain (original
magnification  50).

crest of buccal bone at the fourth pre-molar of the

control was 0.7  0.6 mm on average under the
implant shoulder. Lingual bone crest was
0.75  0.6 mm on average above the implant
platform. At the first molar, the buccal wall
measured 0  0.6 mm on average from the implant, while the lingual crest was 0.5  0.6 mm

c 2011 John Wiley & Sons A/S

Many researchers have demonstrated the effects

of extraction on alveolar tissues over the years.
They have shown that as a consequence of tooth
loss, the volume of tissues in the edentoulous
ridge decreases especially on the buccal side,
resulting in a palatal/lingual shift of the residual
crest (Schropp et al 2003; Pietrokovski & Massler
1967; Barone et al. 2008). Findings from other
studies have evaluated the impact of immediate
implant placement after tooth extraction in terms
of bone crest remodelling (Cornelini et al. 2005;
Botticelli et al. 2006; Covani et al. 2007). Many
authors have also pointed out that several factors
could influence resorption of the buccal and
lingual wall after implant placement, such as
implant diameter, dimensions of the residual
alveolar crest, surgical technique and topography
of implant surface (Araujo et al. 2006; Vignoletti
et al. 2009). Thus, our investigation evaluated
the dimensional changes (from 2 weeks to 3

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Clin. Oral Impl. Res. 22, 2011 / 11311137

Barone et al  Bone remodelling after regenerative procedures around implants placed in fresh extraction sockets

metrical results at 3 months, showed an average

resorption of 0.7  0.6 mm on the buccal wall of
the fourth pre-molar of control side while no
signs of resorption were found on the first molar.
On the other hand, few signs of resorption were
seen on the buccal wall of the test side. In fact,
bone levels were located 0.15 mm under the implant platform on the fourth molar and 0.5 mm
above the implant platform on the first molar.
Comparing test and control results, it is reasonable to assume that the use of regenerative procedures after immediate implant placement has
advantages in terms of preservation of the alveolar
crest. We must underline that experiments in
fresh extraction sockets, where a regenerative
procedure with different material was carried
out, have shown that this practice may modify
modelling and limit the marginal ridge contraction, which normally occurs after tooth removal
(Die`s et al. 1996; Artzi et al. 2000; Carmagnola et
al. 2003; Norton et al. 2003; Vasilic et al. 2003;
Froum et al. 2004; Vance et al. 2004; Nevins et al.
2006; Araujo & Lindhe 2009). However, many
studies concluded that regenerative procedures
may limit buccal resorption, although a complete
preservation of the alveolar contour has never
been documented (Lekovic et al. 1997; Nevins
et al. 2006; Araujo et al. 2008).
The present study evaluated bone remodelling
after the implant placement in fresh extraction
sockets contextually to regenerative procedures,
and its findings are in accordance with other
similar studies. Little resorption occurs on the
buccal wall of the fourth pre-molar although the

first molar alveolar crest did not show any signs

of remodelling in the vertical direction. It was
suggested that the possible influence of socket
dimension could explain this result. Araujo et al.
(2005) observed the role of a wider gap between
the implant surface and the bone bed, concluding
that a lower reduction in bone height was obtained when implants were placed into a molar
rather than when placed into pre-molar socket.
However, whether the thickness of the wall or
the width of the gap between the implant surface
and bone crest plays a role in remodelling is still
under debate. Araujo et al. (2005) have observed
that the amount of bundle bone is higher in the
buccal area and Vignoletti et al. (2009) assumed
that this may explain the lack of bone resorption
at the lingual side. Our results also highlight little
resorption at the lingual aspect. The fact that the
implant platforms were placed at the level of the
buccal crest, resulting in the lingual wall frequently overtopping the implant at the baseline,
should be taken into account.
Fickl et al. (2009) described that the incomplete success of the regenerative techniques could
be dependent on surgical trauma during tooth
extraction such as incision flap elevation and
suturing. It has been proved that the use of a
mucoperiosteal flap for periodontal surgery induces a loss of bone height, due to both the acute
inflammation and the interruption of blood support to the alveolar bone after flap elevation
(Wilderman 1963; Staffileno et al. 1966; Wood
et al. 1972; Bragger et al. 1988). In the authors
opinion, this could explain the incomplete bone
preservation obtained after regenerative procedures, also seen in this experiment.
In conclusion, with the limits of this study,
due to the low numbers of samples, the findings
showed that GBR techniques were able to limit
resorption of the alveolar crest after tooth extraction. A pattern of bone remodelling after tooth
extraction and implant placement was observed
in the control sites (no GBR) as well as in test
sites (GBR), and although the exact cause of this
is unclear, surgical trauma could play a role.
However, it should be kept in mind that the
amount of bone remodelling in sites that received
augmentation techniques was lower than sites
that did not receive regenerative procedures.
Further studies are necessary to confirm these
results and to clarify the precise causes of bone
remodelling in fresh extraction sockets.

Periodontics and Restorative Dentistry 28:

12335.
Araujo, M.G. & Lindhe, J. (2005) Dimensional ridge
alterations following tooth extraction. An experimen-

tal study in the dog. Journal of Clinical Periodontology 32: 21221.

Araujo, M.G. & Lindhe., J. (2009) Ridge alterations
following tooth extraction with and without flap

Fig. 12. Higher magnification of Fig. 11. Micrograph showing the maturity of the new formed bone. Moreover, the presence of
residual bone particles indicate that remodelling was still occurring after 12 weeks.

Bone remodelling continued on the control side

during the first month. An average resorption of
0.5  0.43 and 0.75  0.43 mm was recorded
on the buccal walls of the fourth pre-molar and
the first molar. In contrast, the bone levels on the
test side were located barely 0.1  0.47 mm
under the implant platform on the buccal wall
of the fourth pre-molar, while 1  0.47 mm of
bone overtopped the implant platform of the first
molar. There were no differences between the
bone levels of the lingual wall of the test and
those of the control sites as the table shows.
These results are therefore partly in agreement
with the literature. In fact, De Sanctis et al.
(2009) showed that after immediate implant
placement, the healing process induces bone
resorption at the buccal aspect with an average
bone loss of 2.5 mm after 6 weeks. Their findings
are similar to the Araujo et al. (2006), who
observed that buccal crest was located 2.6 
0.4 mm apical to the implant platform.
More recently, a similar experimental study in
Beagle dogs using the same surgical approach has
confirmed our conclusions reporting an average
bone loss of 0.77  0.8 mm after only 2 weeks
and 0.7  0.24 mm a month later (Vignoletti
et al. 2009). Moreover, comparable results were
also reported in another experimental study in
dogs where implants 3.3 mm large in diameter
were placed using flap vs. flapless surgery. Vertical bone resorption at the buccal wall was 1.33
in the flapped group and 0.8 mm in the flapless
group, respectively, after 3 months of healing
(Blanco et al. 2008). Similarly, our histomorpho-

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