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Chorion and amnion/chorion membranes in oral and periodontal surgery: A systematic review

Article

Chorion and amnion/chorion membranes in oral and periodontal surgery: A systematic review

Abstract and Figures

The aim of this study was to perform a systematic review on the clinical applications where chorion membrane (CM) and amnion/chorion membrane (ACM) were used for oral tissue regeneration procedures. Selection of articles was carried out by two evaluators in Pubmed and Scopus databases, and Outcomes (PICO) method was used to select the relevant articles. Clinical studies reporting the use of CM or ACM for oral soft and hard tissue regeneration were included. The research involved 21 studies conducted on 375 human patients. Seven clinical applications of CM and ACM in oral and periodontal surgery were identified: gingival recession treatment, intrabony and furcation defect treatment, alveolar ridge preservation, keratinized gum width augmentation around dental implants, maxillary sinus membrane repair, and large bone defect reconstruction. CM and ACM were compared to negative controls (conventional surgeries without membrane) or to the following materials: collagen membranes, dense polytetrafluoroethylene membranes, platelet‐rich fibrin membranes, amnion membranes, and to a bone substitute. Several studies support the use of CM and ACM as an efficient alternative to current techniques for periodontal and oral soft tissue regeneration procedures. However, further studies are necessary to increase the level of evidence and especially to demonstrate their role for bone regeneration.
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REVIEW
ARTICLE
Chorion
and
amnion/chorion
membranes
in
oral
and
surgery:
A
systematic
review
Sarah
Gulameabasse
1
|
Florelle
Gindraux
2,3
|
Sylvain
Catros
1,4
|
Jean-Christophe
Fricain
1,4
|
Mathilde
Fenelon
1,4
1
Département
de
chirurgie
orale,
UFR
d'Odontologie,,
Université
de
Bordeaux,
46
rue
Léo-Saignat,
Bordeaux,
France
2
Laboratoire
de
Nanomédecine,
Imagerie,
Thérapeutique
EA
4662,
Université
Bourgogne
Franche-Comté,
Besançon,
France
3
Service
de
Chirurgie
Orthopédique,
Traumatologique
et
Plastique,
CHU
Besançon,
Besançon,
France
4
Univ.
Bordeaux,
INSERM,
BIOTIS,
U1026,
Bordeaux,
France
Correspondence
Mathilde
Fenelon,
Department
of
Oral
Surgery,
CHU
Bordeaux,
33076
Bordeaux,
France.
Email:
mathilde.fenelon@u-bordeaux.fr
Abstract
The
aim
of
this
study
was
to
perform
a
systematic
review
on
the
clinical
applications
where
chorion
membrane
(CM)
and
amnion/chorion
membrane
(ACM)
were
used
for
oral
tissue
regeneration
procedures.
Selection
of
articles
was
carried
out
by
two
eval-
uators
in
Pubmed
and
Scopus
databases,
and
Outcomes
(PICO)
method
was
used
to
select
the
relevant
articles.
Clinical
studies
reporting
the
use
of
CM
or
ACM
for
oral
soft
and
hard
tissue
regeneration
were
included.
The
research
involved
21
studies
conducted
on
375
human
patients.
Seven
clinical
applications
of
CM
and
ACM
in
oral
and
periodontal
surgery
were
identified:
gingival
recession
treatment,
intrabony
and
furcation
defect
treatment,
alveolar
ridge
preservation,
keratinized
gum
width
aug-
mentation
around
dental
implants,
maxillary
sinus
membrane
repair,
and
large
bone
defect
reconstruction.
CM
and
ACM
were
compared
to
negative
controls
(conven-
tional
surgeries
without
membrane)
or
to
the
following
materials:
collagen
mem-
branes,
dense
polytetrafluoroethylene
membranes,
platelet-rich
fibrin
membranes,
amnion
membranes,
and
to
a
bone
substitute.
Several
studies
support
the
use
of
CM
and
ACM
as
an
efficient
alternative
to
current
techniques
for
periodontal
and
oral
soft
tissue
regeneration
procedures.
However,
further
studies
are
necessary
to
increase
the
level
of
evidence
and
especially
to
demonstrate
their
role
for
bone
regeneration.
KEYWORDS
amniochorion,
chorion,
fetal
membrane,
guided
bone
regeneration,
guided
tissue
regeneration,
oral
surgery,
periodontal
surgery
1
|
INTRODUC
TION
The
h
uman
placen
ta
is
compos ed
of
two
membran
es:
the
amni
otic
membrane,
which
is
in
contact
with
the
fetus
and
the
outer
chorionic
membrane
(CM).
One
of
the
main
properties
of
these
fetal
mem-
branes
is
their
elastic
strength
that
allows
the
amniotic
cavity
to
be
maintained
in
the
uterus
during
f etal
growth.
In
addition,
they
secr
ete
an
ti-
infl
amm
ator
y
cyt
okin
es,
c
hemo
kin
es,
an
d
gr
owth
fac-
tors
su
ch
as
Plat
elet
-Der
ive
d
G
row
th
Fact
or
AA
(PDG
F-AA
)
an
d
Vas
-
cular
end
othe l
ial
growt
h
fac
tor
(VEGF)
.
1,2
Amni
otic
m
embr
ane
s
and
CM
exer
t
anti
-inf
lam
mator
y,
3,4
angi
ogen
ic,
5-7
anti
fib
roti
c,
8,9
and
anti m
icr
obia
l
eff
ects.
10,11
They
a
lso
pos
sess
low
imm
uno
geni
cit
y
and
impr
ove
epi
the
lia li
zat
ion
.
8,12,13
The
pl
acen
ta
is
a
si
mple
so
urc
e
of
biol
ogica
l
memb r
anes
wi
thout
maj
or
rest
rict
ion
s
a
s
it
i
s
co
nsi
dere
d
a
biol
ogica
l
w
ast e.
Wi
th
an
esti
mate
d
bi
rth
rat
e
( an
nual
n
umbe r
of
births/total
population)
of
18.3
worldwide
in
2019,
this
is
a
readily
avail
abl
e
b
iom
ater
ial.
14
These
fetal
membranes
have
been
used
in
medicine
since
the
1910s
for
skin
wound
care
and
ophthalmology.
15-19
Today
clinical
applications
have
expanded
20
:
they
can
be
used
in
dermatology
21
or
plastic
surgery
22
as
a
skin
substitute
to
treat
burns,
23,24
diabetic
foot
ulcers,
25,26
or
venous
leg
ulcers.
27,28
These
membranes
are
also
used
Received:
31
August
2020
Revised:
13
November
2020
Accepted:
8
December
2020
DOI:
10.1002/jbm.b.
34783
J
Biomed
Mater
Res.
