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Limitations and options using resorbable versus nonresorbable membranes for

successful guided bone regeneration

Article in Quintessence international (Berlin, Germany: 1985) · November 2016

DOI: 10.3290/j.qi.a37133

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 Q U I N T E S S E N C E I N T E R N AT I O N A L

ORAL SURGERY

Nikolaos K.
Soldatos

Limitations and options using resorbable versus

nonresorbable membranes for successful guided bone
regeneration
Nikolaos K. Soldatos, DDS, MSD, PhD1/Popi Stylianou, DDS, MS2/Vasiliki P. Koidou, DDS3/
Nikola Angelov, DDS, MS, PhD 4/Raymond Yukna, DMD, MS5/Georgios E. Romanos, DDS, PhD6

Objective: Deficient bony ridges often complicate the implant phatic polyesters. Collagens are the most common type used.
treatment plan. Several treatment modalities are used to They have similar collagen composition to the periodontal
regenerate bone, including guided bone regeneration (GBR). connective tissue. Other materials available include human,
The purpose of this study was to summarize the knowledge on porcine, and bovine pericardium membranes, human amnion
different types of membranes available and currently used in and chorion tissue, and human acellular freeze-dried dermal
GBR procedures in a staged approach or with simultaneous matrix. Nonresorbable membranes used in GBR include
implant placement. The primary role of the membranes is to dense-polytetrafluoroethylene (d-PTFE), expanded-polytetra-
exclude epithelial and connective tissue cells from the wound fluoroethylene (e-PTFE), titanium mesh, and titanium-
area to be regenerated, and to create and maintain the space reinforced polytetrafluoroethylene. Conclusions: The most
into which pluripotential and osteogenic cells are free to common complication of nonresorbable membranes is expo-
migrate. Data Sources: A literature search was performed for sure, which has detrimental effect on the final outcome with
articles that were published in English on the topic. A selected both types of membranes. For vertical bone augmentation
number of studies were chosen in order to provide a review of procedures, the most appropriate membranes are the nonre-
the main characteristics, applications, and outcomes of the sorbable. For combination defects, both types result in a suc-
different types of membranes. Resorbable membranes are cessful outcome. (doi: 10.3290/j.qi.a37133)
made of natural or synthetic polymers like collagen and ali-

Key words: alveolar ridge augmentation, membranes, nonresorbable, resorbable

1 Assistant Professor, Department of Periodontics and Dental Hygiene, School of Lack of adequate bone for implant placement due to a
Dentistry, University of Texas Health Science Center at Houston, Houston, TX, previous history of periodontal disease, traumatic tooth
USA.
2 Clinical Assistant Professor, Department of Periodontics and Dental Hygiene,
extraction, or bone loss from prolonged use of a remov-
School of Dentistry, University of Texas Health Science Center at Houston, Hous- able prosthesis, is a common challenge in implant
ton, TX, USA.
3 Periodontal Resident, Department of Periodontology, School of Dentistry, Uni- 6
Prof Dr med dent, Department of Periodontology, Stony Brook University School
versity of Minnesota, Minneapolis, MN, USA.
of Dental Medicine, Stony Brook, NY, USA; and Department of Oral Surgery and
4 Professor and Chair, Department of Periodontics and Dental Hygiene, School of Implant Dentistry, Johann Wolfgang Goethe University of Frankfurt, Frankfurt,
Dentistry, University of Texas Health Science Center at Houston, Houston, TX, Germany.
USA.
Correspondence: Dr Nikolaos Soldatos, Department of Periodontics
5 Professor, Division of Periodontics, Department of Surgical Dentistry, University and Dental Hygiene, School of Dentistry, University of Texas Health
of Colorado School of Dental Medicine, Aurora, CO, USA; and Professor Emeritus, Science Center at Houston, 7500 Cambridge Street, Suite 6470, Hous-
Louisiana State University School of Dentistry, New Orleans, LA, USA. ton, TX 77054, USA. Email: Nikolaos.K.Soldatos@uth.tmc.edu

