Some aspects of bone remodeling around dental implants

Abstract

Considering that success of dental implants is not only related to osseointegration, but also with their survival rates, the aim of this study was to perform a literature review about bone remodeling around osseointegrated implants. A detailed search strategy was used for this, and articles published between the years 1930 and 2012 were selected. The rare data found in the literature demonstrated that implants are osseointegrated 30 days after their placement. However, active bone remodeling with osteoclasts and osteoblasts working in synchrony continues to occur. Therefore, after osseointegration, the initially formed bone, which presents characteristics of spongy bone, is gradually resorbed and replaced by compact bone after 90 days. Furthermore, other portions of bone tissue a little more distant from the interface, which establish direct contact with the implant, are also damaged during the drilling process, and therefore, they also need to be remodeled. Among the rare studies found in the literature about bone remodeling after osseointegration, there were no verified studies on the possible influence of implant surface treatments on bone remodeling that occurs after osseointegration. Only studies involving implants with machined surfaces have been conducted up to now.

Full text

Please
cite
this
article
in
press
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Mello
ASS,
et
al.
Some
aspects
of
bone
remodeling
around
dental
implants.
Rev
Clin
Periodoncia
Implantol
Rehabil
Oral.
2016.
http://dx.doi.org/10.1016/j.piro.2015.12.001
ARTICLE IN PRESS
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Rev
Clin
Periodoncia
Implantol
Rehabil
Oral.
2016;xxx(xx):xxx---xxx
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Revista
Clínica
de
Periodoncia,
Implantología
y
Rehabilitación
Oral
REVIEW
ARTICLE
Some
aspects
of
bone
remodeling
around
dental
implants
Amaro
Sérgio
da
Silva
Melloa,
Pamela
Letícia
dos
Santosb,
Allan
Marquesic,
Thallita
Pereira
Queirozd,
Rogério
Margonard,
Ana
Paula
de
Souza
Falonid,∗
aMaster’s
Degree
in
Implantology,
Implantology
Post-Graduation
Course,
University
Center
of
Araraquara
---
UNIARA,
Araraquara,
São
Paulo,
Brazil
bProfessor
and
Researcher,
Department
of
Oral
Biology
Post
Graduation,
Universidade
do
Sagrado
Corac¸ão,
Bauru,
São
Paulo,
Brazil
cDental
Surgeon,
School
of
Dentistry,
University
Center
of
Araraquara
---
UNIARA,
Araraquara,
São
Paulo,
Brazil
dProfessors
and
Researchers,
Implantology
Post-Graduation
Course,
University
Center
of
Araraquara
---
UNIARA,
Araraquara,
São
Paulo,
Brazil
Received
26
August
2015;
accepted
29
December
2015
KEYWORDS
Dental
implants;
Bone
remodeling;
Osteoclast;
Osteoblast
Abstract
Considering
that
success
of
dental
implants
is
not
only
related
to
osseointegration,
but
also
with
their
survival
rates,
the
aim
of
this
study
was
to
perform
a
literature
review
about
bone
remodeling
around
osseointegrated
implants.
A
detailed
search
strategy
was
used
for
this,
and
articles
published
between
the
years
1930
and
2012
were
selected.
The
rare
data
found
in
the
literature
demonstrated
that
implants
are
osseointegrated
30
days
after
their
placement.
However,
active
bone
remodeling
with
osteoclasts
and
osteoblasts
working
in
synchrony
continues
to
occur.
Therefore,
after
osseointegration,
the
initially
formed
bone,
which
presents
characteristics
of
spongy
bone,
is
gradually
resorbed
and
replaced
by
compact
bone
after
90
days.
Furthermore,
other
portions
of
bone
tissue
a
little
more
distant
from
the
interface,
which
establish
direct
contact
with
the
implant,
are
also
damaged
during
the
drilling
process,
and
therefore,
they
also
need
to
be
remodeled.
Among
the
rare
studies
found
in
the
literature
about
bone
remodeling
after
osseointegration,
there
were
no
verified
studies
on
the
possible
influence
of
implant
surface
treatments
on
bone
remodeling
that
occurs
after
osseointegration.
Only
studies
involving
implants
with
machined
surfaces
have
been
conducted
up
to
now.
©
2016
Sociedad
de
Periodoncia
de
Chile,
Sociedad
de
Implantología
Oral
de
Chile
y
Sociedad
de
Prótesis
y
Rehabilitación
Oral
de
Chile.
Published
by
Elsevier
España,
S.L.U.
This
is
an
open
access
article
under
the
CC
BY-NC-ND
license
(http://creativecommons.org/licenses/
by-nc-nd/4.0/).
∗Corresponding
author.
E-mail
address:
apfaloni@hotmail.com
(A.P.
de
Souza
Faloni).
http://dx.doi.org/10.1016/j.piro.2015.12.001
0718-5391/©
2016
Sociedad
de
Periodoncia
de
Chile,
Sociedad
de
Implantología
Oral
de
Chile
y
Sociedad
de
Prótesis
y
Reha-
bilitación
Oral
de
Chile.