2020;1
14.
wileyonlinelibrary.com/journa
l/jbmb
©
2020
Wiley
Periodicals
LLC
1
Printed by [Universite de Bordeaux Service Facturier - 193.050.102.025 - /doi/epdf/10.1002/jbm.b.34783] at [28/12/2020].
in
orthopedic
surgery,
in
particular
for
repairing
tendons
and
liga-
ments,
to
treat
joints
and
cartilage
diseases
or
prevent
scars
forma-
tion.
29,30
They
are
used
in
gynecology
31
and
urology.
32,33
Fetal
membrane
and
their
derivates
are
also
considered
as
attractive
biolog-
ical
scaffolds
for
tissue
engineering.
34-36
There
is
also
a
growing
interest
in
the
use
of
placental
membranes
allografts
as
an
alternative
to
conventional
membranes
in
oral
sur-
gery.
37-39
Indeed,
both
absorbable
and
nonabsorbable
membranes
currently
used
to
regenerate
oral
soft
and
hard
tissues
have
some
limi-
tations.
40,41
Nonresorbable
membranes
have
often
been
associated
with
oral
exposure
through
the
soft
tissue
and
a
second
surgical
inter-
vention
is
always
needed
for
membrane
removal.
Resorbable
mem-
branes
have
low-mechanical
strength
and
their
degradation
can
induce
a
strong
inflammatory
response
during
the
post-operative
healing
phase.
They
also
lack
biological
properties,
thereby
justifying
search
for
alternatives.
42
Placental
membranes
are
thus
promising
bio-
active
membranes
for
oral
guided
tissue
regeneration.
43-46
We
previ-
ously
investigated
the
usefulness
of
amniotic
membrane
in
the
field
of
oral
surgery:
periodontal
surgery,
prosthodontics
and
peri-implant
sur-
gery,
cleft
palate
surgery,
and
tumoral
reconstruction
were
identified
as
the
main
clinical
indications.
47
Another
study
investigated
the
dif-
ferent
properties
of
the
amnion
and
CM
and
their
potential
uses
in
periodontology.
Fourteen
clinical
applications
were
identified.
Most
of
them
used
the
amnion
alone,
whereas
only
three
studies
used
the
CM
or
the
CM
in
combination
with
the
amnion
(ACM).
12
However,
the
amniotic
membrane
is
thin
which
makes
its
manipulation
difficult.
To
overcome
this
limitation,
the
use
of
CM,
which
is
four
to
five
times
thicker
than
amnion,
or
the
CM
in
conjunction
with
amnion
(ACM)
could
be
an
interesting
alternative.
Besides,
the
antibacte
rial
effects
of
the
chorion
are
superior
to
those
of
the
amnion;
it
plays
a
key
role
in
protecting
the
fetus
from
infection.
48
The
CM
or
ACM
contain
four
to
five
times
more
growth
factors
and
cytokines
than
the
equal
sur-
face
area
amnion,
49
thereby
further
promoting
wound
healing.
1
The
mechanical
and
biological
properties
of
CM
and
ACM
thus
provide
new
biological
membrane
options
in
oral
and
periodontal
sur-
gery.
However,
there
is
no
study
that
summarizes
CM
and
ACM
clini-
cal
applications
and
their
efficacy
to
regenerate
oral
soft
and
hard
tissues.
The
purpose
of
this
study
was
thus
to
perform
a
systematic
review
on
the
clinical
use
of
CM
and
ACM
in
oral
and
periodontal
surgery.
2
|
MATERIALS
AND
METHODS
This
review
was
performed
according
to
the
preferred
reporting
items
for
systematic
reviews
and
meta-analyses
(PRISMA),
50
and
has
been
registered
in
PROSPERO
database
(N
CRD42020187215).
2.1
Focused
question
|
The
search
strategy
was
developed
based
on
the
PICO
reporting
sys-
tem.
The
following
focused
question
was
defined:
In
which
clinical
indications
have
chorion
and
amnion/chorion
membranes
(ACM)
been
shown
effective
for
soft
or
hard
tissues
repair
in
the
field
of
oral
surgery?
2.2
PICO
question
|
P
(patients):
patients
who
required
an
oral
surgery
procedure.
I
(intervention):
the
use
of
CM
or
ACM,
combined
or
not
to
a
biomaterial.
C
(comparison):
defined
procedures
without
the
use
of
CM
or
ACM.
O
(outcomes):
oral
soft
or
hard
tissue
repair
and
regeneration
in
oral
area.
2.3
Search
strategy
|
An
electronic
search
of
the
MEDLINE
Pubmed
database
and
the
Scopus
database
was
carried
out.
We
searched
for
articles
published
in
English
up
to
and
including
July
2019.
The
following
search
combi-
nation
was
used:
(chorion*
or
amnion/chorion
or
chorionic
mem-
brane
)
and
(
guided
bone
regeneration
or
bone
regeneration
or
guided
tissue
regeneration
or
oral
surgery
or
tissue
regeneration
or
periodont*
or
tongue
or
maxillary
or
jaw
or
gum
or
oral
mucosa
or
oral
cavity
).
Additional
articles
were
also
added
after
manually
screening
the
list
of
references
of
all
publications
selected
by
the
search.
2.4
Selection
criteria
|
Studies
published
in
English
and
conducted
on
human
subjects
were
included.
Only
studies
analyzing
the
effectiveness
of
CM
or
ACM
in
oral
tissue
reconstruction
were
considered.
Prospective
(randomized
controlled,
nonrandomized
controlled,
cohort)
and
retrospective
stud-
ies
(controlled,
case
control,
single
cohort)
and
case
series
were
included.
in
vitro
studies,
preclinical
studies,
studies
based
on
the
use
of
CM
or
ACM
cells
without
their
matrix
and
case
reports
were
excluded.
2.5
Screening
of
studies
and
data
collectio
n
|
Tw
o
inde
p
en
de
nt
revie
w
ers
(M.F
.
and
S.G.
)
perf
orm
e
d
the
artic
l
e
sel
ec-
tio
n
and
da
ta
extr
a
cti
o
n.
The
tit
l
e
and
the
abs
tra
c
t
were
sc
re
en
ed
in
the
fi
rs
t
tim
e
acco
rd
ing
to
the
ques
ti
on
:
i
n
wh
ich
c
li
n
ica
l
i
nd
ica
t
ion
s
ha
ve
CM
or
ACM
been
sho
wn
eff
ec
ti
ve
fo
r
so
ft
or
hard
tis
su
es
repa
i
r
in
th
e
fi
eld
of
or
al
surg
ery
?
.
Full
-t
ex
t
ar
tic
le
s
we
re
then
ass
ess
ed
,
and
fin
al
ly
,
the
arti
cl
e
sele
cti
o
n
was
ma
de
.