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dentistry. Bone loss after tooth extraction has been for a second surgical site.13 Alternative options to par-
reported to range between 40% and 60% during the ticulate autogenous bone include allogeneic, xeno-
first 3 years, and thereafter it is estimated to range geneic, and alloplastic grafts, which are widely used in
between 0.25% and 0.5% annually.1 In the classic study regenerating lost bone both in width and height.9
by Schropp et al,2 the findings showed a 50% reduction To the authors’ knowledge there are no reviews
in bone width, corresponding to 5 to 7 mm, of which discussing the limitations and options of resorbable
two-thirds of the bone loss occurred during the first 3 and nonresorbable membranes for successful GBR pro-
months post-extraction. cedures, in a staged approach (with implant placement
The presence of anatomical structures, such as the after GBR) or with simultaneous implant placement.
maxillary sinus, the nasal cavity, the inferior alveolar The purpose of this paper is to provide a compre-
nerve, and its extension, the mandibular incisive canal, hensive summary review of the different types of mem-
all limit the bone available for implant placement.3 branes available and currently used in GBR procedures
Therefore, bone regeneration before or during implant Two selected clinical cases are presented to illustrate
placement is often required for the longevity of two different protocols.
implants as well as for the esthetic and functional
results desired.4
Several treatment modalities are used to regenerate
DATA SOURCES
bone on deficient sites including autogenous or alloge- A literature search was performed for articles that were
neic block (cortical, cancellous, or corticocancellous) published in the English language on the topic. The
grafts, ridge split techniques, distraction osteogenesis, search was performed from 1959 to 2015 with the fol-
orthodontic tooth movement, and guided bone regen- lowing key words; “resorbable membranes”, “collagen
eration (GBR) with or without filler materials.5-8 membranes”, “nonresorbable membranes”, “titanium
Autogenous bone is considered to be the gold stan- mesh”, “e-PTFE membranes”, and “guided bone regen-
dard in GBR, with the major advantage of being osteo- eration”. Results were filtered to include only the
genic, osteoinductive, and osteoconductive.9 Autoge- papers relevant to dentistry. Only papers published in
nous bone blocks are harvested from the mandibular the English language were reviewed by the two
symphysis, external oblique ridge, ramus, the iliac crest, authors (NS, PS).
tibia, or cranium.10 Despite the numerous advantages
of autogenous block grafts in the treatment of bone
deficiencies, there are several disadvantages. Some of
RESOURCES SELECTION
the main disadvantages include increased postopera- All the results from the search were independently
tive morbidity, incision dehiscence at the donor site, reviewed by the authors (NS, PS) and considered as
chin ptosis, temporary paresthesia which can last up to either relevant or nonrelevant to the study question.
6 months, altered mandibular incisor sensation, and The relevance was determined based on the perceived
graft resorption during healing which accounts for up clinical significance, study design, data analysis, and
to 25% of volume loss.5,9 Buser et al11 reported that contribution to knowledge on the subject investigated.
without the use of a membrane over the block graft the Only the articles that were deemed relevant by both
resorption rate of autogenous block grafts increases to reviewers were included in this review. A total of 83
30% to 60%. This finding has been verified by Donos et studies were selected as relevant sources to review the
al,12 who showed that the resorption rate is slower main characteristics, applications, and outcomes of the
when membranes are used over block grafts. A less different types of membranes.
invasive approach to harvest particulate autogenous
bone is the use of bone scrapers, eliminating the need

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REVIEW bone. New bone can begin to form as early as 4 weeks

after GBR, and heavily relies on angiogenesis.23,24
General criteria of the membranes Membranes used as cell-occlusive barriers were first
Certain general criteria need to be fulfilled for the use described by Hurley et al,25 in spinal fusions. The pri-
of resorbable and nonresorbable membranes: mary role of membranes is to exclude epithelial and
• biocompatibility: prevention of soft tissue dehis- connective tissue cells from the wound area to be
cence and minimal tissue reactions that will com- regenerated, and to create and maintain the space into
promise the result which pluripotential and osteogenic cells are free to
• host tissue integration migrate.8,26
• space maintenance, structural integrity, and wound
stability, especially during the early stages of healing Resorbable membranes
• ease of use and handling during surgery with no The available resorbable membranes cannot maintain
memory adequate space unless the defect morphology is favor-
• enhanced duration able.8 In the presence of horizontal, vertical, or combi-
• for resorbable membranes, knowledge regarding nation defects, the use of tenting screws to adequately
the method and rate of resorption.14-16 maintain the space has been recommended.8 There are
two types of tenting screws, resorbable and nonresorb-
Creating a space is key for regeneration, and mem- able, and in combination with the resorbable mem-
branes provide soft tissue isolation, while maintaining branes they help decrease graft mobility and relieve
the space necessary for blood clot stability and recruit- external forces applied to the graft.9 Collagen, polymers
ment of mesenchymal and bone forming cells.17-20 The of lactic acid, and oxidized cellulose membranes have
membranes should be easy to use, allowing for good been used successfully around teeth, producing signif-
adaptation to the site, thus minimizing the risk of tissue icant amounts of new attachment.27 The materials used
perforation and dehiscence. In addition, membrane for the fabrication of resorbable membranes are natu-
integration with the soft tissue prevents connective ral, such as collagen, or synthetic polymers, like ali-
tissue proliferation into the defect while providing phatic polyesters. Examples of aliphatic polyesters
access to mesenchymal cells into the defect under the include polyglycolide (PGA) or polylactide (PLA). Specif-
membrane. In order to ensure maximum osteoblast ically, they can be fabricated from poly-DL-lactide,
proliferation, the membrane must be able to create and polyglycolide acid, poly-DL-lactide acid, poly-DL-lac-
maintain the space, thus keeping the blood clot and tide-co-glycolide, hydrolysable polyester, and polygla-
bone graft stable while protecting the site from exter- ctin 910 mesh.28 Natural membranes (collagen) resorb
nal forces.20-22 via enzymatic degradation, whereas synthetic mem-
branes resorb via non-enzymatic (hydrolysis) cleavage
Role of the membranes of PGA and PLA into pyruvic and lactic acids.28
During the first 24 hours after GBR surgery, the wound Collagen membranes are the most common type of
space is initially filled with a blood clot, which is later resorbable membranes used. They have similar colla-
resorbed by neutrophils and macrophages and gen composition as the periodontal connective tissues,
replaced by granulation tissue. The granulation tissue is weak immunogenicity and cytotoxicity, and promote
rich in mesenchymal stem cells and blood vessels, chemotaxis of periodontal ligament (PDL) and gingival
allowing nutrients and cells to arrive at the site, forming fibroblasts.29,30 Moreover, collagen membranes pro-
the osteoid. Deposition of minerals follows and woven mote hemostasis, they are easy to manipulate, and they
bone is then formed, around which bone continues to degrade by physiologic means with the ability to calcify
be deposited, resulting in the formation of lamellar and ossify when placed in close proximity to bone.16,31

