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Art R2
Art R2
N o n re s o r b a b l e M e m b r a n e s
When and Why?
Noel Ye Naung, BDS, Higher Grad Dip Clin Sc (OMFS), MSc (OMFS), FIAOMSa,*,
Ehab Shehata, DDS, MD, MSc (GS), PhDa,b,
Joseph E. Van Sickels, DDS, FICDa
KEYWORDS
! Resorbable membrane ! Nonresorbable membrane ! Guided tissue regeneration
! Guided bone regeneration ! Barrier membrane
KEY POINTS
! Guided tissue engineering has been proved successful for alveolar ridge augmentation,
maxillary sinus implant site development, periodontal furcation defects, and treatment
of intrabony pockets and socket preservation.
! Numerous factors play a role in the success of guided bone regeneration, such as the
choice of resorbable or nonresorbable membranes and the timing of membrane removal.
! The type of membrane chosen depends on the requirements needed for space creation.
! Nonresorbable membranes are required at load-bearing regions, such as in vertical ridge
augmentation.
! Resorbable membranes are recommended to be used in non–load-bearing regions, such
as in maxillary sinus augmentation.
INTRODUCTION
growth in dog femur, ileum, and spinal column using a plastic fenestrated cage as a
barrier to soft-tissue invasion. Recognizing potential benefits of guided bone regener-
ation (GBR) in dentistry, in 1960 Linghorne3 presented the sequence of osteogenesis
events, which he described as “pathologic and physiologic phases,” after bridging a
15-mm ostectomy site in dog fibula. In 1969, Richter and Boyne4 published a paper
on new concepts in facial bone healing and grafting procedures, in which they pre-
sented the use of hematopoietic bone marrow placed in a vitallium meshwork lined
with a Millipore filter to stabilize and discourage the ingrowth of fibrous tissue.
In the intervening period, the evolution of these bone-volume growth techniques has
improved. According to Jimenez Garcia and colleagues,5 the use of a membrane tech-
nique prevents the migration of fibroblasts and soft connective tissue cells into
the intended regeneration site. In 1996, Hermann and Buser6 discussed the critical
surgical factors for adequate and predictable regeneration: use of an appropriate
membrane, attaining primary soft-tissue healing, creation and maintenance of a
membrane-protected space, close adaptation and stabilization of the membrane to
the surrounding bone, and sufficient length of healing period. In 2006 Wang and Boy-
apati7 published the PASS principles: primary wound closure without tension to
enable proper healing by means of first intention and reduction of the risk of mem-
brane exposure, angiogenesis to promote blood supply, space maintenance to create
a bed for the undifferentiated mesenchymal cells, and clot stability to allow for the
proper development of these cells.
Current concepts to increase the outcome of successful bone regeneration are built
on those already discussed and are broken down into ideal properties anticipated
from the barrier membranes.8–10
Biocompatibility: the membrane should not trigger host immune response, sensiti-
zation, or chronic inflammatory reaction and not adversely affect healing.
Space creation and maintenance: the membrane should have adequate toughness
to create and maintain space to allow the ingrowth of nearby osteoblasts to regenerate
bone, and have adequate strength to withstand the pressures from nearby muscles of
mastication and the tongue.
Occlusivity and selective permeability: the membrane should prevent unwanted
cells such as epithelial cells, fibrous tissue, or granulation tissue from entering into
the intended bone-healing space, while permitting nearby osteoprogenitors, osteo-
blasts, and cells responsible for neovascularization as well as facilitating diffusion of
the growth factors, signaling molecules, nutrients, and bioactive substances.
Tissue integration: membrane should fully integrate with the host tissue to provide
structural integrity and provide mucosal support and stability. It should also have a
sufficient adaptability between the bone-membrane border by sealing off the cavity,
preventing fibrous tissue infiltration and encapsulation of the membrane.
Clinical manageability: the membrane should be easy to handle and should maintain
its shape and position for easy placement.
Various materials have been used to fabricate GBR membranes over the last decades.