In
c
ase
of
di
s
agr
e
em
en
t
betw
ee
n
the
re
vie
w
er
s,
artic
l
es
were
dis
cus
s
ed
to
deci
de
the
fina
l
out
c
om
e.
Stru
c-
tur
ed
tabl
e
s
were
gene
ra
t
ed
an
d
use
d
to
col
l
ec
t
dire
ct
ly
rele
va
nt
data
fr
om
sele
cte
d
pap
ers
.
The
data
extr
a
cte
d
fro
m
the
re
po
rts
were
gen
e
ra
l
2
GULAMEABASSE
.
ET
AL
Printed by [Universite de Bordeaux Service Facturier - 193.050.102.025 - /doi/epdf/10.1002/jbm.b.34783] at [28/12/2020].
ch
ara
c
te
ris
ti
cs
(a
ut
ho
rs
and
yea
r
of
pu
bli
c
ati
o
n)
,
type
of
memb
ra
ne
(C
M
or
ACM),
lev
el
of
ev
ide
n
ce,
numb
er
of
pat
ien
ts
i
nvol
ved,
to
tal
duration
of
the
study,
the
clinical
applications,
treatment
procedures,
eval
uati
on
cri
ter
ia,
an
d
effi
cac
y
of
th e
m
emb
rane
s.
The
p
rese
rva
tion
meth
ods
as
well
as
the
use
of
both
me
mbran
es
were
al so
r
ecor
ded:
these
included
the
processing
and
preservation
techniques
of
ACM
or
CM,
t
he
side
applie
d
agains
t
t
he
defect
,
the
m
embr
ane
fixa
tion
using
su
tur
e,
and
if
the
m
embr
ane
was
l
eft
exp
osed
t
o
th
e
oral
ca
vit
y
or
n
ot.
For
mis
sing
in
form
atio
n
i
n
th
e
se
lec
ted
art
icle
s,
the
aut h
ors
were
cont
acte
d
b
y
em
ail
to
co
mple
te
the
d
ata.
The
lev
el
of
evi
den
ce
of
the
i
nclu
ded
st
udie
s
was
ass
es se
d
usi
ng
the
N
ati o
nal
H
ealt
h
and
Medic
al
Res
ear
ch
clas
sif
ica t
ion
.
51
FIGURE
1
Flow
diagram
of
the
screened
publications
GULAMEABASSE
.
ET
AL
3
Printed by [Universite de Bordeaux Service Facturier - 193.050.102.025 - /doi/epdf/10.1002/jbm.b.34783] at [28/12/2020].
2.6
Analysis
of
the
data
|
Data
analysis
was
performed
in
a
descriptive
way,
since
the
informa-
tion
obtained
did
not
enable
meta-analyses.
3
|
RESULTS
3.1
Search
outcomes
|
In
total,
the
search
generated
142
potentially
relevant
articles
from
Pubmed
and
209
from
the
Scopus
database.
After
reading
titles
and
abstracts,
16
articles
from
Pubmed
database
and
5
from
Scopus
were
retained
for
further
investigation.
Entire
publications
have
been
read
and
17
eligible
articles
were
selected.
Four
articles
were
added
to
the
list
after
screening
the
references
of
these
17
publications.
Finally,
21
articles
met
the
eligibility
criteria
and
were
included
in
this
system-
atic
review.
The
selection
process
is
shown
in
Figure
1.
All
included
articles
have
been
published
from
2013
and
11
studies
were
per-
formed
in
India.
Based
on
the
level
of
evidence,
most
of
the
studies
were
randomized
clinical
trials
(n
=
13)
and
eight
were
case
series.
This
selection
was
separated
accordingly
into
three
main
areas:
peri-
odontal
surgery,
3,37,52-64
implant
and
preimplant
surgery
65-69
and
bone
reconstruction
following
tumor
resection.
70
3.2
Methods
of
CM/ACM
preservation
and
use
|
In
11
studie
s,
pati
ents
had
a
CM
allog
ra
ft
3,52
-56,
58,6
0-62
,66
whereas
in
the
othe
r
10
stu
di
es
an
ACM
all
ogr
aft
was
perf
orm
ed
.
37,57,5
9,63
-65,67
-70
Memb
ra
nes
were
free
ze-
drie
d
in
seve
n
studies
,
3,52
,56,
58,6
0-62
dec-
ellu
la
riz
ed
then
fr
eez
e-dr
ie
d
in
one
stud
y,
70
de-e
pi
thel
ia
lize
d
and
dehy
dr
ated
by
the
Puri
on
pro
ces
s
in
nine
studie
s,
37,5
7,59
,63-
65,6
7-69
and
jus
t
dehy
dra
te
d
in
two
stu
di
es.
53,5
5
In
two
public
ati
on
s,
the
preser
va-
tio
n
meth
od
s
wer
e
not
men
ti
oned
.
54,6
6
All
the
memb
ra
nes
were
then
ster
il
ized
.
The
mem
bra
ne
s
suppl
ie
d
by
the
Tata
Me
mori
al
Hos
pita
l
tis-
sue
ban
k
w
er
e
irr
ad
iate
d
w
ith
γ
radia
tion
,
3,52-5
6,
58,6
0-62
,66
Kaka
ba
dze
et
al.
used
rays
at
a
dose
of
15
kGy
,
γ
70
and
the
BioX
clud
e
membra
nes
wer
e
ster
iliz
ed
by
rays
or
irra
diat
ed
by
elec
tron
beams
at
a
dose
of
γ
ap
prox
im
atel
y
17.
5
k
Gy.
37,57,5
9,63-
65,67-69
The
memb
rane
s
wer
e
used
in
mono
lay
er
in
all
st
udie
s,
but
some
autho
rs
sp
ec
ifie
d
th
at
if
the
memb
ra
ne
fol
ds
on
itse
lf
to
get
her,
it
w
as
not
un
fol
de
d.
37
None
of
the
selected
articles
mentioned
which
side
of
the
membrane
was
applied
in
contact
with
the
defect.
However,
some
authors
were
contacted
via
email
and
the
mentioned
that
they
placed
no
importance
on
the
side
during
implantation.
3,53,56,58,60-62,64,67
In
only
four
studies
the
membrane
was
sutured
to
be
stabilized,
55,66,68,70
otherwise
it
was
just
applied
to
the
surgical
site.
3,37,52-54,56-65,67,69
The
membrane
was
left
exposed
voluntarily
in
four
studies.
65-68
In
most
studies,
the
membrane
s
were
applied
dried
and
were
then
rehydrated
by
the
blood
during
the
surgical
procedure.
One
author
rehydrated
the
membrane
in
0.9%
saline
for
30
min
before
grafting.
70
Membrane
use
strategies
were
summarized
in
Table
1.
3.3
Clinical
applications
|
Clinical
studies
are
summarized
in
Table
2.
