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Healing of extraction sockets treated with anorganic bovine bone minerals: a micro-CT analysis

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Healing of extraction sockets treated with anorganic bovine bone minerals: a micro-CT analysis

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Content UNIVERSITY OF SOUTHERN CALIFORNIA

HERMAN OSTROW SCHOOL OF DENTISTRY

HEALING OF EXTRACTION SOCKETS TREATED WITH ANORGANIC BOVINE
BONE MINERALS: A MICRO-CT ANALYSIS

By

NEEMA BAKHSHALIAN

A thesis submitted
in partial fulfillment of the
requirements for the degree of
Masters in Science

Degree Awarded:
Summer Semester, 2014

ii

TABLE OF CONTENTS
List of Tables ................................................................................................................................. iii
List of Figures ................................................................................................................................ iv
Summary ....................................................................................................................................... vii
Highlights ..................................................................................................................................... viii
1. INTRODUCTION .................................................................................................................. 1
2. RESULTS ............................................................................................................................... 3
3. EXPERIMENTAL PROCEDURES ...................................................................................... 5
4. DISCUSSION ......................................................................................................................... 8
5. CONCLUSION .................................................................................................................... 13
6. FIGURES ............................................................................................................................. 14
7. TABLES ............................................................................................................................... 23
REFERENCES ............................................................................................................................. 26

iii

LIST
OF
TABLES

Table
1:
The
demographics
of
the
patients
included
in
the
study.

Table
2:
Distribution
of
the
sockets
treated
with
anorganic
bovine
bone
minerals.

Table
3:
Studies
providing
histomorphometrical
analyses
of
bone
healing
following
the
use

of
large
and
small
ABBM.

iv

LIST
OF
FIGURES

Fig
1:
Clinical
and
radiographic
images
of
a
representative
patient
treated
with
ridge

preservation
procedure.
A)
Buccal
clinical
view
before
extraction,
B)
buccal
clinical
view
of

the
restored
implant,
one
year
after
implant
placement,
C)
radiographic
view
before
the

extraction,
D)
radiographic
view
before
the
implant
placement,
E)
radiographic
views

immediately
post
implant
installation,
F)
one
year
post
implant
placement,
and
G)
two

years
post
implant
placement,
H)
three
year
post
implant
placement.

Fig
2:
Representative
core
sample
harvested
from
an
extraction
socket
and
associated

micro-‐CT
images.
A)
Core
sample
procured
during
implant
placement
using
a
trephine
drill

with
external
diameter
of
3.3
mm,
B)
representative
composite
3D
reconstructed
image
of

micro-‐CT
data
from
the
core
sample,
C)
Segmented
3D
image
of
Bone,
D)
Segmented
3D

image
of
residual
graft.

Fig
3:
Quantitative
analysis
of
micro-‐CT
data.
Mean
proportion
of
bone
(blue),
connective

tissue
(purple),
and
residual
graft
material
(yellow)
as
determined
by
quantitative
analysis

of
micro-‐CT
data
of
core
samples.

Fig
4.
Comparison
of
the
quantitative
analysis
of
micro-‐CT
data
based
on
the
position
of
the

sockets.
Molar
(blue),
premolar
(red),
and
anterior
sockets
(green)
as
determined
by

quantitative
analysis
of
micro-‐CT
data
of
core
samples.

v

Fig
5.
Comparison
of
the
quantitative
analysis
of
micro-‐CT
data
based
on
the
position
of
the

sockets.
Molar
sockets
(blue),
premolar
sockets
(red),
and
anterior
sockets
(green)
as

determined
by
quantitative
analysis
of
micro-‐CT
data
of
core
samples.

Fig
6.
Comparison
of
the
quantitative
analysis
of
micro-‐CT
data
between
the
Maxillary
and

Mandibular
arch.
Maxillary
sockets
(blue),
and
Mandibular
sockets
(red).

Fig
7.
Comparison
of
the
quantitative
analysis
of
micro-‐CT
data
categorized
by
the
age
of

the
patients.

Fig
8.
Comparison
of
the
quantitative
analysis
of
micro-‐CT
data
segregated
according
to

gender.
Females
(blue),
and
Males
(red).

Fig
9.
Percentage
of
residual
graft
materials
and
bone
relative
to
the
healing
time
of
the

sockets.

Fig
10.
The
correlation
between
marginal
bone
changes
on
mesial
and
distal
aspects
of

implants
placed
into
sites
from
which
core
samples
were
obtained
and
the
percentage
of

bone
detected
within
the
bone
cores
(R2=0.42
and
0.04,
for
mesial
and
distal,
respectively).