The types of membrane can vary widely from titanium mesh that is very rigid to mem-
branes that are very flexible, and which may be bioresorbable or might require a sec-
ond surgery to remove it at a later stage.11
Resorbable Versus Nonresorbable Membranes 3
Nonresorbable Membranes
Cellulose acetate (Millipore) was the first material used to keep gingival connective tis-
sue away from the root surface and allow periodontal regeneration.12 Commercially
available nonresorbable guided tissue regeneration (GTR) membranes for periodontal
regeneration and GBR membranes for alveolar bone regeneration are expanded poly-
tetrafluoroethylene (e-PTFE) and high-density PTFE (d-PTFE), both of which are avail-
able with or without titanium reinforcement.13–16
Numerous studies have shown positive results with the use of e-PTFE membranes,
widely known as Gore-tex (W.L. Gore & Associates, Flagstaff, AZ, USA).17–20 How-
ever, premature exposure of e-PTFE membranes is relatively common and is reported
to be around 30% to 40%. Membrane exposure may lead to infection and lack of new
bone formation as a result of fibrous tissue ingrowth.21 Primary closure is necessary
over e-PTFE membranes, which can be challenging in larger defects.22 Another disad-
vantage of nonresorbable membranes is the need for additional surgery to remove the
membrane, increasing the risk of exposing newly regenerated bone to bacteria.
Timing of membrane removal is also important because early removal can lead to
resorption of regenerated bone, whereas late removal can increase the risks of bac-
terial contamination and infection.23
The e-PTFE membrane has been replaced with d-PTFE, marketed as Cytoplast bar-
rier membranes (Osteogenic Biomedical, Lubbock, TX, USA). This membrane has high
density and smaller pore size (0.2 mm), preventing bacterial infiltration and leading to
lower risks of infection when exposed. In addition, primary closure over the membrane
is not necessary.22,24 In a randomized controlled trial, no difference was detected in
the mean vertical bone defect fill after 6 months with either e-PTFE and d-PTFE mem-
brane; however, d-PTFE membrane was easier to remove than e-PTFE.25
Titanium mesh (eg, Ti-Micromesh; ACE, Brockton, MA, USA) is also commercially
available as nonresorbable GBR membrane. Various studies have demonstrated
that titanium mesh membranes have sufficient strength and toughness to provide
space maintenance and prevent contour collapse from mucosal compression
because of its elasticity.26 In addition, they are less susceptible to bacterial contami-
nation secondary to its smooth surface.27 However, stiffness of the material and sharp
edges caused by trimming and contouring can cause mucosal irritation and are asso-
ciated with higher risk of membrane exposure.27–29 In addition, the removal of titanium
mesh can be challenging. In a randomized clinical treatment trial of atrophic alveolar
bone in the posterior mandible, similar vertical bone gain and implant stability was
achieved by using either titanium mesh or d-PTFE membrane.30
Resorbable Membranes
Requirement for a second surgical procedure to remove a barrier membrane is the major
disadvantage of nonresorbable membranes. Since the early 1990s, bioresorbable mem-
branes have been successfully used clinically.31–33 Resorbable membranes are available
as natural and synthetic membranes. Natural membranes are manufactured using
bovine or porcine collagen or chitosan.34,35 Commercially available synthetic mem-
branes are made up of organic aliphatic polymers such as polyglycolic acid or polylactic
acid, and their modifications. These include poly-DL-lactic acid, polylactic-glycolic acid,
polyglycolic acid-trimethylene carbonate, poly-LD-lactic-glycolic acid-trimethylene car-
bonate, and poly-DL-caprolactone.23
Collagen has the ability to attract and activate gingival fibroblast cells and stimulate
fibroblast DNA synthesis.31,34,36 Biocompatible type 1 and type 3 collagen mem-
branes are commercially available with varying rates of resorption ranging from
4 Naung et al
0.5 month (CollaPlug; Zimmer Biomet, Warsaw, IN, USA) up to 10 months (Mem-Lok
RCM; BioHorizons, Birmingham, AL, USA).23 Chitosan is biodegradable and biocom-
patible, and possesses antimicrobial and osteoinductive properties.35 Synthetic mem-
branes have advantages of biocompatibility and complete hydrolysis as well as