3.3.1
Period
ontal
surgery
|
Use
of
CM
or
ACM
for
treatment
of
gingival
recessions
Seven
studies
reported
the
use
of
CM
52-56,58
and
ACM
57
associated
with
a
coronally
advanced
flap
technique
to
perform
root
coverage
of
gingival
recessions.
Five
of
them
were
clinical
trials,
which
compared
CM
to
amniotic
membranes
52-55
or
to
platelet-rich
fibrin
(PRF)
membranes.
56
One
study
reported
a
significant
improvement
of
all
investigated
parameters
using
CM
compared
to
PRF
membrane,
except
for
the
recession
width
where
the
difference
was
not
significant
between
both
groups.
56
Two
studies
showed
no
significant
difference
in
cover-
ing
gingival
recession
using
CM
or
the
amnion.
52,54
In
another
study,
CM
was
significantly
better
than
the
amnion
for
part
of
the
parame-
ters
(recession
width
and
root
coverage),
and
there
was
no
significant
difference
for
the
rest
of
parameters.
55
Chakraborthy
et
al.
showed
a
significant
gain
of
keratinized
gingiva
after
3
months
for
the
CM
group
compared
with
the
amnion
group,
whereas
a
significantly
smaller
recession
width
was
observed
in
the
amnion
group.
53
These
four
studies
concluded
that
CM
showed
equal
or
better
results
compared
to
the
use
of
the
amnion
alone
for
gingival
recession
treatment.
The
two
remaining
studies
were
case
series
which
reported
significant
improvement
of
the
gingival
recession
using
CM.
57,58
Use
of
CM
or
ACM
for
intrabony
defect
regeneration
The
use
of
CM
and
ACM
to
treat
periodontal
pockets
was
reported
in
six
studies,
including
five
randomized
trials.
Temraz
et
al.
compared
the
implantation
of
ACM
alone
to
a
bone
substitute
(DBM
putty)
without
a
membrane,
and
no
significant
difference
was
observed
between
both
groups
for
clinical
and
radiological
parameters
after
6
months.
59
In
three
studies
Kothiwale
et
al.
compared
CM
to
a
con-
trol
group
(open
flap
debridement
without
membranes)
and
they
observed
significantly
superior
results
for
all
investigated
parameters
using
CM.
3,60,62
In
one
study,
the
CM
was
used
to
cover
two
types
of
bone
substitutes.
The
study
criteria
were
significantly
improved
in
both
groups.
61
The
last
study
was
a
case
series
where
ACM
was
used
in
combination
with
a
freeze-dried
cortical
bone
allograft.
An
improve-
ment
of
pocket
depth
and
clinical
attachment
level
was
recorded
in
this
study.
37
Use
of
ACM
for
furcation
defect
treatment
ACM
was
used
in
two
studies
to
treat
furcation
lesions.
In
Taalab
et
al.,
randomized
clinical
trial
study,
ACM
was
associated
with
an
alloplastic
bone
graft
and
was
compar
ed
to
a
collagen
membrane
in
combination
with
the
same
bone
graft.
ACM
showed
significantly
bet-
ter
results
at
180
days
concerning
clinical
attachment,
quantity
of
keratinized
gum
and
furcation
components.
There
was
no
difference
between
the
groups
for
pocket
depth.
63
The
other
study
was
a
case
4
GULAMEABASSE
.
ET
AL
Printed by [Universite de Bordeaux Service Facturier - 193.050.102.025 - /doi/epdf/10.1002/jbm.b.34783] at [28/12/2020].
TABLE
1
Preservation
methods
and
uses
strategies
of
amniochorionic
membrane
(ACM)
and
chorionic
membrane
(CM).
N/A
not
applicable
Author/year
CM/ACM
Preservation
method
Flap
technique
Suture
of
the
membrane
Exposition
of
the
membrane
in
the
oral
cavity
Chakraborthy
et
al.
2015
CM
(Tata
memorial
hospital
TB)
Dehydrated
Split-thickness
flap
No
Nonexposed
Gupta
et
al.
2018
CM
(Tata
memorial
hospital
TB)
Freeze-dried
Split-thickness
flap
No
Nonexposed
Chopra
et
al.
2019
CM
(Tata
memorial
hospital
TB)
Dehydrated
Split-thickness
flap
Yes
Nonexposed
Dandekar
et
al.
2019
CM
(Tata
memorial
hospital
TB)
Freeze-dried
Split-thickness
flap
No
Nonexposed
Pundir
et
al.
2015
CM
(Tata
memorial
hospital
TB)
Not
specified
Split-thickness
flap
No
Nonexposed
Nevins
et
al.
2016
ACM
BioXclude
De-epithelialized
+
dehydrated
(PURION)
Split-thickness
flap
No
Nonexposed
Esteves
et
al.
2015
CM
(Tata
memorial
hospital
TB)
Freeze-dried
Split-thickness
flap
No
Nonexposed
Temraz
et
al.
2019
ACM
BioXclude
De-epithelialized
+
dehydrated
(PURION)
Full
thickness
flap
No
Nonexposed
Kothiwale
et
al.
2019
CM
(Tata
memorial
hospital
TB)
Freeze-dried
Full
thickness
flap
(Kirkland)
No
Nonexposed
Kothiwale
et
al.
2015
CM
(Tata
memorial
hospital
TB)
Freeze-dried
Full
thickness
flap
No
Nonexposed
Kothiwale
et
al.
2018
CM
(Tata
memorial
hospital
TB)
Freeze-dried
Full
thickness
flap
No
Nonexposed
Kothiwale
et
al.
2013
CM
(Tata
memorial
hospital
TB)
Freeze-dried
Full
thickness
flap
No
Non
exposed
Holtzclaw
et
al.
2013
ACM
BioXclude
De-epithelialized
+
dehydrated
(PURION)
Full
thickness
flap
No
Nonexposed
Rosen
et
al.
2015
ACM
BioX
clude
De-epithelialized
+
dehydrated
(PURION)
Split-thickness
flap
No
Nonexposed
Taalab
et
al.
2018
ACM
BioXclude
De-epithelialized
+
dehydrated
(PURION)
Full
thickness
flap
No
Nonexposed
Hassan
et
al.
2017
ACM
BioXclude
De-epithelialized
+
dehydrated
(PURION)
No
flap
No
Exposed
Joshi
et
al.
2017
CM
(Tata
memorial
hospital
TB)
Non
specified
No
flap
Yes
Exposed
Cullum
et
al.
2019
ACM
BioXclude
De-epithelialized
+
dehydrated
(PURION)
No
flap
No
Exposed
De
Angelis
et
al.
2019
ACM
BioXclude
De-epithelialized
+
dehydrated
(PURION)
Full
thickness
flap
Yes
Exposed
Holtzclaw
et
al.