Fig
11.
Micro-‐CT
images
of
bone
harvested
from
a
socket
following
healing
of
ridge

preservation
procedure,
showing
3D
reconstruction
(A),
higher
magnification
of
the

vi

outlined
area
(B),
and
2D
slice
through
the
center
(B).
The
secluded
islands
of
bone
provide

evidence
for
de
novo
bone
formation.
The
residual
graft
(blue)
is
surrounded
by
bone.

vii

SUMMARY

Bone
resorption
and
ridge
atrophy
result
from
tooth
extraction
due
to
the
lack
of
the

stimulating
signals
from
periodontal
ligament.
Ridge
preservation
using
various
bone

grafting
materials
has
been
proposed
as
a
means
to
minimize
post-‐extraction
atrophy.
This

case-‐series
study
evaluated
the
healing
of
extraction
sockets
following
ridge
preservation

procedure
with
anorganic
bovine
bone
minerals
(ABBM)
using
micro-‐computed

tomography.
The
purpose
of
the
present
study
was
to
examine
the
quality
of
the
bone

found
in
sites
following
of
healing
of
ridge
preservation
procedure
utilizing
micro-‐CT

imaging.
The
sockets
of
68
teeth
extracted
by
reduced-‐trauma
technique
were
filled
with

large
particles
(1-‐2
mm)
of
ABBM
and
covered
by
Polytetrafluoroethylene
membrane
for

four
weeks.
Following
the
ridge
preservation
procedure
(mean
147
+
100
days),
core

samples
were
collected
from
each
site
using
trephine
drills
(3.3
mm
outer
diameter)
prior

to
implant
placement.
Core
samples
were
scanned
using
micro-‐computed
tomography
and

the
3D
reconstructed
volumes
were
examined
using
Amira
software.
The
percentage
of

bone,
connective
tissue,
and
remaining
graft
material
were
measured
in
each
sample.

Furthermore,
de
novo
bone
formation
was
evaluated
by
3D
rendering
of
the
images.

Quantitative
analysis
of
different
segments
revealed
that
the
core
samples
were
comprised

by
material
with
densities,
which
were
consistent
with
the
following
material:
bone

(40.1%),
connective
tissue
(47.9%)
and
residual
graft
particles
(12.0%).
Evidence
of
de

novo
bone
formation
was
observed,
as
islands
of
bone
in
direct
apposition
to
the
graft

particles.

viii

HIGHLIGHTS:

• The
micro-‐CT
results
revealed
40%
bone,
48%
connective
tissue,
and
12%

residual
grating
materials
in
sockets
grafted
with
anorganic
bovine
bone.

• The
samples
from
the
age
group
55-‐59
year
old,
showed
lower
amount
of

residual
graft
material
and
higher
amount
of
bone
(p=0.053).

• The
position
of
the
tooth,
healing
time
of
the
grafted
socket,
and
the
gender

of
the
patient
had
no
effect
on
the
amount
of
residual
graft
material
or
bone.

• This
study
provided
clear
evidence
for
de
novo
bone
formation
following

healing
of
extraction
sockets
grafted
with
anorganic
bovine
bone
minerals.

1

1.
INTRODUCTION

A
number
of
animal
and
clinical
studies
have
demonstrated
post-‐extraction

remodeling
of
the
alveolar
bone,
leading
to
varying
degrees
of
atrophy
(Araújo
and

Lindhe,
2005;
Berendsen
et
al.,
2009;
Cardaropoli
et
al.,
2005;
Hämmerle
et
al.,

2011;
Vignoletti
et
al.,
2011).
Recent
consensus
report
of
human
clinical
data
have

reported
the
magnitude
of
the
ridge
atrophy
to
be
3.8
mm
and
1.24
mm
in

horizontal
and
vertical
dimensions,
respectively
(Hämmerle
et
al.,
2011).
Most
of

the
ridge
atrophy
occurs
within
the
first
3
months
after
extraction;
however
it
has

been
reported
that
ridge
resorption
could
continue
up
to
one
year
post
extraction

(Schropp
et
al.,
2003).
An
array
of
therapeutic
strategies
has
been
proposed
to

reduce
the
magnitude
of
the
alveolar
ridge
atrophy
with
varying
degrees
of
success,

including
immediate
implant
placement,
ridge
preservation
procedure
and
root

retention.
Various
ridge
preservation
techniques
using
different
bone
grafting

materials
have
been
proposed
as
a
means
to
minimize
post-‐extraction
atrophy

(Araújo
et
al.,
2010;
2006;
Barone
et
al.,
2012;
Cardaropoli
et
al.,
2005;
Fickl
et
al.,