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Table 1 Advantages and disadvantages of resorbable membranes

Advantages Disadvantages
Decreased patient morbidity Uncontrolled duration of barrier function
No need for second stage surgery
The need for tenting screws and bone to support the membrane and to avoid its collapse
to remove the membrane
Simplified surgical procedure Remnants of the membrane found in direct contact with dental implants
Lower rate of exposure Micromovement of the membrane leads to movement of grafting material and disruption of the blood clot
Memory, especially for the highly cross-linked membranes

The most common sources of collagen are human, por- consists of the innermost lining of the placenta and has
cine, or bovine, and can be made from pericardium, two layers. Placental tissue offers anti-inflammatory
calfskin, dermis, and Achilles tendon.16,28 The first colla- and anti-bacterial effects during tissue healing.35,36
gen membranes used comprised two layers, with the Amnion tissue includes laminin-5 protein for cellular
inner porous surface facing the bone and consisting of adhesion of gingival epithelial cells, type I, II, IV, V, and
loosely arranged collagen fibers, thus allowing osteo- VI collagen, platelet-derived growth factor-α (PDGF-α),
blasts to enter the site. The outer dense surface was platelet-derived growth factor-β (PDGF-β), fibroblast
facing the soft tissue and acted as a barrier, preventing growth factor, and transforming growth factor-β.37-39
fibroblasts from proliferating into the bony defect.32 However, the use of the membrane is a technique-sen-
However, there was a risk for disease transmission, and sitive approach because it is very thin and fragile.
they posed limitations, especially for patients with spe- Dermal allograft is another type of resorbable mem-
cific religious beliefs.28 brane that was initially introduced as an alternative to
Human, bovine, or porcine pericardium membranes the conventional connective tissue grafts in mucogin-
have been introduced for both guided tissue regenera- gival procedures. It is an acellular freeze-dried dermal
tion (GTR) and GBR procedures demonstrating resorp- matrix graft composed mainly of type I collagen.28 In a
tive stability. Bovine pericardium membranes are man- case report study, dermal allograft was evaluated clini-
ufactured under the Tutoplast Process, which cally and histologically for its ability to serve as a barrier
inactivates any pathogens and removes unwanted in GBR. The results demonstrated complete incorpora-
materials, such as cells, antigens, and viruses.33 One tion of the dermal allograft in the surrounding tissues
disadvantage is the delayed vascular penetration, by 6 months and the histologic sections showed new
which could potentially inhibit bone regeneration. bone adjoining residual bone particles.40
Rothamel et al34 concluded that the compact intercon- The main advantages and disadvantages of resorb-
necting porcine pericardium collagen showed a high able membranes are summarized in Table 1.8,12,16,32
degree of biocompatibility, supported bone cell prolif-
eration, and resorbed without inflammation at 12 Duration of the membranes
weeks. Collagen membranes have unpredictable resorption
In 2008, a new type of resorbable membrane of rates, which can vary from 4 to 24 weeks.16,41 Hürzeler et
human amnion and chorion tissue was introduced in al15 found intact porcine membranes 6 months follow-
dentistry. It has been used in medicine for over 100 ing GBR. However, prolonged resorption rate does not
years for skin wound applications and ophthalmologic always result in greater bone regeneration.16 The pres-
surgery. This tissue is obtained from mothers undergo- ence of periodontal pathogens at the surgical site may
ing elective caesarian section deliveries. The membrane cause early degradation and compromise the final