2015
ACM
BioXclude
De-epithelialized
+
dehydrated
(PURION)
N/A
No
Nonexposed
Kakabadze
et
al.
2016
ACM
Decellularized
+
freeze-dried
N/A
Yes
Nonexposed
GULAMEABASSE
.
ET
AL
5
Printed by [Universite de Bordeaux Service Facturier - 193.050.102.025 - /doi/epdf/10.1002/jbm.b.34783] at [28/12/2020].
TABLE
2
Clinical
applications
of
amniochorionic
membrane
(ACM)
and
chorionic
membrane
(CM)
Author/study
design
(NHMRC)
Using
strategy
Condition
Patients
(n
total)/
follow-up
(t)
Evaluated
parameters
Results
Chakraborthy
2015/
Randomized
clinical
trial
Level
II
Miller's
class
I
and
II
gingival
recessions
(1)
Amnion
(2)
CM
N=1
2
t
=
6
months
-Gingival
index
(IG)
-Length
of
recession
(GR)
-Relative
attachment
level
(RAL)
-Width
of
recession
(GRW)
-Width
of
keratinized
gingival
(WGK)
-Root
coverage
-Significant
improvement
of
all
parameters
in
both
groups
compared
to
baseline
-WGK:
significantly
higher
in
the
CM
group
at
3
months
and
no
significant
difference
at
6
months
-GRW:
significantly
higher
for
the
CM
group
at
3
et
6
months
-IG,
GR
et
RAL
and
root
coverage:
no
significant
difference
between
the
groups
Gupta
2018
/
randomized
clinical
trial
Level
II
Miller's
class
I
and
II
gingival
recessions
(1)
Amnion
(2)
CM
N=1
0
t
=
6
months
-Plaque
index
(IP)
and
gingival
index
(IG)
-Probing
pocket
depth
(PPD)
-RAL
-Position
of
gingival
margin
-Gingival
thickness
-IP,
IG,
RAL
and
position
of
gingival
margin
showed
a
significant
reduction
in
each
group
compared
to
baseline
-PDD:
no
significant
difference
in
both
groups
-Both
groups
showed
a
statistically
significant
mean
increase
in
the
gingival
thickness
-IP,
IG,
PPD,
RAL
and
position
of
gingival
margin:
no
significant
difference
between
the
groups
-Gingiva
was
thicker
in
the
chorion
grou
p
without
significant
difference
Chopra
2019
/
randomized
clinical
trial
Level
II
Miller's
class
I
and
II
gingival
recessions
(1)
CAF
(control)
(2)
CAF
+
DFDBA
+C
M
(3)
CAF
+
DFDBA
+
amnion
N=3
0
t
=
/3
months
-IG
-GR
-GRW
-RAL
-Complete/partial
root
coverage
-WGK
-Score
IG,
GR,
GRW
and
RAL
showed
a
significant
reduction
in
the
three
groups
compared
to
baseline
-A
highly
significant
reduction
of
GRW
was
seen
in
the
CM
+
DFDBA
group
-A
highly
significant
reduction
of
GR
and
a
more
efficient
root
coverage
was
seen
in
the
CM
+
DFDBA
grou
p
-WGK
significantly
increased
in
all
the
study
groups
-CM
versus
control:
CM
has
significantly
better
results
at
3
months
for
IG,
GRW
and
WGK;
but
no
significant
difference
between
the
groups
for
RAL
et
GR
-CM
versus
amnion:
GRW
and
root
coverag
e
significantly
increased
in
the
CM
group
versus
the
amnion
group;
but
no
significant
difference
for
the
rest
of
the
parameters
Dandekar
2019
/
randomized
clinical
trial
Level
II
Miller's
class
I
and
II
gingival
recessions
(1)
CM
(2)
PRF
N
=
20/
t
=
6
months
-Clinical
attachment
level
(CAL)
-GR
-GRW
-WGK
-Gingival
thickness
-HR,
GRW,
CAL
and
WGK:
significantly
improved
in
both
groups
compared
to
baseline
-CM
for
CAL,
GR,
WGK
and
gingival
thickness:
significantly
improve
d
with
CM
compared
to
PRF
-GRW:
no
difference
between
the
groups
Pundir
2015
/
randomized
clinical
trial
Level
II
Miller's
class
I
canine
recessions
(1)
Amnion
(2)
CM
N=6
/
t
=
6
months
-WGK
-PPD
-GR
-CAL
-Gingival
biotype
-All
parameters
were
significantly
improved
in
both
groups
compared
to
baseline
-No
significant
difference
between
the
groups
after
3
and
6
months
-9/12
recessions
showed
100%
root
coverage
-10/12
recessions
developed
a
thick
biotype
6
GULAMEABASSE
.
ET
AL
Printed by [Universite de Bordeaux Service Facturier - 193.050.102.025 - /doi/epdf/10.1002/jbm.b.34783] at [28/12/2020].