2008a;
2008b;
2008c;
Vignoletti
et
al.,
2012).
Based
on
the
meta
analysis
of
the
data,

ridge
preservation
techniques
can
reduce
the
amount
of
ridge
resorption
by
1.84

mm
in
width
and
1.47
mm
in
height
(Vignoletti
et
al.,
2011).
In
the
author’s
opinion,

the
reduction
in
height
may
be
very
significant
for
implant
placement
in
the
esthetic

area,
especially
in
patients
with
a
high
small
line.
Also
about
1.84
mm
less

resorption
in
width
of
the
ridge
may
be
the
defining
parameter
in
the
possibility
of

implant
placement
after
extraction
or
the
need
for
complex
ridge
augmentation

procedures
prior
to
implant
placement.
A
recent
meta-‐analyses
reported
the
range

2

of
width
reduction
after
extraction
to
be
2.46
to
4.56
vs
1.14
to
2.5
mm
for
the

spontaneous
healing
and
ridge
preservation,
respectively.
Moreover,
the
range
of

vertical
dimension
loss
is
reported
to
be
0.9
to
3.6
vs
a
gain
of
1.3
to
a
loss
of
0.62

mm
in
spontaneous
healing
and
ridge
preservation,
respectively
(Morjaria
et
al.,

2012).

Previous
studies
have
used
anorganic
bovine
bone
minerals
(ABBM)
with
or

without
a
membrane
for
ridge
preservation
procedures
(Araújo
and
Lindhe,
2009;

2010;
Araújo
et
al.,
2008;
Artzi
et
al.,
2000;
Cardaropoli
et
al.,
2012;
Carmagnola
et

al.,
2003;
Froum
et
al.,
2004;
Lee
et
al.,
2009;
Molly
et
al.,
2008;
Norton
et
al.,
2003;

Vance
et
al.,
2004).
These
studies
reported
various
degrees
of
new
bone
formation,

connective
tissue
and
residual
graft
material.
The
present
report
is
part
of
a
multi-‐
part
case-‐series
study,
each
reporting
a
discrete
outcome
of
a
particular
ridge

preservation
protocol.

The
ridge
preservation
protocol
entailed
minimally
invasive

tooth
extraction
without
flap,
loose
placement
of
ABBM
graft
material
without

condensation
and
coverage
of
the
graft
material
with
a
non-‐resorbable
PTFE

membrane,
which
extended
only
within
the
socket
without
deliberate
extension

under
a
flap.
The
present
report
provides
analyses
of
the
healing
patterns
of
tissues

formed
following
ridge
preservation
procedure.
Other
parts
of
this
multi-‐part
series

report
on
histologic
outcomes,
as
well
as
the
outcome
of
implants
placed
within

ridge
preservation
sites.

3

2.
RESULTS

Clinical
characteristics
of
the
patients.
Fifty
patients
were
included
in
the
study

including
32
females
and
18
males
with
average
age
of
59
and
57,
respectively

(Table
1).
Sixty-‐eight
bone
core
samples
were
harvested
during
the
installation
of

dental
implants
in
sites
previously
grafted
with
ABBM
using
the
protocol
outlined
in

the
material
and
methods
section.

The
samples
included
10
anterior,
21
premolar

and
37
molar
sockets
(Table
2).
The
outcome
of
implants
installed
into
sites
treated

in
this
study
is
reported
separately.

Micro-‐CT
analyses:
Volumetric
analysis
demonstrated
the
mean
height
of
the

core
samples
was
7.38
mm.
This
is
important
to
note,
confirming
that
core
samples

were
taken
from
the
crestal
part
of
the
alveolar
ridge,
which
primarily
consisted
of

grafted
bone
and
not
host
bone.

Quantitative
analysis
of
different
segments
revealed
that
the
core
samples

were
comprised
by
volumes
with
densities,
which
were
consistent
with
bone

(40.1±10.83%),
connective
tissue
(47.9±4.86%)
and
residual
graft
particles

(12.0±8.89%)
(Fig
3).

The
amount
of
residual
graft
material
was
different
in
anterior
and
posterior

sockets,
however,
the
difference
was
no
statistically
significant
(Fig
4),
among

molar,
premolar,
or
anterior
teeth
(Fig
5),
or
between
maxillary
versus
mandibular

regardless
of
their
position
(Fig
6).