Published
by
Elsevier
España,
S.L.U.
This
is
an
open
access
article
under
the
CC
BY-NC-ND
license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please
cite
this
article
in
press
as:
Mello
ASS,
et
al.
Some
aspects
of
bone
remodeling
around
dental
implants.
Rev
Clin
Periodoncia
Implantol
Rehabil
Oral.
2016.
http://dx.doi.org/10.1016/j.piro.2015.12.001
ARTICLE IN PRESS
+Model
PIRO-84;
No.
of
Pages
9
2
A.S.S.
Mello
et
al.
PALABRAS
CLAVE
Implantes
Dentales;
Remodelación
Ósea;
Osteoclastos;
Osteoblastos
Consideraciones
con
respecto
remodelación
ósea
alrededor
de
los
implantes
dentales
Resumen
Teniendo
en
cuenta
que
el
éxito
de
los
implantes
no
solo
se
asocia
a
su
osteoin-
tegración,
sino
también
a
su
tasa
de
supervivencia,
en
otras
palabras,
a
la
permanencia
de
los
mismos,
en
función,
a
largo
plazo,
el
presente
artículo
tiene
como
objetivo
realizar
una
revisión
bibliográfica
acerca
de
la
remodelación
ósea
alrededor
de
los
implantes
dentales.
Se
utilizó
una
estrategia
de
búsqueda
detallada,
y
se
seleccionaron
los
artículos
publicados
entre
los
a˜
nos
1930
y
2012.
Los
pocos
datos
en
la
literatura
muestran
que
en
las
ratas
los
implantes
osteointegrados
se
presentan
después
de
30
días
de
su
instalación.
Sin
embargo,
una
remod-
elación
ósea
activa
por
los
osteoclastos
y
los
osteoblastos
que
trabajan
sincrónicamente
sigue
ocurriendo,
de
manera
que
después
de
la
osteointegración,
el
hueso
formado
inicialmente,
que
presenta
características
de
hueso
esponjoso,
se
reabsorbe
y
se
sustituye
por
hueso
com-
pacto
después
de
90
días
gradualmente.
Además,
otras
porciones
de
tejido
óseo
un
poco
más
distantes
de
la
interfaz,
que
establecen
contacto
directo
con
el
implante,
también
se
da˜
nan
durante
el
proceso
de
perforación
antes
de
la
implantación,
y
por
lo
tanto,
también
necesitan
ser
remodeladas.
Entre
los
pocos
estudios
en
la
literatura
sobre
el
remodelado
después
de
la
osteointegración
no
hay
estudios
sobre
una
posible
influencia
de
los
tratamientos
de
superficie
del
implante
en
la
remodelación
ósea
que
ocurre
después
de
la
osteointegración.
Hasta
ahora
solo
se
han
realizado
estudios
con
implantes
con
superficies
mecanizadas.
©
2016
Sociedad
de
Periodoncia
de
Chile,
Sociedad
de
Implantología
Oral
de
Chile
y
Sociedad
de
Prótesis
y
Rehabilitación
Oral
de
Chile.
Publicado
por
Elsevier
España,
S.L.U.
Este
es
un
artículo
Open
Access
bajo
la
licencia
CC
BY-NC-ND
(http://creativecommons.org/licenses/
by-nc-nd/4.0/).
Introduction
Bone,
a
type
of
connective
tissue,
presents
cells,
and
in
spite
of
being
mineralized,
it
is
constantly
renewed
by
means
of
the
bone
remodeling
process.
This
process
is
characterized
by
bone
resorption
by
osteoclasts,
followed
by
bone
for-
mation
by
osteoblasts.1Diverse
studies
have
demonstrated
the
relevance
of
bone
remodeling
to
tissue
responses
that
guarantee
osseointegration,2 --- 6 which
is
defined
as
the
direct
structural
and
functional
connection
between
the
organized
vital
bone
and
the
surface
of
a
titanium
implant,
capable
of
receiving
functional
loads.7 --- 9
The
success
of
implants
is
associated
first
with
their
osseointegration,
and
later
on
with
their
survival
rate;
that
is
to
say,
their
long
term
permanence
in
function.
Although
there
are
several
studies
involving
osseointegration
of
dental
and/or
orthopedic
implants,
the
majority
of
the
investigations
have
elucidated
the
tissue
responses
that
con-
stitute
the
initial
process
of
bone-implant
integration.2,10---14
Considering
that
the
remodeling
process
is
continuous,
it
may
be
of
relevance
not
only
to
osseointegration,
but
also
to
the
longevity
of
dental
implants.
Therefore,
the
purpose
of
this
study
was
to
conduct
a
review
of
the
literature
with
a
view
of
elucidating
the
events
associated
with
bone
remod-
eling
after
the
osseointegration
of
implants.
In
addition,
it
was
also
performed
a
search
to
data
with
respect
to
a
pos-
sible
influence
of
treatments
for
modifying
implant
surfaces
on
these
same
events.