TABLE
2
(Continued)
Author/study
design
(NHMRC)
Using
strategy
Condition
Patients
(n
total)/
follow-up
(t)
Evaluated
parameters
Results
Nevins
2016
/
case
series
Level
IV
Recessions
>4
mm
(1)
CM
N
=
19/
t
=
6
months
-IP,
IG
-PPD
-GR
-GRW
-CAL
-WGK
-PPD:
no
significant
difference
from
baseline
-GR,
GRW,
CAL,
WGK:
significantly
improved
-Mean
root
coverage
at
24
weeks:
56%
Esteves
2015
/
Retrospective
case
series
Level
IV
Miller's
class
I
gingival
recessions
(1)
CM
N
=
6/
t
=
6
months
-PPD
-CAL
-GR
-WGK
-Gingival
thickness
-All
parameters
were
significantly
improved
at
3
and
6
months
compared
to
baseline
-At
6
months,
nine
recessions
with
thin
biotypes
developed
thick
ones
and
14
recessions
showed
a
100%
root
coverage
-The
overall
percentag
e
of
root
coverage:
89.92
±
15.59%
Temraz
2019
/
randomized
clinical
trial
Level
II
Intrabony
defects
>6
mm
(1)
ACM
(2)
DBM
(C-blast
puttyTM,
demineralized
bone
matrix
with
cancellous
bone)
N
=
22/
t
=
6
months
Clinical
parameters:
-IP
-IG
-PPD
-CAL
Radiographic
parameters:
-Bone
defect
area
-IP:
no
difference
between
the
groups
-IG:
significant
improvement
in
both
groups
-PPD
and
CAL:
significant
improvement
in
both
groups
at
3
and
6
months
compared
to
baseline;
no
difference
between
3
and
6
months
-Bone
defect:
significant
improvement
in
both
groups
-No
significant
difference
between
both
groups
at
6
months
for
all
parameters
Kothiwale
2019
/
randomized
clinical
trial
Level
II
Molar
intrabony
defects
>6
mm
(1)
FDBA
+
CM
(2)
DFDBA
+
CM
N=9
/
t
=
12
months
Clinical
parameters:
-IP
-IG
-PPD
-CAL
-Mobility
Radiographic
parameters:
-Bone
defect
area
-IP,
IG,
PD,
CAL,
bone
defect
and
mobility
significantly
reduced
at
12
months
in
both
groups
compared
to
baseline
-No
significant
difference
between
the
groups
for
clinical
parameters
-Bone
density
at
12
months
was
significantly
higher
in
the
FDBA
+
CM
groups
Kothiwale
2015/
randomized
clinical
trial
Level
II
Intrabony
defects
>5
mm
anterior
zone
(1)
Open
flap
debridement
(control)
(2)
CM
N=5
/
t
=
6
weeks
-Gingival
thickness
-Significant
improvement
of
gingival
thickness
in
the
CM
group
at
6
weeks
compared
to
baseline
and
to
the
control
Kothiwale
2018
/
randomized
clinical
trial
Level
II
Intrabony
defects
>6
mm
Molar
zone
(1)
Open
flap
debridement
(control)
(2)
CM
N
=
10/
t
=
4
weeks
Clinical
parameters:
-IP
-Sulcus
bleeding
index
-PPD
-CAL
Biochemical
parameters:
-IL-11
in
gingival
crevicular
fluid
-All
clinical
parameters
were
significantly
reduced
after
4
weeks
in
both
groups
compared
to
baseline
-Significantly
better
results
in
the
CM
group
(except
IP:
No
difference
between
the
groups)
-Significant
improvement
of
biochemical
parameters
in
both
groups
at
4
weeks
-IL-11
levels
was
significantly
increased
in
the
CM
group
compared
to
the
control
group
Kothiwale
2013
/
randomized
clinical
trial
Level
II
Intrabony
defects
>5
mm
(1)
Open
flap
debridement
(control)
(2)
CM
N
=
10/
t
=
1
year
-IG
-IP
-PPD
-RAL
-Bone
gain
area
-Statistically
significant
improvement
of
IP,
IG,
PD,
RAL
and
bone
gain
in
both
groups
-The
results
of
the
CM
group
were
highly
better
at
12
months
for
all
parameters
compared
to
the
control
group,
except
for
RAL
where
the
difference
between
the
groups
was
not
significant
(Continues)
GULAMEABASSE
.
ET
AL
7
Printed by [Universite de Bordeaux Service Facturier - 193.050.102.025 - /doi/epdf/10.1002/jbm.b.34783] at [28/12/2020].
TABLE
2
(Continued)
Author/study
design
(NHMRC)
Using
strategy
Condition
Patients
(n
total)/
follow-up
(t)
Evaluated
parameters
Results
Holtzclaw
2013
/
retrospective
case
series
Level
IV
Intrabony
defects
(1)
Cortical
freeze-
dried
bone
allograft
+ACM
N
=
64/
t
=
12
months
-PPD
-CAL
-PPD
and
CAL
were
reduced
at
12
months
Rosen
2015
/
case
series
Level
IV
Glickman's
class
III/IV
furcations
1)
PDGF-BB
+
composite
allograft
+
ACM
N=5
/
t
=
6
months
to
2.5
years
Furcation
outcome:
-Furcation
invasion
-PDD
-CAL
-Periapical
radiographic
-3
Furcations
closed
-2
Furcations
reduc ed
to
class
I
in
their
facial
aspect
and
closed
on
the
lingual
aspect
-1
Furcation
remained
in
class
III
Taalab
2018
/
randomized
clinical
trial
Level
II
Glickman's
class
II
furcations
associated
to
Miller's
class
I
gingival
recessions
(1)
Alloplast
bone
graft
(biphasic
calcium
Phosphat
+
HA)
+
ACM
(2)
Alloplast
bone
graft
(biphasic
calcium
Phosphat
+
HA)
+
collagen
membrane
N
=
14/
t
=
9
months
Clinical
parameters:
-Healing
index
of
landry
(HIL)
-PPD
-CAL
-WGK
Radiographic
parameters
(CBCT):
-Horizontal
component
of
the
furcation
(CHF)
-Vertical
component
of
the
furcation
(CVF)
-HIL:
significant
increas
e
of
healing
in
the
collagen
group
whereas
no
significant
difference
in
the
ACM
group/significant
difference
between
groups
with
higher
collagen
content
-PPD
significantly
reduced
from
baseline
to
90
and
180
days
for
the
ACM
group/
greater
reduction
of
PPD
in
the
ACM
group
without
significant
difference
-Significant
reduction
for
CAL
from
baseline
to
90
and
180
days
in
the
ACM
group/no
difference
between
groups
from
baseline
to
30
and
90
days,
but
from
baseline
to
180
days
CAL
was
significantly
reduced
in
the
ACM
group
comp
ared
to
the
control
group
-WGK
improved
in
the
ACM
group
without
significant
difference.
No
change
in
the
collagen
group/the
difference
between
the
two
was
significant
at
90
and
180
days
where
the
ACM
grou
p
was
higher.
-Significant
decrease
of
CHF
in
both
groups
and
of
CVF
in
the
ACM
group
compared
to
baseline
-Significantly
greater
dec
rease
of
CHF
and
CVF
in
the
ACM
group
compared
to
the
control
group
Hassan
2017
/
single
blind
randomized
clinical
trial
Level
II
Alveolar
ridge
preservation
in
nonmolar
zone
(1)
ACM
+
freeze-
dried
bone
(2)
dPTFE
non
absorbable
+
freeze-drie
d
bone
N
=
20/
t
=
22
months
Clinical
and
radiographic
parameters
(CBCT):
-Horizontal
and
vertical
ridge
dimensions
-Histomorphometric
analysis
-Microtomographic
analysis
-Pain
score
(VAS)
-Clinical
and
radiographic
ridge
dimensions
were
not
significantly
different
between
the
treatments
-Histomorphometric
parameters
(bone
quality)
were
significantly
better
with
ACM:
ACM
sites
had
significantly
more
osteoids
and
higher
bone
density
volume,
but
significantly
less
graft
particles
compared
to
the
dPTFE
group
-VAS
was
significantly
lower
for
the
ACM
group
the
first
2
days
Joshi
2017
/
prospective
randomized
clinical
trial
Level
II
Alveolar
ridge
preservation
in
nonmolar
zone
(1)
FDBA
allograft
+
CM
(2)
Entire
tooth
allograft
+
CM
(3)
Dentin
allograft
+C
M
(4)
CM
(control)
N
=
15/
t
=
4
months
Radiographic
analysis
(CBCT):
-Horizontal
and
vertical
ridge
dimensions
Histologic
analysis
-Clinically
uneventful
he
aling
was
observed
at
all
sites
-Smaller
reduction
in
alveolar
crest
height
and
width
in
entire
tooth
and
dentin
allograft
sites
compared
to
the
control
and
the
FDBA
group
-Better
integration
of
graft
particles,
better
osteogenesis
and
angiogenesis
in
entire
tooth
and
dentin
sites
8
GULAMEABASSE
.