The
samples
from
the
age
group
55-‐59
year
old,
showed
lower
amount
of

residual
graft
material
and
higher
amount
of
bone
(p=0.053).
The
amount
of
bone

4

increased
and
the
amount
of
residual
graft
decreased
from
40
to
50-‐54
years
old

and
reversed
after
that
up
to
65
years
of
age
and
above
(Fig
7).
Gender
showed
no

effects
on
the
amount
of
bone
or
residual
graft
material
(Fig
8).
Healing
time
did
not

show
a
correlation
with
bone
and
residual
graft
material
(R
2
=0.034
and
0.028,

respectively,
Fig
9).

The
marginal
bone
changes
around
the
implants
placed
in
the
sites
treated

with
ABBM
were
analyzed
and
reported
previously
(Wu,
2013).
The
percentage
of

bone
showed
a
moderate
negative
correlation
with
the
marginal
bone
loss
on
the

mesial
aspects
of
the
implant
(R
2
=0.42).
Surprisingly
not
such
correlation
was

observed
with
the
marginal
bone
loss
on
the
distal
aspects
of
the
implants
(R
2
=0.04,

Fig
10).

Secluded
islands
of
bone
were
observed
in
the
3D
reconstructed
volumes,

which
were
not
connected
to
the
parent
bone.
Following
sectioning
of
these
islands,

residual
graft
particles
were
observed
in
the
center
of
the
islands
with
bone

apposition
directly
around
them
(Fig
11).
This
finding
confirms
the
de
novo
bone

formation
around
the
particles
of
bone
graft.
This
manifestation
of
healing
was
more

apparent
during
earlier
healing
periods,
prior
to
complete
healing
of
the
sockets,

where
the
new
bone
had
coalesced.

5

3.
EXPERIMENTAL
PROCEDURES

Ridge
preservation
procedure.
Fifty
patients
were
included
in
this
case-‐series
study

(Table
1).
Sixty-‐eight
non-‐maintainable
teeth
were
extracted
using
reduced-‐trauma

technique
(Table
2).
Patients
received
premedication
an
hour
prior
t
the
procedure

(preferably
2
grams
of
amoxicillin).
Extraction
of
teeth
was
carried
out
without

reflection
of
a
flap
and
with
the
aid
of
periotomes
and/or
piezoelectric
surgical

device
to
sever
the
periodontal
ligaments.
Multi-‐rooted
teeth
were
sectioned
using
a

high-‐speed
hand
piece
and
each
root
extracted
separately.
Following
extraction,
the

sockets
were
debrided
thoroughly
with
surgical
curettes
to
remove
all
the
soft

tissue
remnants
and
periodontal
ligament
from
socket
walls.

Polytetrafluoroethylene
(PTFE)
membranes
(GBR-‐200,
Osteogenics,
Lubbock,
TX,

USA)
were
attached
to
gingival
tissues
surrounding
extraction
sockets
using
a
single

horizontal
mattress
suture,
which
extended
from
facial
to
lingual/palatal
aspect.

The
sutures
were
initially
placed
loosely
before
addition
of
graft
material.
The

sockets
were
filled
with
large
particles
(1-‐2
mm)
of
ABBM
(Bio-‐Oss,
Geistlich,

Switzerland)
avoiding
condensation
of
graft
particles
so
that
the
spaces
between

particles
were
maintained.

Immediately
after
the
addition
of
graft
material,
the

suture
was
tightened
and
the
membrane
was
secured
in
an
effort
to
rapidly
cover

the
graft
material
and
prevent
its
contamination.
Patients
received
antibiotic

(preferably
Amoxicillin
500
mg
TID
for
7
days)
and
Naproxen
sodium
(550
mg
BID

for
2-‐7
days)
following
the
procedure.
They
were
instructed
to
brush
the
area
with

an
ultra-‐soft
toothbrush
starting
immediately
post-‐operatively
and
rinse
with

Chlorhexidine
Gluconate
(0.12%
rinse
twice
daily
for
one
week
and
brush
the
area

6

with
that
antiseptic
solution
for
and
additional
3
weeks).
The
membranes
were

removed
4
weeks
following
the
extraction,
at
which
point
any
loose
unincorporated

ABBM
granules
removed
from
the
surface.