Materials
and
methods
In
order
to
conduct
this
literature
review
a
detailed
search
strategy
was
used
in
various
data
bases,
between
the
years
1930
and
2012.
The
following
descriptors
were
used:
‘‘Osseointegrated
Implant’’,
‘‘Bone
remodeling’’,
‘‘Osteoclast’’,
‘‘Osteoblast’’
and
‘‘Surface
treatments’’.
The
inclusion
criteria
were
systematic
review
studies,
meta-
analyses,
conventional
reviews
of
the
literature,
controlled
and
randomized
case
studies,
non-randomized
clinical
cases
and
articles
of
opinion,
with
an
approach
to
the
above-
mentioned
uniterms.
Studies
that
were
not
written
in
the
Portuguese
and
English
languages
were
excluded.
After
crit-
ical
analysis
of
the
bibliography
surveyed,
the
suitable
articles
were
selected.
The
data
obtained
were
carefully
analyzed
and
correlated
for
discussion
of
the
results
pointed
out
in
the
literature.
Literature
review
Considerations
about
bone
tissue
and
the
process
of
bone
remodeling
Bone,
a
connective
tissue,
has
cells,
and
in
spite
of
presenting
the
particularity
of
being
mineralized,
it
is
con-
stantly
renewed
by
means
of
the
bone
remodeling
process.1
In
clinical
terms,
the
rate
of
bone
remodeling,
also
denomi-
nated
bone
turnover,
is
the
period
necessary
for
new
bone
to
replace
the
existent
bone,
guaranteeing
adaptation
of
the
neoformed
bone
to
its
microenvironment.15 Microscopically,
bone
remodeling
consist
in
bone
resorption
by
osteoclasts,
followed
by
bone
formation
by
osteoblasts16,17 (Fig.
1).
Both
cells
may
be
characterized
by
morphological
and
biochem-
ical
aspects.
Osteoclasts,
formed
by
the
fusion
of
mononu-
cleated
cells
of
the
hematopoietic
lineage,18,19 are
mult-
inucleated
giant
cells
that
degrade
the
mineralized
bone
matrix.
They
are
located
in
excavation
on
the
bone
surface,

Please
cite
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Mello
ASS,
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Some
aspects
of
bone
remodeling
around
dental
implants.
Rev
Clin
Periodoncia
Implantol
Rehabil
Oral.
2016.
http://dx.doi.org/10.1016/j.piro.2015.12.001
ARTICLE IN PRESS
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Some
aspects
of
bone
remodeling
around
dental
implants
3
Oc
B
Ob
BB
Oc
nOt
BM
A
B
C
100 μm
90 μm
Ob
Ot
Figure
1
Light
micrographs
of
portions
of
tibiae
which
were
surrounding
the
implants.
(1A)
Several
bone
trabeculae
(B)
and
bone
marrow
regions
(BM)
are
observed.
Osteoblasts
(Ob)
and
osteoclasts
(Oc)
are
located
on
bone
surface,
whereas
osteocytes
(Ot)
are
located
inside
the
bone
matrix
(B).
H&E.
Bar:
100
␮m.
(1B)
Osteoblasts
(Ob),
located
on
bone
surface
(B),
show
alcaline
phosphate
(ALP)-positive
cytoplasm
(brown-yellow
color).
Immunohistochemistry
for
detection
of
ALP
(osteoblast
marker)
counterstained
with
Hematoxylin.
Bar:
30
␮m.
(1C)
Giant
multinucleated
osteoclasts
(Oc)
exhibiting
intense
TRAP-positivity
in
the
cytoplasm
(brown
color)
are
observed.
n:
nuclei.
Ot:
osteocytes.
Arrowheads:
Howship
lacunae.
Immunohistochemistry
for
detection
of
TRAP
(osteoclast
marker)
counterstained
with
Hematoxylin.
Bar:
90
␮m.
denominated
Howship
lacunae.16,20,21 In
their
cytoplasm,
osteoclasts
present
the
enzyme
acid
phosphatase,
which
may
be
distinguished
from
the
other
isoenzymes
because
it
is
resistant
to
inhibition
by
tartaric
acid,
thus
denominated
tartrate
resistant
acid
phosphatase
(TRAP).4,29 In
addition
to
TRAP,
the
osteoclasts
also
synthesize
other
enzymes,
such
as
metalloproteinase-9
(MMP-9)
and
cathepsin
K.22
On
the
other
hand,
the
osteoblasts,
cells
originating
from
precursors
of
mesenchymal
origin,
are
mononucleated,
smaller
in
size
than
osteoclasts
and
related
to
the
produc-
tion
and
mineralization
of
bone
tissue
matrix.
They
are
disposed
in
a
continuous
layer
on
the
surface
of
the
bone
matrix.