removal by proteolytic enzymes from the body.23,37 These membranes are resorbed
by the body with variable resorption time from 1.5 to 24 months depending on the
type and properties of the materials.23,37
More recently, resorbable allograft membranes derived from natural biological ma-
terials such as human placental amnion chorion tissue (BioXclude; Snoasis Medical,
Golden, CO, USA), human pericardium (Mem-Lok Pericardium; BioHorizons), human
fascia lata (Fascia Lata Tissuenet; TissueNet, Orlando, FL, USA), and human fascia
temporalis (Tutoplast Fascia Temporalis; Biodynamics International, Milwaukee, WI,
USA) has become commercially available. As processed biological materials, they
carry minimal risk of inflammatory or foreign body reactions. In a study comparing
different types of membranes on New Zealand white rabbits, fascia lata, pericardium,
and e-PTFE membranes showed significantly better bone regeneration than fascia
temporalis.38
Because resorbable membranes do not require secondary surgery for their removal,
there is a reduced risk of infection and less tissue damage. As such, there is decreased
pain and discomfort, along with decreased costs associated with a second sur-
gery.26,39 However, the timing and degree of resorption of the membrane can be un-
predictable.40 Premature resorption can lead to gradual loss of strength, membrane
collapse, and loss of the ability to maintain space. Loss of strength can decrease
bone regeneration, allowing fibrous tissue ingrowth, and prolonged or incomplete
resorption can be associated with membrane exposure, inflammation, and bacterial
contamination. These disorders can jeopardize the healing of the newly formed
bone. In general, as resorbable membranes are not as stiff as nonresorbable mem-
branes they do not allow tenting of the tissues.
Clinical Trials
Class II furcation defects
A substantial number of comparative studies of resorbable and nonresorbable mem-
branes exists regarding the treatment of class II furcation defects. Coffesse and col-
leagues42 (1997), Scott and colleagues (1997)43, Eickholz and colleagues44 (1997), and
Karapataki and colleagues45 (1999) found no significant difference in probing depth
reduction, clinical attachment gain, and vertical and horizontal bone fill between
groups. Both resorbable membrane groups and nonresorbable membrane groups
showed significant clinical and radiographic improvements. In a randomized
Resorbable Versus Nonresorbable Membranes 5
In routine practice, the type of membrane used will vary with the choice of grafting ma-
terial and the nature of the bony defect. When a cortical or corticocancellous block
graft is used, the graft material will act as a tenting device; therefore, the use of resorb-
able membrane is recommended (Fig. 1), whereby a large anterior defect was recon-
structed with a combination of cortical and cancellous grafts augmented with a bone
morphogenetic protein (BMP) sponge and a resorbable membrane. Extensive under-
mining of mucosa of the lip was done before placement of the grafts. The cortical
grafts and autogenous marrow were obtained from the patient’s hip. The cortical
grafts were held in place with titanium screws that act as their own tenting of the graft
site. The space was created and maintained by the cortical blocks stabilized by the
titanium screws. The membrane was occlusive and did not need to be rigid, as the
grafting provided this aspect of GBR. With the necessary undermining to provide a
tension-free closure, the anterior vestibule was eliminated. At a secondary stage after
implants were placed, a maxillary vestibuloplasty was performed.
Likewise, with a sinus lifts the authors prefer a resorbable GBR because there is no
pressure on the graft after it is placed. In Fig. 2 the patient has a long-standing defect
from the loss of the upper first molar and second bicuspid. The maxillary sinus is
approached from a standard lateral window technique. Once the maxillary membrane
has been lifted and inspected for perforations, the sinus is lifted and a resorbable
membrane is placed, creating a space for the bone graft. In this case, demineralized
bone was packed against the maxillary floor and the membrane. A second membrane
was placed on the labial to provide an occlusive barrier laterally, and the flap was
closed.