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outcome. In addition, early exposure of the membranes Case 1

leads to faster degradation; though highly cross-linked A 58-year-old Caucasian man, American Society of
membranes may keep their integrity as long as bac- Anesthesiologists (ASA) classification I, was referred
terial contamination is prevented.42 The need for tent- from the undergraduate clinic with Seibert Class III
ing screws and bone graft is mandatory to support the defects in the area of the mandibular right first and
membrane and maintain the space.8 Mellonig et al43 second molars. The teeth were extracted a year previ-
found that the use of a bone graft material prevents ously and only the first molar site was ridge-preserved
membrane collapse while creating the necessary space at the time (Figs 1a and 1b). The case was treated with
for regeneration. Moreover, micromovement of the the following protocol:
resorbable membrane following surgery may lead to 1. An intrasulcular incision was placed around the
disruption of the blood clot, disruption of the bone mandibular right second premolar, and a midcrestal
grafting material, and soft tissue dehiscences.19 incision was placed at the area of the first and sec-
PLA/PGA membranes are biodegradable, biocom- ond molar sites extending from the distal surface of
patible, and easier to handle clinically, compared to the second premolar to the retromolar pad and
polytetrafluoroethylene (PTFE) membranes. PLA/PGA continuing to the mandibular ramus for 1 cm.
resorption rate ranges between 5 and 12 months and a 2. Mylohyoid (Fig 1c) and periosteal releases were
minimum duration of 4 to 6 weeks is necessary to placed.13
enable successful bone regeneration.28 3. Cortical perforations were made with #8 round bur.
Non-cross-linked collagen membranes have a half- 4. 8-mm tenting screws were placed with 3 mm incor-
life that varies between 7 and 28 days.16,43 Cross-linking porated into the bone (Fig 1d).
is used to prolong the duration of the membranes. 5. A highly cross-linked resorbable membrane was
Some methods used to increase the cross-linking of placed.
collagen membranes include ultraviolet light, hexa-
methylene diisocyanate, diphenylphosphorylazide, glu-
taraldehyde, and sugar-D-ribose.16,44 Glutaraldehyde is
the most commonly used chemical cross-linking tech-
nique.16 The higher the degree of cross-linking, the
slower the rate of degradation, thus providing more
Fig 1a Periapical
time for osteogenic cells to repopulate the regenera- radiograph before
tive site.16,45 The use of ribose, a natural cross-linking the extractions of
mandibular right
agent, facilitates controlled biodurability of the barrier
first and second
membrane for up to 4 to 6 months, while retaining molars.
sufficient permeability to sustain osteoblasts in
vitro.44,46 This type of membrane enhances the capacity
to withstand bacterial collagenolytic degradation in
case of exposure, allowing for soft tissue healing and
dehiscence closure.44,47
The role of mechanical compression of the grafting
material was discussed by Romanos et al.48 By increas-
Fig 1b Preopera-
ing the compressive force, the small defects were filled tive clinical and
and the amount of new bone formation increased. radiographic over-
view of area man-
Thicker collagen membranes allow for better compres- dibular right first
sion and better blood clot stabilization.48 and second molars.

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Fig 1c Flaps re-

flected and mylohy-
oid muscle release at
area of mandibular Fig 1d Tenting screws placed to support the membrane and
right first and sec- bone, after bone decortication with #8 round bur at area of man-
ond molars. dibular right first and second molars.

Fig 1e Highly cross-linked membrane tacked on the lingual

aspect and mixed bone covering the tenting screws (mandibular
right first and second molars).

Figs 1f to 1h CBCTs before (f)

and after (g and h) the GBR,
showing an average bone gain
f of 5 to 6 mm.