Osteoblasts
and
pre-osteoblasts
exhibit
high
lev-
els
of
alkaline
phosphatase
enzyme
(ALP)
on
the
surface
of
their
cytoplasmic
membranes
which,
when
released,
con-
tribute
to
the
initiation
of
mineralization
and
progressive
growth
of
hydroxyapatite
crystals.
In
the
initial
process
of
bone
tissue
formation,
after
the
osteoblasts
have
secreted
the
first
layer
of
organic
matrix,
they
appear
to
assume
an
important
role
in
its
mineralization.
From
the
osteoblasts
adjacent
to
the
recently
synthesized
organic
bone
matrix,
small
vesicles
emerge.
ALP
belongs
to
a
family
of
enzymes
that
hydrolyze
phosphate
ions,
supplying
them
to
the
inte-
rior
of
the
vesicles.
An
increase
in
the
concentration
of
calcium
ions
inside
these
vesicles
also
occurs,
probably
through
the
phospholipids
in
their
membranes.
Thus
a
super-
saturation
of
phosphate
and
calcium
occurs,
resulting
in
the
precipitation
of
phosphate
and
calcium
inside
the
vesicles.

Please
cite
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article
in
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Mello
ASS,
et
al.
Some
aspects
of
bone
remodeling
around
dental
implants.
Rev
Clin
Periodoncia
Implantol
Rehabil
Oral.
2016.
http://dx.doi.org/10.1016/j.piro.2015.12.001
ARTICLE IN PRESS
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A.S.S.
Mello
et
al.
Afterwards,
there
is
vesicle
membranes
rupture
and
min-
eralization
spreads
throughout
the
matrix.
This
process
is
characteristic
of
the
sites
in
which
bone
tissue
formation
and
mineralization
is
occurring.
Thus,
ALP
contributes
to
the
beginning
of
mineralization
and
progressive
growth
of
hydroxyapatite
crystals
of
bone
matrix.21,23 In
this
context
of
tissue
renewal,
the
periosteum
may
be
included,
because
it
is
an
important
source
of
osteogenic
cells.
It
is
made
up
of
two
layers:
An
external
layer
of
fibrous
conjunctive
tissue,
in
which
there
are
few
cells
and
vessels,
and
an
internal
layer,
that
has
osteoprogenitor
mesenchymal
stem
cells,
and
a
vast
network
of
blood
vessels
in
direct
contact
with
the
bone.2,24
As
bone
matrix
is
produced,
some
osteoblasts
become
trapped
within
its
lacunae,
and
begin
to
exhibit
cytoplas-
mic
extensions,
which
are
found
inside
the
bone
canaliculi.
These
extensions
go
toward
to
the
extensions
of
adja-
cent
osteocytes,
and
in
the
direction
of
other
cells.
Then,
gap
juctions
which
allow
intercellular
communications
are
established
between
osteocytes/osteocytes
and
osteo-
cytes/other
bone
cells.
The
junctional
communications
enable
even
the
osteocytes
located
in
the
deepest
regions
of
bone
to
respond
to
systemic
changes,
and
modifications
on
the
bone
surface.
Therefore,
osteocytes
constitute
a
com-
plex
network
that
interconnects
the
bone
surface
with
the
most
internal
portions,
and
are
responsible
for
the
main-
tenance
and
vitality
of
the
bone
matrix.21,23 In
addition,
the
osteocytes
are
considered
essential
for
bone
remodel-
ing,
and
it
has
been
demonstrated
that
apoptosis
of
this
cell
appears
to
stimulate
the
resorptive
activity
of
osteo-
clasts.25 Osteoclasts
be
responsible
for
the
phagocytosis
of
these
osteocytes,
thereby
avoid
triggering
an
inflammatory
process
within
bone
tissue.26---28
Osseointegration
and
bone
remodeling
around
osseointegrated
implants
In
the
1960s,
the
Swedish
orthopedist
Branemark
and
his
col-
laborators
discovered,
by
chance,
the
occurrence
of
bone
integration
with
titanium,
denominated
osseointegration.
Thus,
osseointegration
consists
of
the
clinically
asymp-
tomatic,
rigid
fixation
of
alloplastic
materials,
maintained
during
functional
loads.7
In
rats,
osseointegration
is
acquired
around
1
month
after
implants
placement,3and
is
characterized
by
the
cover-
age
of
the
implant
threads
by
the
adjacent
bone
tissue,
in
addition
to
the
presence
of
insignificant
inflammation
and
absence
of
fibrous
tissue.3,5,12 A
suitable
model
for
this
type
of
study
was
introduced
in
1998,
using
the
rat
maxilla
for
observation
of
the
tissues
responsible
for
tita-
nium
implantation
from
1
to
30
days
after
insertion
of
the
implant.
In
this
study,
it
was
observed
that
the
appear-
ance
of
neoformed
bone
tissue
occurred
on
the
fifth
day
after
implant
placement,
and
covered
the
entire
implant
30
days
after
osseointegration.