ET
AL
Printed by [Universite de Bordeaux Service Facturier - 193.050.102.025 - /doi/epdf/10.1002/jbm.b.34783] at [28/12/2020].
series
where
ACM
was
used
with
a
composite
allograft
containing
mesenchymal
stem
cells
in
a
matrix
of
freeze-dried
demineralized
bone
and
freeze-dried
bone.
An
improvement
of
the
furcation
defects
was
observ
ed
clinically
but
the
study
did
not
include
any
statistical
analysis.
64
3.3.2
Implant
and
preimplant
surgery
|
Use
of
CM
and
ACM
for
alveolar
ridge
preservation
Hassan
et
al.
compared
ACM
to
dense
polytetrafluoroethylene
(dPTFE)
membranes.
Both
membranes
were
used
after
extraction
sockets
filling
with
freeze-dried
b
one.
No
significant
difference
was
observed
between
the
groups
for
the
clinical
and
radio-
graphic
dimensions
of
the
residual
ridge.
Interestingly,
histomorphometric
results
show
ed
more
osteoid
tissue,
a
higher
bone
density,
and
less
graft
particles
after
3
months
in
ACM
group.
Besides,
pain
was
significantly
lower
for
the
ACM
group
after
24
and
48
hr.
65
Another
randomized
controlled
trial
evalu-
ated
allogenous
tooth
graft
in
comparison
with
freeze-dried
bone
allograft.
Both
grafts
were
covered
by
CM.
An
improvement
in
clinical
para meters
was
noted
in
al l
groups.
66
Finally,
a
case
series
reported
the
absence
of
inflammation
and
optimal
wound
healing
after
alveolar
ridge
preservation
using
a
bone
substitute
(Biooss)
covered
by
ACM.
67
Use
of
ACM
to
increase
keratinized
tissue
around
implants
Only
one
study
investigated
the
effectiveness
of
ACM
to
increase
keratinized
gingiva
around
dental
implants.
This
was
a
case
series
where
ACM
graft
could
be
performed
either
at
the
time
of
the
implant
placement
or
during
surgical
reopening
time
(in
a
two-stage
proce-
dure).
Application
of
ACM
leads
to
a
gain
of
2
mm
in
keratinized
gum
width.
68
Use
of
CM
and
ACM
to
repair
Schneider
membrane
in
sinus
elevation
procedure
A
case
series
reported
the
efficacity
of
ACM
in
repairing
perforations
of
the
maxillary
sinus
membrane
perforations.
However,
only
one
study
with
a
weak
level
of
evidence
has
been
conducted.
69
3.3.3
Use
of
CM
and
ACM
to
repair
large
|
mandibular
defects
Kakabadze
et
al.
used
ACM
for
covering
mandibular
reconstructions
after
segmental
mandibulectomy
following
tumor
resection.
Only
one
series
of
four
cases
was
identified,
and
it
was
focused
on
the
bone
graft
evaluation
(autogenous
versus
bioactive
bone).
All
bone
trans-
plants
were
covered
with
ACM
and
no
failure
was
noted.
ACM
mem-
branes
fulfilled
their
role
of
protection
against
fibrous
tissue
invasion
between
the
bone
graft
and
the
host
bone.
70
TABLE
2
(Continued)
Author/study
design
(NHMRC)
Using
strategy
Condition
Patients
(n
total)/
follow-up
(t)
Evaluated
parameters
Results
Cullum
2019
/
case
series
Level
IV
Alveolar
ridge
preservation
in
anterior
zone
(case
1)
and
molar
zone
(case
2)
(1)
BioOss/
InnerOss
+
ACM
N=2
/
case
1:
t
=
11
months
Case
2:
t
=
1
year
Clinical
assessment:
-Gingival
inflammation
Radiological
assessment:
-Bone
healing
-No
inflammation
-Satisfying
bone
volume
De
Angelis
2019/
case
series
Level
IV
Expansion
of
the
zone
of
keratinized
tissue
around
dental
implants
(1)
ACM
N
=
15/
t
=
1
month
-IP
-IS
-WGK
-Reduction
of
IP
and
IS
-Significant
increase
of
WGK
from
baseline
to
7,
15,
and
60
days
post
surgery
(average
gain
=
2
mm)
Holtzclaw
2015/
retrospective
case
series
Level
IV
Schneider
membrane
perforations
repair
(1)
ACM
+
freeze-
dried
cortical
bone
allograft
+
ACM
N
=
77/
t
=
5
years
Implant
survival
according
to
Albrektsson
criteria
Of
the
nine
cases
of
perforations,
23
implants
placed
and
one
failure
Of
the
95
cases
of
nonperforation,
158
implants
were
placed
and
three
failed
Kakabadze
2016/
c
ase
series
Level
IV
Reconstruction
of
mandibular
defects
after
tumoral
resection
(1)
Autogenous
bone
graft
+ACM
(2)
Biologically
active
bone
+
ACM
N=4
/
t
=
5
years
Clinical
criteria:
-Complications
occurrence
Radiological
criteria:
-Bone
volume
-No
complications
-Bone
volume
was
maintained
Abbreviations:
BDA,
bone
defect
area;
CAF,
coronally
advanced
flap;
CAL,
clinical
attachment
level;
CEJ,
cemento-ename
l
junction;
DFDBA,
demineralized
freeze-dried
bone
allograft;
dPTFE,
dense
polytetrafluoroetylene;
FDBA,
fried
-dried
bone
allograft;
GR,
length
of
recession
;
GRW,
width
of
recession;
HA,
hydroxyapatite;
HIL,
healing
index
of
landry;
IG,
gingival
index;
IP,
plaque
index;
PPD,
probing
pocket
depth;
PRF,
platelet-rich
fibrin;
RAL,
relative
attachment
level;
WGK,
width
of
keratinized
gingival.
GULAMEABASSE
.
ET
AL
9
Printed by [Universite de Bordeaux Service Facturier - 193.050.102.025 - /doi/epdf/10.1002/jbm.b.34783] at [28/12/2020].
4
|
DISCUSSION
The
objective
of
this
systematic
review
was
to
report
the
current
clini-
cal
applications
of
CM
and
ACM,
as
well
as
their
treatment
modalities,
in
oral
and
periodontal
surgery.
Among
the
21
included
articles,
CM
and
ACM
were
processed
using
four
different
preservation
methods.