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6. A mix of 1:1 anorganic bovine bone matrix (ABBM) 8. The sutures were removed at 5 weeks postopera-
and autogenous bone, harvested from the external tively.
oblique ridge with bone scrapers, was used (Fig 1e). 9. With the use of CBCT, an average bone gain of 5 to
7. Double-line suturing was performed using PTFE 6 mm was noted both horizontally and vertically 6
(4-0) sutures, and polypropylene sutures (4-0 and months postoperatively (Figs 1f to 1h).
6-0); amoxicillin 500 mg tablets, hydrocodone/APAP 10. The tenting screws were removed (Fig 1i), and a
10/325, 0.12% chlorhexidine solution, and ibupro- trephine biopsy was performed showing histologi-
fen 600 mg were prescribed. cally 50% and 60% of vital bone at the areas of the

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Fig 1i Clinical overview of the regenerated bone, after the Fig 1j Two implants were placed uneventfully with the use of a
removal of tenting screws. surgical guide.

mandibular right first and second molars respect-

ively.
11. Two Straumann bone level implants were placed
(Figs 1j and 1k); the quality of bone was evaluated
as Type I bone.
12. Three months later, the stage-two surgery was per-
formed, and the case was referred back to the re-
storative dentist for the final restoration.

Nonresorbable membranes
There are four common nonresorbable membranes Fig 1k Final periapical radiograph after implant placement.
and materials used today in dentistry for GBR proced-
ures. These include: brane.51,53,54 Currently, the e-PTFE membrane has been
• expanded-polytetrafluoroethylene (e-PTFE) discontinued and other nonresorbable membranes are
• dense-polytetrafluoroethylene (d-PTFE) widely used in lieu of the e-PTFE membrane.20 The use
• titanium mesh of d-PTFE in dentistry is becoming more widely
• titanium-reinforced PTFE.8,19,49,50 accepted because it has a smaller pore size compared
to e-PTFE.50 A smaller pore size minimizes bacterial
e-PTFE membrane has numerous small pores that pro- infiltration, and d-PTFE membranes can in fact be left
mote tissue cell attachment, stabilizing the wound area exposed to the oral cavity without running the risk of
while at the same time restricting migration of connec- bacterial contamination and infection. d-PTFE mem-
tive tissue and epithelial cells.49 A major disadvantage branes maintain the space and stabilize the wound
of the e-PTFE membranes is that once they become sufficiently, allowing sufficient time for bone regenera-
exposed to the oral cavity there is an increased risk of tion. In addition, since the membrane does not attach
bacteria penetration.8,51 In those cases, premature to the tissue, the removal through the mucosal flap is
removal is mandatory. However, there is a higher rate possible without disturbing or traumatizing the muco-
of resorption with the resorbable membranes after sal tissue. Due to the limited porosity of the d-PTFE
exposure, which can also adversely affect the out- membranes, the blood supply to the area is limited,
come.52 Furthermore, because of the ability of the thus successful bone regeneration relies on adequate
e-PTFE membrane to attach to the tissue, a second blood supply from the marrow space through cortical
surgery is usually necessary to remove the mem- perforations.54

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Table 2 Advantages and disadvantages of nonresorbable membranes

Advantages Disadvantages
Mechanical stability of the graft or the space under the membrane Increased risk of exposure
Excellent biocompatibility Increased risk of soft tissue ingrowth
Stiffness which is suitable for space maintenance, wound stability and success-
Increased risk of infection after exposure
ful bone regeneration
Plasticity, allows for bending, contouring and adaptation to any defect morph-
Necessary primary fixation of the membrane at the initial surgery
ology
Necessary second surgery to remove it
Technique-sensitive approach

Titanium mesh provides the necessary rigidity the maxillary left central incisor necessitated its
required for stability of the surgical site as well as main- extraction (Fig 2a). The case was treated with the fol-
taining the space for bone regeneration, preventing lowing protocol:
micromovement, membrane collapse, and graft dis- 1. Extraction of the maxillary left central incisor and
placement from external forces. In case of membrane ridge preservation using freeze-dried bone allograft
exposure, there is a low risk of infection with the tita- (FDBA) and collagen membrane utilizing the “ice-
nium mesh membranes, and premature removal of the cream cone technique” (Fig 2b).57 The membrane
membrane is rare.52 There are two types of titanium was placed into the socket against the buccal wall
mesh materials, microporous and macroporous. In a and was secured under the palatal tissue.
study by Gutta et al,49 it was found that there was
greater bone formation and regeneration with the mac-
roporous titanium mesh compared to the microporous
titanium mesh and resorbable membrane. In addition,
there was a significant soft tissue ingrowth with the
resorbable membrane, whereas the macroporous tita-
nium mesh prevented soft tissue ingrowth better com-
pared to the other two types of membranes. However,
the mineral apposition rate was found to be higher
Fig 2a Initial periapical radio-
with the resorbable membrane compared to either graph of the sites of the maxil-
titanium mesh membranes.49 Finally, studies showed lary central incisors.

loss of up to one half of the graft due to complications

associated with the use of titanium micromesh.55,56
To summarize, the main advantages of nonresorb-
able membranes are included in Table 2.8,51,53,54

Case 2
A 40-year-old Hispanic man, ASA I, was referred from
the graduate prosthodontics clinic to the graduate
periodontics clinic with Seibert Class III defect in the
area of the maxillary right central incisor. This tooth had Fig 2b Clinical view at the time of ridge preservation with the
been extracted 7 years earlier, and recurrent caries on use of ice-cream cone technique (maxillary left central incisor).