However,
concomitant
with
osseointegration,
damaged
bone
was
observed,
exhibiting
lacunae
of
empty
osteocytes,
or
osteocytes
with
a
picnotic
appearance
between
the
pre-existent
and
neoformed
bone
around
the
implants.3,5,12 Considering
that
the
remodeling
process
is
continuous,
it
may
be
of
relevance
with
respect
not
only
to
osseointegration,
but
also
to
the
longevity
of
dental
implants,
the
purpose
of
this
study
was
to
conduct
a
review
of
the
literature
with
a
view
to
elucidating
the
events
associated
with
bone
remodeling
after
the
osseoin-
tegration
of
implants.
In
addition,
it
was
performed
a
search
to
investigate
the
existence
of
data
with
respect
to
a
possi-
ble
influence
of
treatments
for
modifying
implant
surfaces
on
these
same
events.
A
long
term
study
investigating
the
response
to
bone
tissue
present
around
titanium
implants
that
had
become
osseointegrated
in
rats,
was
conducted
by
Haga
et
al.29 These
authors
showed
by
means
of
active
bone
remodeling,
with
osteoclasts
and
osteoblasts
working
in
synchrony,
the
bone
initially
formed
around
the
implant,
which
presents
characteristics
of
spongy
bone,
is
gradually
resorbed
until
it
disappears
at
the
end
of
90
days,
when
it
is
completely
replaced
by
compact
bone.
The
morpholog-
ical
and
biochemical
alterations
associated
with
the
bone
remodeling
process,
which
occur
around
machined
implants
from
1
to
3.5
months
after
osseointegration
are
illustrated
in
Fig.
2.29
One
month
after
implant
placement
Osseointegration
is
observed
in
all
the
surfaces
of
the
implants.3,29 There
is
a
thin
layer
of
neoformed
bone
present
on
the
implant
surface.
However,
a
part
of
this
surface
is
shown
not
to
be
in
contact
with
the
neoformed
bone.
In
these
areas,
medullary
spaces
containing
small
blood
capillaries
are
shown
to
be
in
contact
with
the
implant
surface.
The
neoformed
bone
contains
osteocytic
lacunae
exhibiting
intact
osteocytes.
In
the
region
of
pre-existent
bone,
a
cement
line
is
easily
identified
beyond
the
empty
osteocytic
lacunae.
The
double
markings
of
TRAP
and
ALP
enzymes
for
the
detection
of
osteoclasts
and
osteoblasts,
respectively,
show
positivity
for
both
cells
on
the
neoformed
bone
surface.
ALP-positive
osteoblasts
are
found
close
to
the
area
occupied
by
TRAP-positive
osteoclasts,
suggesting
the
occurrence
of
synchrony
and
equivalence
of
the
activity
of
these
cells,
and
therefore,
of
bone
remodeling.29
From
1.5
to
2.5
months
after
the
placement
of
implants
The
formation
of
bone
tissue
proceeds
in
the
direction
of
the
damaged
bone
containing
empty
osteocytic
lacunae,
resulting
in
a
reduction
in
it.
Practically
the
entire
implant
surface
is
covered
by
neoformed
bone.
The
portion
of
neo-
formed
bone
exhibits
characteristics
of
spongy
bone.
Some
empty
osteocytic
lacunae
remain,
however,
the
area
con-
taining
this
type
of
structure
is
shown
to
be
smaller.
There
is
the
presence
of
an
evident
cementing
line
between
the
pre-existent
bone
(containing
empty
osteocytic
lacunae)
and
the
neoformed
bone.
A
lower
number
of
ALP-positive
osteoblasts
and
TRAP-positive
osteoclasts
are
observed.
In
addition,
both
cell
types
present
reduced
volumes,
suggest-
ing
less
cell
activity.29
Three
months
after
implant
placement
There
is
the
absence
of
empty
osteocytic
lacunae.
The
area
of
pre-existent
bone
has
been
replaced
by
neo-
formed
bone
containing
intact
osteocytes.
The
neoformed
bone
presents
the
morphological
characteristics
of
compact
bone.
There
are
only
some
capillaries
found
between
the
implant
and
neoformed
bone.
ALP-positive
osteoblasts
and
TRAP-positive
osteoclasts
are
rarely
observed
around
the
implants,
except
in
the
bone
marrow
regions.

Please
cite
this
article
in
press
as:
Mello
ASS,
et
al.
Some
aspects
of
bone
remodeling
around
dental
implants.
Rev
Clin
Periodoncia
Implantol
Rehabil
Oral.
2016.
http://dx.doi.org/10.1016/j.piro.2015.12.001
ARTICLE IN PRESS
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No.
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Pages
9
Some
aspects
of
bone
remodeling
around
dental
implants
5
A
D
B
E
C
F
Figure
2
Light
micrographs
showing
morphological
changes
in
the
surrounding
bone
around
implants
at
1,
2
and
3
months
after
osseointegration
(2A---2C).
Bar:
100
␮m.
The
schematic
representation
of
each
light
micrograph
summarizes
the
main
histological
events
in
the
replacement
of
the
injured
bone
by
newly
formed
bone
(2D---2F).