Membrane
s
were
dehydrated
in
11
studies
and
this
dehydration
was
mostly
preceded
by
de-epithelialization
(Purion
process).
They
were
freeze-dried
in
eight
studies.
Lyophilization
was
preceded
by
decellularization
in
one
study.
The
freeze-dried
and
dehydrated
membranes
were
subse-
quently
sterilized
by
radiation.
Such
sterilization
procedures
allow
γ
membrane
storage
at
room
temperature
for
several
years.
Although
the
included
studies
did
not
investigate
this
parameter,
preservation
methods
might
affect
the
extracellular
matrix
of
the
basement
mem-
brane
and
lead
to
change
in
the
membrane's
biological
and
mechanical
properties.
35
Freeze-drying
appears
to
decrease
the
thickness
and
strength
of
the
membrane,
but
it
improves
the
adhesion
properties
compared
to
fresh
and
cryopreserved
membranes.
71
The
Purion
pro-
cess
is
a
de-epithelialization
followed
by
gentle
dehydration
that
pre-
serves
structural
integrity
and
biochemical
activity
of
the
tissues.
68
After
decellularization
and
lyophilization,
the
majority
of
growth
fac-
tors
and
cytokines
and
their
structural
and
mechanical
properties
seem
to
be
preserved.
72-74
The
biological
properties
of
dehydrated
ACM
grafts
have
been
investigated
in
other
studies:
cytokines,
chemokines,
growth
factors,
and
therefore
biological
activities
were
still
present
after
preservation.
74,75
In
our
review,
these
parameters
were
not
investigated
and
the
heterogeneity
of
preservation
methods
makes
the
results
difficult
to
compare.
In
this
study,
we
mainly
identified
seven
clinical
applications
of
CM
and
ACM
in
oral
and
periodontal
surgery:
gingival
recession
treat-
ment,
intrabony
and
furcation
defect
treatment,
alveolar
ridge
preser-
vation,
keratinized
gum
width
increase
around
dental
implants,
Schneiderian
membrane
repair
and
large
bone
defect
reconstruction.
CM
and
ACM
were
compared
to
a
conventional
surgery
without
membrane
or
to
the
following
materials:
collagen
membranes,
dPTFE
membranes,
PRF
membranes,
amnion
membranes,
and
to
a
bone
substitute.
CM
and
ACM
were
superior
to
PRF
membranes
and
amnion
in
gingival
recessions
treatment.
53,55,56
ACM
showed
better
clinical
and
radiological
results
than
a
collagen
membrane
for
furcations
treat-
ment.
63
One
study
reported
no
significant
difference
between
ACM
and
a
bone
substitute
used
alone
in
the
treatment
of
intrabony
defects.
59
Three
studies
reported
a
significant
improvement
in
treating
periodontal
pockets
using
CM
compared
to
conventional
sur-
gery
(open
flap
debridement).
3,60,62
Promising
results
were
also
observed
using
CM
and
ACM
for
alveolar
ridge
preservation.
65-67
ACM
showed
similar
results
than
a
conventional
nonresorbable
mem-
brane
for
post-extraction
ridge
preservation,
as
no
significant
differ-
ence
in
ridge
volume
dimensions
were
recorded.
Besides
histological
analysis
showed
a
better
bone
quality
using
ACM.
65
These
studies
also
reported
the
absence
of
post-operative
inflammation
and
satis-
factory
bone
healing
was
radiologically
observed
using
CM
and
ACM.
66,67
For
all
these
clinical
indications,
using
CM
or
ACM
showed
better
or
comparable
results
to
conventional
biomaterials.
This
could
be
explained,
among
other
things,
by
their
attractive
biological
proper-
ties.
The
use
of
CM
and
ACM
for
keratinized
gum
width
increase
around
dental
implants,
Schneiderian
membrane
repair
as
well
as
to
cover
large
bone
defects
reconstruction
were
only
investigated
through
case
series.
68-70
While
satisfactory
results
were
obtained,
studies
with
higher
levels
of
evidence
are
needed
to
draw
some
conclusions
for
these
applications.
In
all
included
studies,
CM
and
ACM
were
used
in
allografts
and
no
rejection
reactions
were
reported.
in
vitro
studies
have
shown
that
amniotic
and
chorionic
cells
do
not
trigger
an
immune
response
and
suppress
lymphocyte
proliferation.
Fetal
membranes
have
low
immu-
nogenicity,
which
reduces
the
risk
of
complications
in
comparison
with
xenografts.
76
They
do
not
express
classical
HLA
class
I
antigens
or
HLA
class
II
antigens,
which
protects
them
from
a
defensive
response.
They
also
express
nonclassical
immunoregulatory
antigens
such
as
HLA-G.
77
No
inflammatory
or
infectious
complications
were
observed
post-
operatively
in
the
selected
articles.
The
risk
of
infection
is
decreased
thanks
to
the
antiviral
and
antimicrobial
properties
of
these
fetal
membranes.
Talmi
et
al.
emphasized
the
antibacterial
properties
of
fetal
membranes
in
1991.
78
Since
then,
the
antimicrobial
and
antibiofilm
properties
of
AM
and
CM
against
Streptococcus
pneumoniae
,
found
in
the
nasopharynx,
were
highlighted
by
Yadav
et
al.
in
2017.
79
More
specific
studies
on
the
endobuccal
flora
lead
to
the
same
conclusions.
Ashraf
et
al.
highlighted
the
bactericidal
activity
of
ACM
in
vitro,
whereas
the
control
collagen
membrane
has
not
demonstrated
any
anti-bacterial
activity.
11
The
powerful
adhesive
properties
of
the
membranes
prevent
the
formation
of
a
gap
between
the
barrier
membrane
and
the
defect,
especially
in
irregular
areas,
which
would
also
reduce
the
risk
of
infection.
CM
and
ACM
were
left
exposed
voluntarily
in
four
studies.
65-68
Unlike
conventional
mem-
branes
CM
and
ACM
demonstrate
antibacterial
properties.
It
is
thus
possible
to
leave
them
exposed
without
risk
of
infection,
thereby
avoiding
the
inconvenience
of
flap
traction.
Some
authors
reported
that
dPTFE
membranes
could
also
be
left
exposed,
especially
since
their
pores
are
smaller
than
conventional
PTFE
membranes,
which
were
permeable
to
bacteria.
However,
dPTFE
membranes
remain
nonresorbable
and
biologically
inert.
65
Moreover,
placental
mem-
branes
possess
anti-inflammatory
properties.
These
membranes
reduce
inflammation
by
capturing
inflammation
cells,
12
and
express
interleukin
receptor
antagonists,
endostatins,
TIMP
1,2,3,4
matrix
metalloproteinase
inhibitors,
and