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Fig 2c Postoperative view 6 weeks after the ridge preservation Fig 2d Bone morphology after cortical perforations (#2 and 4
(maxillary left central incisor) and the Siebert class III defect on the round burs) and prior to guided bone regeneration (maxillary right
maxillary right central incisor. central incisor).

Fig 2e Titanium mesh in position and secured with fixation Fig 2f Reentry at 6 months demonstrating sufficient ridge width
screws after bone placement (maxillary central incisors). for implant placement (maxillary central incisors).

Fig 2h Final periapical

radiograph after implant
Fig 2g Check of the final implant position (maxillary central placement (maxillary
incisors). central incisors).

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2. Approximately 6 months later, the patient returned e-PTFE membranes without bone resulted in compres-
for ridge augmentation at the sites of the maxillary sion of the membrane into the space of the defect,
central incisors (Fig 2c). A midcrestal incision was compromising the final result.15,58-60
performed at the sites of the maxillary central inci- In a multicenter study by Becker et al,61 e-PTFE
sors and a vertical incision was placed on each site membranes around immediate implants were used
preserving the papillae on the mesial of the lateral without bone grafts or fillers. The implants were placed
incisors. slightly subcrestally and the flaps were sutured, obtain-
3. Periosteal release was placed for flap advancement. ing primary closure. Out of 49 sites, 29 membranes
4. Cortical perforations with #2 and #4 round burs remained in place until abutment connection, 20 mem-
were placed (Fig 2d). branes were removed after an average time of 84 days,
5. The titanium mesh membrane was secured with 28.5% of membranes were prematurely exposed, and
two titanium screws on the buccal and one on the 12.2% were removed due to infection or inflammation.
palatal aspect (Fig 2e). At abutment connection time (6 months after implant
6. FDBA was used. placement), membrane-retained sites demonstrated an
7. There was no use of growth factors. average bone fill of 4.8 mm and sites with early mem-
8. Double-line suturing was performed with PTFE and brane exposure had an average bone fill of 4 mm. In
chromic gut sutures. Clindamycin 300 mg tablets, the membrane-retained group, 0.6 threads were
hydrocodone/APAP 5/325 tablets, 0.12% chlorhexi- exposed, compared to 2.6 threads exposed at the early
dine solution, and ibuprofen 600 mg were pre- exposure group, which was found statistically signifi-
scribed. cant.61
9. The sutures were removed at 3 weeks postopera- Simion et al51 evaluated the use of exposed e-PTFE
tively. membranes without bone graft in cases of immediate
10. A 6-month healing period was allowed prior to implant placement, and completely covered e-PTFE
reentry and dental implant placement. membranes with delayed implant placement (30 to 40
11. An average of 3 mm of vertical bone and 6 mm of days after the extraction). Complete bone regeneration
horizontal bone gain was achieved as measured on was noted only in cases with no membrane exposure.
radiographs and clinically (Fig 2f). In the exposed membrane group, the membranes were
12. Two Astra implants were placed uneventfully and removed approximately 30 to 40 days postoperatively,
left to heal for 4 months (Figs 2g and 2h). The qual- and findings showed incomplete bone regeneration
ity of bone was evaluated as Type II bone. with the implants extending 1 to 2 mm above the bone
13. Four months later, the implants were uncovered crest. The bacteriologic findings indicate the ability of
and healing abutments were placed. bacteria to penetrate through the membrane and
14. The case was referred back to the restorative dentist potentially compromise the result of bone regenera-
who placed the final porcelain-fused-to-metal tion, especially in the case of prematurely exposed
screw-retained crowns. membranes.51
In another study by Simion et al,62 PLA/PGA mem-
branes were compared to e-PTFE membranes for their
DISCUSSION efficacy to regenerate bone around implants without
GBR around implants at time of implant the use of bone graft in post-extraction sockets. A third
placement group without a membrane served as control. Histo-
Several investigators in the mid-1990s showed that logic findings showed denser bone with e-PTFE mem-
resorbable membranes failed to predictably foster new branes compared to PLA/PGA. No remnants of the PLA/
bone formation around dental implants. The use of PGA membranes were detected 6 months after the