(2A,
2D):
One
month
(30
days)
after
implant
osseointegration,
woven
bone
and
bone
marrow
regions
(BM)
are
observed
in
the
light
micrograph.
Many
osteoblasts
(Ob)
and
osteoclasts
(Oc)
are
located
on
bone
surface.
It
can
be
found
many
regions
of
newly
formed
bone
(NB),
which
are
represented
in
pink
color
in
the
scheme.
Inside
the
bone
matrix,
several
osteocytes
(Ot)
are
observed.
However,
empty
osteocytes
lacunae
are
still
observed
(white
color),
mainly
in
the
regions
of
damaged
bone
(DB),
in
yellow
color.
(2B,
2E):
Two
months
(60
days)
post-
osseointegration,
the
woven
bone
seems
to
reduce
in
volume
when
compared
with
1-month
period.
Moreover,
the
woven
bone
previously
in
contact
with
the
implant
is
being
replaced
by
cortical.
In
the
period
comprised
between
3
and
3.5
months
after
acquisition
of
osseointegration,
minimal
morphological
and
biochemical
changes
are
related,
such
as
for
exam-
ple,
a
slight
increase
in
neoformed
bone
thickness
(with
its
corticalization
proceeding
for
up
to
12
months
after
osseoin-
tegration).
The
distribution
and
density
of
ALP-positive
osteoblasts
and
TRAP-positive
osteoclasts,
and
the
distance
between
the
cementing
lines
are
identical
to
those
observed
in
the
period
of
3
months
after
implant
placement.
Once
again
it
is
important
to
emphasize
that
the
neoformed
bone
under-
goes
gradual
changes
from
spongy
to
compact
bone
due
to
its
continuous
remodeling.
However,
it
exhibits
the
same
biological
properties
as
intact
bone
after
osseointegration
is
acquired.29
Implant
surface
treatments
and
bone
remodeling
after
acquisition
of
osseointegration
Commercially
pure
titanium
(cpTi),
biocompatible
mate-
rial,
shows
no
biological
properties
of
osteoinduction
or
osteogenesis.
For
this
reason,
various
surface
treatments
of
titanium
implants
have
been
proposed,
and
carefully

Please
cite
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article
in
press
as:
Mello
ASS,
et
al.
Some
aspects
of
bone
remodeling
around
dental
implants.
Rev
Clin
Periodoncia
Implantol
Rehabil
Oral.
2016.
http://dx.doi.org/10.1016/j.piro.2015.12.001
ARTICLE IN PRESS
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No.
of
Pages
9
6
A.S.S.
Mello
et
al.
investigated.
These
studies
have
allowed
one
to
observe
that
the
process
of
osseointegration
is
favored
by
surface
treatments,
both
in
terms
of
duration
of
the
events
asso-
ciated
with
complete
osseointegration
and
in
situation
of
unfavorable
bone
quantity
and
quality.30,47 The
biological
logic
of
these
treatments
is
to
make
this
microenvironment
as
similar
as
possible
to
the
bone
microenvironment,
making
the
implant
surface
mimic
the
morphology
and
composition
of
the
constituents
of
bone
tissue
itself.30,31,47
The
process
of
changing
the
cpTi
surface
may
be
per-
formed
by
the
techniques
of
subtraction,
particle
adhesion
or
by
association
of
both.31
The
treatments
of
subtraction
consist
of
removal
of
por-
tions
of
the
implant
surface.
An
example
of
subtraction
treatment
is
irradiation
of
the
implant
surface
with
a
LASER
beam.
This
process
results
in
an
increase
in
resistance
to
corrosion
and
biocompatibility
of
titanium,
due
to
its
oxi-
dation
and
subsequent
formation
of
oxides
and
nitrides.32
Moreover,
irradiation
with
LASER
joins
advantages
char-
acteristics,
such
as
non-contamination
of
the
surface
and
a
high
degree
of
reproducibility
of
this
technique,
which
produces
a
complex
and
homogeneous
surface
morphology,
with
a
high
degree
of
purity,
thus
favoring
osseointegra-
tion
and
increasing
the
removal
torque.30,32---34 In
addition
to
these
techniques,
treatments
with
acids
either
associ-
ated
with
airborne
particle
abrasion
with
titanium
oxide
---
TiO2or
aluminum
oxide
---
Al2O3,35 or
not,
are
also
forms
of
subtraction
techniques.
As
opposed
to
subtraction
treatments,
addition
treat-
ments
consist
of
the
addition
of
substances
to
the
implant
surface,
such
as,
for
example,
the
incorporation
of
ceramics
such
as
hydroxyapatite
(HA)
[Ca10(PO4)6(OH)2].36 It
has
been
shown
that
coating
implant
surfaces
with
calcium
phosphate
accelerates
osseointegration,
especially
under
conditions
of
a
limited
quantity
and
quality
of
bone
tissue.37,38 This
may
be
owing
to
the
fact
that
HA
helps
to
establish
an
early
chemical
bond,
and
consequently,
a
strong
physical
chemical
interac-
tion
with
bone
in
the
initial
stages
of
osseointegration.