Fig. 1. Augmentation of maxillary anterior region in preparation for implant placement us-
ing resorbable membrane. (A) Cortical grafts stabilized with titanium screws. (B) Cancellous
graft with autogenous marrow segment with autogenous marrow. (C) Resorbable mem-
brane placed over collagen sponge membrane with BMP-2, both placed before closure of
the wound.
Resorbable Versus Nonresorbable Membranes 7
Fig. 2. Maxillary sinus augmentation using resorbable membrane. (A) Exposure of bone
defect in the first M second bicuspid region. (B) Window developed, sinus lifted, and sinus
membrane visible above elevator. (C) Resorbable membrane about to be placed against the
sinus membrane. (D) Sinus packed, surgical site just before placement of a second resorbable
membrane on the labial surface.
Fig. 3. Vertical ridge augmentation of the posterior mandibular alveolar ridge using
nonresorbable membrane. (A) Horizontal defect mandible site developed. (B) Placement
of demineralized bone and a nonresorbable membrane secured with tenting screw. (C) Post-
operative panorex of grafted site. (D) Impacts placed and restored 1 year 6 months later.
When the exposure is late—for example, after a month or two—antibiotic use and
chlorhexidine use will be required along with removal of the membrane. When expo-
sures occur late in the course of treatment, there will usually be some success with the
augmentation (Table 1).
Table 1
Criteria for the choice of membranes
SUMMARY
The use of guided membranes in an attempt to improve the quality of bone grafting
is not a new concept. However, the evolution of these bone-volume growth
techniques has improved and most likely will continue to improve with time.5 In
routine daily practice, both types of membranes will be used depending
on the needs of the case. Whether a nonresorbable or a resorbable membrane
is used, it should be biocompatible, allow selective permeability with good
tissue integration, and have satisfactory handling properties. Surgical techniques
to attain primary soft-tissue healing, the creation and maintenance of a
membrane-protected space with close adaptation and stabilization of the mem-
brane to the surrounding bone, and sufficient length of healing period are very
important.6
Commercially available nonresorbable GTR membranes comprise e-PTFE and
d-PTFE, both of which are available with or without titanium reinforcement.13–16 In
addition to titanium mesh membranes, these have sufficient strength and toughness
to provide space maintenance and prevent contour collapse while preventing mucosal
compression caused by its elasticity.26 The authors’ preference is to use such mem-
branes when vertical augmentation is needed. The biggest disadvantages of nonre-
sorbable membranes are early exposure, infection, and loss of graft material. Gor-
tex (e-PTFE) has a 30% to 40% risk of exposure with subsequent infection and sup-
puration. d-PTFE, marketed as Cytoplast barrier membranes, has high density and
smaller pore size (0.2 mm), eliminating bacterial infiltration, and poses a lower risk of
infection when exposed. Currently the authors use d-PTFE when we nonresorbable
membrane is required.
There are numerous resorbable membranes available as natural and synthetic
membranes. Natural membranes are manufactured using bovine or porcine
collagen or chitosan. Resorbable allograft membranes derived from natural bio-
logics are currently available. Synthetic membranes are made of organic aliphatic
polymers (polyglycolide or polylactide) and are commercially available.26 The
biggest advantage of resorbable membranes is that they do not require secondary
surgery and usually have less tissue damage with less pain and discomfort. How-
ever, the timing and degree of membrane resorption are unpredictable. Premature
resorption can lead to loss of membrane strength and space collapse. Resorbable
membranes are preferred in the authors’ practice when the graft material will func-
tion to maintain the space (eg, corticocancellous bone graft), when there is no pres-
sure on the graft after its placement (eg, as in sinus lift procedures), or when
occlusion is needed, as in socket preservation. It is clear that one type of mem-
brane will not fit all clinical needs, and further work on this valuable clinical tool
is warranted.
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