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surgery. The e-PTFE specimens showed visibly more in the e-PTFE group. e-PTFE membranes resulted in a
bone formation, which may be attributed to lack of significantly higher percentage of overlying soft tissue
space maintenance and duration of the PLA/PGA mem- dehiscence and membrane exposures compared to
branes.62 collagen barriers. Regardless of the membrane used,
The same research group evaluated the same mem- when the barrier was primarily fixed with polylactic
branes with the use of autogenous grafts around acid pins, 63.6% of the sites healed uneventfully com-
implant dehiscences and fenestrations at the time of pared to 28.6% where no fixation of the membrane was
implant placement. After 6 to 7 months of healing, the applied, which was statistically significant.19
e-PTFE group showed a higher percentage of bone fill Zubery et al65 analyzed histologically seven human
(98.2%) than the PLA/PGA group (88.56%), but the dif- specimens around implants using ribose cross-linked
ference was not found to be statistically significant.63 collagen membrane and one of the following filler ma-
Zitzmann et al32 used collagen membranes with terials: FDBA alone, FDBA with autogenous composite
anorganic bovine bone around short-term delayed graft, DFDBA alone, autogenous bone alone or bovine
implants and long-term delayed implants. The initial bone mineral. Six months postoperatively, in five out of
average surface area of the defect was 16.3 mm,2 which seven specimens, the membrane acted as a physical
reduced to 1.7 mm2 at reentry surgery, with mean barrier with no signs of connective tissue cell or active
defect resolution of 87%. Defect resolution was statisti- macrophage invasion. In the same specimens, a typical
cally higher in the maxilla compared to the mandible. pattern of mineralization was noted followed by osteo-
Furthermore, the presence of a provisional restoration blastic cell invasion. New dense bone formed in close
reduced the defect size. Defect resolution was three to proximity to the membrane, which was characterized
four times more likely to be achieved with a provisional by numerous osteocytes in lacunae and bone marrow
in place compared to sites with no provisional restor- spaces.65
ation.32 Lorenzoni et al66 evaluated 129 implants demon-
Sevor et al64 used highly cross-linked resorbable strating a combination of vertical and horizontal defect
membranes around hydroxyapatite-coated and grit- at the time of implant surgery. The groups were divided
blasted implants placed on the mandible. No mem- to e-PTFE membranes with DBB or autogenous bone
branes were used in the control group. At 8 weeks, the (group 1), titanium reinforced e-PTFE membranes with
defect fill was significantly greater in the membrane DBB or no bone (group 2), and polyglycolide self
group.64 inforced-PGA with autogenous bone (group 3). Surgical
Hürzeler et al15 evaluated the outcome of GBR reentry was performed in 24 weeks. Group 1 showed
around implants with exposed threads at the time of 84% of defect reduction, group 2 showed 81% of defect
implant placement. The groups consisted of resorbable reduction, and group 3 showed 60%. There was a stat-
membranes with or without deproteinized bovine istical significance between groups 1 and 3, and groups
bone (DBB), e-PTFE membranes with DBB, and a control 2 and 3.66
group. The groups with the membranes and bone Simion et al67 evaluated the outcome of vertical
showed similar results, and new mineralized bone was bone regeneration with the use of titanium reinforced
found in contact with the implants.15 e-PTFE membranes and the use of either autogenous or
Carpio et al19 compared resorbable and nonresorb- DFDBA bone graft around implants. The autogenous
able membranes in GBR around implants at the time of bone group had higher vertical bone gain and the qual-
implant placement with the use of anorganic bone ity of the preexisting bone was found to be the most
mineral. Twenty-two percent of the implants in the important factor in the regeneration.67
collagen barrier group failed compared to the 16.67%