Core
sample
biopsy.
Following
the
ridge
preservation
procedure
(mean

147±100
days),
at
the
time
of
implant
placement,
core
samples
were
collected
from

each
site
using
a
trephine
drills
(3.3
mm
outer
diameter),
which
were
narrower
than

the
diameter
of
the
final
drill
utilized
in
placing
the
implants
(Fig
1).
Dental
implants

were
placed
after
completion
of
osteotomy
without
any
further
ridge
augmentation.

Core
samples
were
stored
in
buffered
10%
formalin
until
micro-‐CT
imaging
and

histologic
preparation.

Micro-‐Computed
Tomography
Analyses.
Core
samples
were
scanned
using
micro-‐
computed
tomography
(MicroCAT
II,
Siemens
Medical
Solutions
Molecular
Imaging,

Knoxville,
TN).
The
spatial
resolution
of
the
scanned
image
was
43.743
µm
(Voxel

dimension),
and
bit
depth
was
16bits.
After
scanning,
the
2D
image
data
were
stored

in
the
Digital
Imaging
and
Communications
in
Medicine
(DICOM)
format,
and

transferred
to
a
computer,
where
a
3-‐D
reconstruction
and
analysis
were

performed.
Data
image
analysis
was
carried
out
using
Amira
software
(Visage

Imaging,
San
Diego,
CA).
The
tissues
contained
within
each
core
sample
were

segmented
using
a
global
thresholding
procedure.
The
thresholds
were
defined

based
on
the
known
density
ranges
for
bone,
graft
material,
and
connective
tissue

graft.
Areas
corresponding
to
different
thresholds
were
color
coded
and
used
to

develop
3D
volumes
of
each
segment.
3D
volumes
were
reconstructed
and

7

quantified
for
the
total
core
sample,
area
corresponding
to
connective
tissue,
bone

and
residual
graft
material
(Fig
2).

Statistical
analysis.
The
effect
of
different
factors
including
the
position
of
the

sockets,
age,
gender,
and
healing
time
on
the
amount
of
bone
and
residual
graft

material
were
analyzed.
In
order
to
do
so,
the
homogeneity
of
the
variances
were

performed
by
Levene’s
test
and
the
percentage
of
bone,
residual
graft
material,
and

connective
tissue
were
analyzed
using
ANOVA
and
Tukey
HSD
post-‐hoc
test.

Moreover,
the
correlation
between
the
percentage
of
bone
and
the
marginal
bone

loss
around
the
implants,
which
were
reported
separately
(Wu,
2013),
was

calculated.

8

4.
DISCUSSION

The
results
of
this
study
showed
a
higher
amount
of
bone
and
lower
amount
of

residual
graft
material
in
the
core
samples
comparing
to
the
similar
studies
done

previously
(Brownfield
and
Weltman,
2012;
Carmagnola
et
al.,
2003;
Molly
et
al.,

2008;
Norton
et
al.,
2003;
Vance
et
al.,
2004).
In
the
authors
opinion
the
reasons
for

this
phenomenon
are
2
folds:
First,
in
this
procedure
the
graft
material
was
placed

loosely
in
the
entire
length
of
the
socket
unlike
previous
techniques
where
the
graft

material
was
condensed
into
the
sockets
(Artzi
and
Nemcovsky,
1998;
Barone
et
al.,

2008;
Molly
et
al.,
2008).
This
type
of
graft
placement
will
allow
more
spaces

between
the
graft
particles
and
hence
there
is
more
room
for
angiogenesis
and
new

bone
formation,
which
eventually
bridged
the
graft
particles
and
therefore
led
to
an

increase
in
the
amount
of
total
bone.
Second,
in
this
technique
all
the
sockets
were

grafted
using
the
large
particle
(1-‐2
mm
3
)
material,
which
led
to
even
more
spaces

between
the
particles
and
further
increased
the
amount
of
bone
in
the
core
samples.

Also
large
graft
particles
occupy
more
volume
with
less
material
and
therefore
the

total
amount
of
graft
needed
to
fill
up
the
socket
will
be
less
comparing
to
the
use
of

small
size
particles.
Testori
et
al,
(2013)
compared
the
effect
of
ABBM
particle
size

on
the
amount
of
vital
bone
following
maxillary
sinus
lift
procedure.
They
compared

large
particle
(1-‐2
mm)
with
small
particles
(0.25-‐1
mm)
and
reported
that
the

amount
of
vital
bone
6-‐8
months
after
the
surgery
was
significantly
higher
in
the

group
with
large
particle
(26.77%
vs
18.77%).
However,
in
a
similar
study,

Chackartchi
et
al
(2010),
showed
that
there
was
no
statistically
significant

differences
between
the
amount
of
vital
bone
and
residual
graft
material
following

9

the
use
of
small
or
large
particle
sizes
in
maxillary
sinus.
Table
3
summarizes
some

of
the
studies
that
reported
histomorphometric
results
of
the
bone
healing
following

the
use
of
small
and
large
particles
of
ABBM
in
different
augmentation
procedures.