On
the
implant
surface,
a
layer
of
apatite
hydroxycarbonate
is
formed,
which
is
chemically
and
structurally
equivalent
to
the
mineral
phase
of
bone,
thus
a
biochemical
bond
occurs
between
the
implant
surface
and
bone
by
means
of
bone
matrix
deposition
on
the
HA
surface.
This
physical
chemi-
cal
interaction
between
the
collagen
of
bone
and
HA
of
the
implant
is
denominated
biointegration.
Moreover,
greater
bone
tissue
formation
is
observed
around
implants
coated
with
HA,
than
in
cpTi
implants.39
When
materials
such
as
HA,
considered
bioactive,
are
in
contact
with
the
live
tissue,
they
undergo
superficial
dissolution
induced
by
cell
activity,
releasing
calcium
and
phosphorous
ions
into
the
extracellular
medium.
These
ions
are
incorporated
into
the
microcrystals
of
HA
of
the
bone;
that
is
to
say,
bone
matrix
is
deposited
on
the
HA
surface,
leading
to
biointegration.40 Furthermore,
HA
is
commonly
used
for
coating
metal
implants,
due
to
the
mechanical
advantages
of
metals
added
to
the
excellent
biocompat-
ibility
and
bioactivity
of
HA.
This
association
(cpTi
and
HA)
provides
an
increase
in
the
strength
of
the
interface
with
bone
tissue.30,41-43 Methods
of
chemical
deposition
of
HA
have
been
studied
to
improve
the
bond
of
the
coating
to
the
implant
surface.
Among
these,
there
is
empha-
sis
on
the
biomimetic
method,
which
mimics
the
body’s
biological
process
of
hard
tissue
formation
and
consists
of
immersion
of
the
substrate
to
be
coated
in
a
synthetic
solution
denominated
simulated
body
fluid
solution
(SBF)36
and
was
performed
by
Queiroz
et
al.30 SBF
has
chemi-
cal
composition,
temperature
and
pH
that
simulate
blood
plasma.
The
implant
surface
treatment
methods
may
also
be
clas-
sified
according
to
the
topographic
characteristics
they
give
implants.
Implant
surface
topography
varies
according
to
the
method
by
which
it
is
obtained;
that
is
to
say,
by
means
of
macro,
micro
or
nanotechnology.14,30,34,44
By
means
of
implant
surface
treatments
greater
implant
surface
roughness
may
be
obtained.
Roughness
represents
a
micro
or
nanomorphological
structural
modification
that
provides
an
increase
in
the
area
of
contact
between
the
bone
and
implant.6One
is
able
to
distinguish
between
macroroughness
(100
␮m
to
millimeters),
microroughness
(100
nm---100
␮m)
e
nanoroughness
(less
than
100
nm).31
Each
type
of
topography
has
a
specific
influence
on
the
mechanisms
involved
in
osseointegration.
For
example,
accumulation
and
organization
of
the
blood
clot
on
the
rough
surface,
create
an
important
physical
phenomenon
for
osteogenesis,
such
as
greater
adhesion,
proliferation
and
expression
of
osteoblast
differentiation
markers.
This
leads
to
an
increase
in
the
bone-implant
bond
strength,
and
consequently,
to
success
of
therapy
with
implants
in
the
long
term.45---47 Clinical
proof
of
the
positive
influ-
ence
of
surface
treatments
on
osseointegration
is
the
higher
torque
required
for
removal
of
implants
with
rough
surfaces,
when
compared
with
those
that
have
smooth
surfaces.11,48
cpTi
implants
modified
on
a
nanometric
scale
by
LASER
beam
with
HA
deposition
by
the
biomimetic
method,
with
and
without
afterwards
receiving
heat
treatment
in
an
oven
at
600 ◦C,
favor
osseointegration
in
the
periods
of
evaluation
of
30
and
60
days
after
implant
place-
ment
in
rabbit
tibias.
Moreover,
the
surface
containing
HA
that
did
not
undergo
heat
treatment
presented
greater
biological
activity,
reducing
the
time
of
osseointegra-
tion.
This
latter
result
is
probably
associated
with
the
lower
degree
of
crystallinity
of
hydroxyapatite,
which
therefore
becomes
more
soluble
and
similar
to
biological
hydroxyapatite.30
In
general,
the
goal
of
surface
treatments
is
to
reduce
the
time
of
loading
after
surgery;
accelerate
bone
growth
and
maturation
to
allow
immediate
loading;
increase
pri-
mary
stability;
guarantee
the
success
of
implants
when
they
are
placed
in
regions
that
present
bone
with
lower
quality
and
quantity;
obtain
bone
growth
directly
on
the
implant
surface;
obtain
the
largest
possible
area
of
osseointegration;
obtain
bone-implant
contact
with-
out
the
interposition
of
amorphous
protein
layers;
attract
mesenchymal,
pre-osteoblastic
and
osteoblastic
cells,
in
addition
to
proteins
with
specific
binding
to
osteogenic
cells.9,44,49,50
The
success
of
osseointegration,
and
the
maintenance
of
implants
in
the
long
term
is
dependent
on
adequate
rates
of
bone
remodeling.44,51 However,
up
to
the
present
time,
we
have
not
found
any
studies
in
the
literature,
which
investigate
a
possible
differential
effect
of
these
surface
treatments
of
implants
on
the
bone
remodeling
that
occurs
after
the
establishment
of
osseointegration.