Previous
reports
in
this
area
mostly
used
histomorphometry
and
usually

looked
at
few
sections
from
each
sample,
which
provides
valuable
information.

Nonetheless,
few
histologic
sections
may
not
represent
the
whole
core
sample.
The

result
of
this
study
refines
the
range
of
bone
and
residual
graft
material
following

the
ridge
preservation
procedures
reported
in
the
literature
with
the
use
of
3D

imaging
technology
which
includes
the
whole
volume
of
the
samples
and
can
be

considered
innovative
(Brownfield
and
Weltman,
2012).
Previously,
Atrzi
reported

that
the
percentage
of
vital
bone
increases
in
the
apical
portion
of
the
core
samples

following
ridge
preservation
procedure
and
therefore
the
location
of
the
samples

taken
for
histomorphometry
could
be
a
very
important
factor
regarding
the
results

of
the
study,
which
could
be
considered
one
of
the
limitations
of
histomorphometry

in
comparison
to
a
3D
volumetric
study
(Artzi
et
al.,
2000).
In
our
study,
our

samples
were
taken
from
the
crestal
portion
(mean
7mm).

The
effects
of
different
factors
on
the
percentage
of
bone
and
residual
graft

material
were
evaluated
in
the
present
study.
Samples
obtained
from
anterior

sockets
showed
a
higher
amount
of
residual
graft
and
lower
amount
of
bone.
One
of

the
possible
reasons
for
this
result
could
be
the
wider
sockets
of
the
anterior
teeth

which
require
more
graft
material.
A
possible
explanation
for
higher
amount
of

residual
graft
and
lower
presence
of
bone
in
the
anterior
region
may
be
due
to
the

thin
facial
plates
in
this
region
(Nahass
and
N
Naiem,
2014),
which
inevitably
is
lost

10

during
the
healing
of
sockets
(Heggeler
et
al.,
2010).
This
may
lead
to
fewer
alveolar

ridge
walls
contribute
to
healing
within
graft
material.
Also
since
the
diameter
of
the

sockets
are
well
beyond
the
3
mm
diameter
of
the
core
samples,
there
is
a
lower

possibility
of
harvesting
host
bone
with
the
samples
which
could
be
further

decreased
by
the
absence
of
septum
in
those
sockets.
The
cores
from
mandibular

anterior
sockets
contained
less
graft
material,
which
could
also
be
explained
by

their
smaller
diameter
in
comparison
to
their
maxillary
counterparts.
The
samples

from
premolar
and
molar
extraction
sockets
showed
no
differences
in
the
amount
of

residual
graft
and
bone
demonstrating
that
the
positions
of
the
sockets
have
no

effect
except
for
the
size
of
them.

The
amount
of
bone
showed
an
increase
in
samples
from
patient
40
to
59

years
old
and
then
a
decrease
in
older
patients
while
the
residual
graft
material

showed
an
opposite
pattern.
The
55-‐59
year
old
group
showed
the
highest
amount

of
bone,
albeit
the
difference
was
not
statistically
significant
(p=0.053).

Unfortunately
the
authors
cannot
offer
any
explanation
for
this
finding.
The
healing

time
showed
no
effect
on
the
amount
of
bone
or
the
residual
graft
material,
which
is

consistent
with
previous
reports.
Norton
et
al,
reported
that
the
core
samples

harvested
4-‐5
months
after
ridge
preservation
showed
comparable
amount
of
vital

bone
and
residual
graft
materials
in
comparison
to
cores
harvested
after
6-‐10

months
(Norton
et
al.,
2003).
Also
other
studies
showed
that
even
cores
that

harvested
about
3
years
after
the
procedure
were
comprised
of
bone
and
graft

material
within
the
range
of
earlier
samples
(Piattelli
et
al.,
1999;
Skoglund
et
al.,

1997).
The
range
of
the
healing
time
in
this
study
was
49-‐635
days.
Several
factors

11

such
as
the
size
of
the
extraction
socket,
the
number
of
contiguous
teeth
extracted,

the
presence
of
endodontic
lesions
prior
to
extraction,
and
possible
sinus

communication
prior
or
following
the
extraction
should
be
considered
when

deciding
about
the
healing
period
for
every
individual
case.

Although
this
study
and
the
previous
reports
provided
valuable
information

regarding
the
pattern
of
the
healing
of
extraction
sockets
following
ridge

preservation
procedures,
there
is
no
evidence
to
show
the
significance
of
the

amount
of
bone
or
the
residual
graft
material
in
the
success
rate
of
the
implants

placed
in
those
sockets.
This
study
examined
the
correlation
between
the
amount
of

bone
and
the
implant
outcome.
The
amount
of
bone
in
the
core
samples
showed
a

negative
correlation
with
the
mesial
marginal
bone
loss
around
the
implants
placed

in
the
grafted
sockets.
Marginal
bone
loss
on
the
mesial
side
ranged
between
0.3
to

5.5
mm
in
this
study.
One
of
the
factors
causing
this
bone
loss
could
be
the

topography
of
the
bone
at
the
implant
site
and
the
adjacent
teeth.
In
most
cases

where
there
is
no
tooth
distal
to
the
implant.
the
level
of
attachment
on
the
teeth

mesial
to
the
implants
are
much
higher
which
causes
a
bony
ramp
on
that
side
and

therefore
deeper
pockets
and
higher
chance
of
local
inflammation,
infection
and

bone
loss.
It
has
been
reported
previously
that
the
absence
or
presence
of
teeth

adjacent
to
the
implant
and
also
the
attachment
levels
on
the
adjacent
teeth
could
be

important
in
the
level
of
the
bone
following
ridge
preservation
and
implant

placement
(Barone
et
al.,
2008).

The
marginal
bone
loss
on
the
distal
side
showed

no
correlation
to
the
amount
of
bone
in
the
core
samples.

12

One
of
the
concerns
regarding
the
use
of
non-‐resorbable
graft
materials
in

the
socket
preservation
procedure
is
the
possibility
of
the
residual
graft
interfering

with
a
successful
implant
placement.
However,
several
studies
showed
that
the

outcome
of
implant
therapy
in
sites
with
previous
ridge
preservation
procedure
did

not
differ
form
implants
placed
in
the
pristine
bone
(Crespi
et
al.,
2009;
Nevins
et
al.,

1998).
Moreover,
previous
reports
(Berglundh
and
Lindhe,
1997)
have
showed
that

the
residual
bone
graft
particles
will
never
be
in
direct
contact
with
the
implant

surface
and
contact
osteogenesis
always
occurs
on
the
implant
surface,
which
leads

to
apposition
of
a
layer
of
vital
bone
on
the
implant
surface.

Previously
serial
histologic
samples
(Barone
et
al.,
2008;
Vance
et
al.,
2004)

were
used
to
evaluate
the
pattern
of
bone
healing
in
the
extraction
socket
and
the

general
belief
was
that
bone
formation
in
the
sockets
occurs
through
distant

osteogenesis
from
the
walls
of
the
sockets
and
the
graft
material
does
not
play
a
role

in
bone
formation.
With
the
use
of
3D
imaging
technology
employed
in
this
study,
it

was
possible
to
find
secluded
bone
nodules
within
the
core
samples
that
were
not

connected
to
the
host
bone
in
any
direction.
Following
sectioning
of
these
bony

islands,
graft
material
was
observed
in
the
center
of
these
nodules
with
bone

apposition
around
them
which
is
a
clear
evidence
for
contact
osteogenesis
(or
de

novo
bone
formation
(Berglundh
et
al.,
2003;
Vignoletti
et
al.,
2009))
around
the

graft
particle.

13

5.
CONCLUSIONS

The
results
of
the
present
study
provided
valuable
information
regarding
healing
of

the
extraction
sockets
treated
with
the
ridge
preservation
technique
using
large

particle
size
ABBM,
placed
loosely
in
extraction
sockets
protected
with
non-‐
resorbable
membrane.
The
samples
were
comprised
of
areas
consistent
with
40.1%

bone,
47.9%
connective
tissue
and
12.0%
residual
graft
material.
Further
studies

are
required
to
determine
what
percentage
of
residual
graft
material
is
necessary

for
successful
implant
outcomes.

14

6.
FIGURES

Fig
1:

Fig
2:

15

Fig
3:

Fig
4.