Please
cite
this
article
in
press
as:
Mello
ASS,
et
al.
Some
aspects
of
bone
remodeling
around
dental
implants.
Rev
Clin
Periodoncia
Implantol
Rehabil
Oral.
2016.
http://dx.doi.org/10.1016/j.piro.2015.12.001
ARTICLE IN PRESS
+Model
PIRO-84;
No.
of
Pages
9
Some
aspects
of
bone
remodeling
around
dental
implants
7
Discussion
Osseointegration
is
described
as
an
effective
interaction
between
bone
tissue
and
the
implant
surface.7 --- 9 How-
ever,
damaged
bone
tissue,
with
empty
osteocytic
lacunae,
resulting
from
cutting
of
the
bone
for
implant
placement,
remains
in
the
microenvironment
around
the
implant,
even
after
its
osseointegration.29 In
the
literature,
studies
with
respect
to
bone
remodeling
around
implants
that
have
already
become
osseointegrated
are
rare.
Of
the
articles
selected
for
this
review,
only
one
study
directly
analyzed
the
events
involving
renewal
of
bone
tissue
in
the
microen-
vironment
around
the
implant
after
osseointegration,
in
the
absence
of
loads,
in
an
animal
model
(rats).29 This
study
was
conducted
on
the
basis
of
the
results
obtained
by
Fuji
et
al.3
who
demonstrated
that
this
type
of
investigation
could
be
conducted
in
animal
models
(rats)
30
days
after
the
place-
ment
of
a
conventional
implant
with
a
machined
surface,
which
was
shown
to
be
almost
completely
covered
by
bone
tissue.
Haga
et
al.29 observed
that
one
month
after
osseoin-
tegration,
there
was
still
bone
tissue
around
the
implant,
presenting
empty
or
picnotic
osteocytic
lacunae.
By
means
of
balanced
bone
remodeling,
in
which
bone
resorption
by
TRAP-positive
osteoclasts
and
bone
neoformation
by
ALP-positive
osteoblasts
are
synchronic
and
equivalent,
the
damaged
bone
is
remodeled
in
a
gradual
manner
and
dis-
appears
completely
3
months
after
implantation.
Initially,
there
is
replacement
of
the
pre-existent
bone,
damaged
by
cutting,52 by
spongy
bone,
and
of
this,
by
compact
bone,
thus
improving
the
bone
quality.29 These
data
clearly
demonstrated
that
continual
bone
remodeling,
even
after
osseointegration
is
essential
for
the
survival
and
success
of
dental
implants
in
the
long
term.
It
is
important
to
emphasize
that
the
studies
investi-
gating
events
associated
with
bone
remodeling
after
the
acquisition
of
osseointegration,
mentioned
in
this
review
of
the
literature,
were
conducted
in
the
absence
of
loads.29
In
the
presence
of
loading
and
depending
on
the
value
of
the
load
applied,
modifications
occur
in
the
bone
tissue
located
around
the
implant,
which
must
have
its
structure
adequately
adapted
to
receive
the
forces
applied.53 Fur-
thermore
it
requires
continuous
remodeling
to
replace
the
regions
damaged
by
fatigue,
in
order
to
prevent
the
occur-
rence
of
fractures
and
loss
of
the
implant.4,6,54 Therefore,
there
are
higher
bone
remodeling
rates
in
implants
submit-
ted
to
the
action
of
loads.6
In
spite
of
the
large
number
of
studies
on
the
topo-
graphical,
physical
and
chemical
changes
on
implant
surfaces,14,30,34 up
to
the
present
time,
we
have
found
no
articles
in
the
literature,
which
have
investigated
a
possi-
ble
differential
effect
of
these
surface
treatments
on
the
bone
remodeling
that
occurs
after
osseointegration
has
been
established.
Conclusions
It
is
reasonable
to
suggest,
for
example,
that
bioactive
sur-
faces
may
continue
to
be
active
in
the
long
term,
stimulating
the
bone
cells
and
leading
to
a
higher
degree
of
tissue
turnover.
On
the
other
hand,
it
is
also
possible
that
the
properties
obtained
by
means
of
the
surface
treatments
may
influence
osseointegration
only,
seeing
that
at
this
time
the
bone
cells
have
greater
access
to
the
treated
surface.
Source
of
funding
None
declared.
Conflict
of
interest
No
conflicts
of
interest
have
been
declared.
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