0

10

20

30

40

50

60

70

Residual
Graft
%
Bone
%
Connective
Tissue
%

%

Molars
Premolars
Anteriors

16

Fig
5.

0

10

20

30

40

50

60

70

Maxilla
Mandible
Maxilla
Mandible
Maxilla
Mandible

Anterior
Premolar
Molar

%

Residual
Graft
Bone
Connective
Tissue

17

Fig
6.

0

10

20

30

40

50

60

70

Residual
Graft
%
Bone
%
Connective

Tissue
%

%

Maxilla

Mandible

18

Fig
7.

0

10

20

30

40

50

60

70

Residual
Graft
Material
Bone
Connective
Tissue

%

40-‐44
45-‐49
50-‐54
55-‐59
60-‐64
65-‐above

19

Fig
8.

0

10

20

30

40

50

60

70

Residual
Graft
%
Bone
%
Connective
Tissue

%

%

Female

Male

20

Fig
9.

0

10

20

30

40

50

60

70

0
100
200
300
400
500
600
700

Bone
(%)

Healing
Time
(days)

0

5

10

15

20

25

30

35

0
100
200
300
400
500
600
700

Residual
Graft
Material
(%)

Healing
Time
(days)

21

Fig
10.

-‐6.00

-‐5.00

-‐4.00

-‐3.00

-‐2.00

-‐1.00

0.00

0
20
40
60
80

Marginal
Bone
Changes
Around
Implants
(mm)

Bone
(%)

Mesial

Distal

22

Fig
11.

23

7.
TABLES

Table
1:
The
demographics
of
the
patients
included
in
the
study.

Number
Mean
Age
(Range)

Total
50
58
(40-‐85)

Females
32
59
(40-‐85)

Males
18
57
(45-‐77)

Table
2:
Distribution
of
the
sockets
treated
with
anorganic
bovine
bone
minerals.

Total
Anterior
Premolar
Molar

Maxilla
31
4
12
15

Mandible
37
6
9
22

24

Table
3:
Studies
providing
histomorphometrical
analyses
of
bone
healing
following

the
use
of
large
and
small
ABBM.

Study

Type
of

Procedure

Bone

Connective

Tissue

Residual

Graft

Material

Small
Particles
(0.25-‐1
mm)

Froum
et
al.
(2004)

Ridge

Preservation

42%

Norton
et
al.
(2003)

Ridge

Preservation

27%
47%
26%

Zitzmann
et
al.

(2001)

Bone

Augmentation

27%
38%
30.5%

Artzi
et
al.
(2000)

Ridge

Preservation

46%
23%
31%

Yildirim
et
al.
(2000)
Sinus
Lift
15%
56%
30%

Araújo
and
Lindhe

(2010)

Ridge

Preservation

54%

(old),

18%

new

16%
9%

Cardaropoli
et
al.

(2012)

Ridge

preservation

26%
55%
18%

25

Large

Particles

(1-‐2

mLm)

Molly
et
al.
(2008)

Ridge

Preservation

21%

20%

Simunek
et
al.
(2008)

Sinus

Augmentation

34%
31%
35%

Unknown

Lee
et
al.
(2009)

Ridge

Preservation

24%
34%
25%

26

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Abstract (if available)

Abstract Bone resorption and ridge atrophy result from tooth extraction due to the lack of the stimulating signals from periodontal ligament. Ridge preservation using various bone grafting materials has been proposed as a means to minimize post-extraction atrophy. This case-series study evaluated the healing of extraction sockets following ridge preservation procedure with anorganic bovine bone minerals (ABBM) using micro-computed tomography. The purpose of the present study was to examine the quality of the bone found in sites following of healing of ridge preservation procedure utilizing micro-CT imaging. The sockets of 68 teeth extracted by reduced-trauma technique were filled with large particles (1-2 mm) of ABBM and covered by Polytetrafluoroethylene membrane for four weeks. Following the ridge preservation procedure (mean 147 + 100 days), core samples were collected from each site using trephine drills (3.3 mm outer diameter) prior to implant placement. Core samples were scanned using micro-computed tomography and the 3D reconstructed volumes were examined using Amira software. The percentage of bone, connective tissue, and remaining graft material were measured in each sample. Furthermore, de novo bone formation was evaluated by 3D rendering of the images. Quantitative analysis of different segments revealed that the core samples were comprised by material with densities, which were consistent with the following material: bone (40.1%), connective tissue (47.9%) and residual graft particles (12.0%). Evidence of de novo bone formation was observed, as islands of bone in direct apposition to the graft particles.

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