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In a case series by Llambės et al,68 resorbable mem- sure, with 16.3% incidence around implants treated with
branes were used for vertical augmentation at the time resorbable membranes and 11.1.% to 24.4% incidence
of implant placement, with the implants serving as around implants treated with e-PTFE membranes.
tenting screws. A total of 14 posterior mandibular sites In a case series by Scheyer and McGuire,44 GBR
were treated. The mean bone regeneration was 3 mm, around implants with dehiscence defects ranging from
corresponding to 83% of the exposed implant surface. 5 to 9 mm and fenestrations ranging from 5 to 10 mm
At the 1-year follow-up after loading, 24 implants was evaluated. Cross-linked membranes trimmed to
showed 100% vertical regeneration, two implants extend 2 to 3 mm beyond the defect margins and fixed
> 50% to < 100%, three implants > 20% to < 50%, and with either sutures, screws, or tacks were used. At the
three implants 0%. A histologic examination of one of 6-month reentry, the majority of the defects were fully
the successful sites demonstrated a thin external layer covered by bone and 66.6% of the membranes
of connective tissue in contact with the membrane and remained physically intact.44
new trabecular bone covering large marrow spaces
underneath.68 GBR before implant placement
In a systematic review by Rocchietta et al,69 studies (staged approach)
using a one-stage approach with e-PTFE membranes, Locci et al71 cultured in vitro human fibroblasts using as
either with machined or rough surface implants, were substrates an extracellular matrix membrane (95% col-
included. After an observation period of 1 to 7 years lagen type I and III, and 5% chondroitin glycosamino-
there was a vertical bone gain of 2 to 8 mm. However, glycan) and e-PTFE membranes in the presence of
bone loss of 1.27 to 2.00 mm was reported. Complica- labeled precursors such as H-thymidine, H-glucos-
tions varied between 0% and 45.5%, with the most amine, and H-proline to study the neosynthesis of DNA,
common being membrane exposure. The use of a bone glucosaminoglycans (GAG), and collagen proteins, re-
replacement graft resulted in more favorable augmen- spectively. The results demonstrated that gingival
tation of the sites. Distraction osteogenesis resulted in fibroblasts, grown on the matrix membrane, have an
5 to 15 mm of bone gain; however, the complication enhanced ability to accumulate GAG and collagen pro-
rate was higher, up to 75%.69 teins with an increased proliferative activity compared
Canullo and Malagnino70 used DBB in conjunction to e-PTFE membranes.71
with titanium-reinforced e-PTFE membrane around Colangelo et al72 used cross-linked bovine Achilles
implants with bone defects ranging from 2 to 9 mm tendon type I collagen membrane, demonstrating heal-
(average 5.1 mm) at the time of implant placement. ing of the defects with a layer of lamellar bone with
There was a bone height gain of 3 to 9 mm (average osteoblastic activity.
5.3 mm) with a distance between the implant head and Parodi et al73 evaluated ridge expansion using
bone crest varying between −3 to +2 mm. Histologic resorbable collagen membranes with collagen
evaluation was characterized by new bone formation sponges. With less than or equal to 4 mm of baseline
interposed with graft particles. The authors concluded crestal bone width, at the time of implant placement
that this combination can be a predictable procedure there was a mean increase in crestal size by 2.5 mm (3.0
in regenerating bone around implants.70 to 5.5 mm).73
Bunyaratavej and Wang16 supported that mem- Dongieux et al56 used mongrel dogs with fixed
brane exposure was most commonly found in e-PTFE onlay bone grafts either left uncovered, covered with
and highly cross-linked resorbable membranes. resorbable membranes, or covered with e-PTFE mem-
Donos et al7 reported that the most common com- branes. There was no significant difference between
plication was flap dehiscence and/or membrane expo- the three groups in mean volume gain. Histologically,

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the bone regenerated was predominantly cortical with months postoperatively, the results of GBR demon-
minimal cancellous bone.56 strated mean vertical bone gain of 4.7 mm in group A,
Felice et al74 compared two techniques to vertically 5.1 mm in group B, and 7.4 mm in group C. Eighty-five
augment atrophic posterior mandibles with residual implants were left submerged for 6 months. No signifi-
bone height ranging from 5 to 7 mm. Interpositional cant differences were noted statistically between the
bone block graft from the iliac crest or a block of anor- groups in mean marginal bone remodeling 1 to 6 years
ganic bovine bone was used. Two study implants were later (1.01 mm during the first year and 0.2 mm at 6
placed on each side of the mandible. Implants were years).77
submerged and left to heal for 4 months. No statistical Similar results were reported in a case report using
difference was found between the two groups, with the rhPDGF-BB in addition to the bovine bone and autoge-
autogenous group demonstrating 5.1 mm bone gain nous particles. Without the use of autogenous particu-
and 6.2 mm with the bovine bone. The complications late grafts, vertical bone gain over 4 mm seemed
were not significantly different.74 impossible as stated by Urban et al78 and Simion et al.79
Caldwell et al75 used dermal allograft in horizontal Sterio et al80 evaluated bovine pericardium mem-
augmentation procedures with either FDBA alone or in brane in combination with FDBA in horizontal defects
combination with autogenous graft in a 1:1 ratio. The before implant placement. A reentry surgery was per-
surgical technique included cortical perforations, and formed 6 months later showing an average gain of
the membrane was fixed with titanium tacks. At the 2.61 mm. The mean percentage of material resorption
reentry surgery, there was no statistically significant was measured radiographically between 33.7% and
difference between the two groups. The FDBA alone 59.4%, and a high percentage (58%) of vital bone was
group demonstrated bone gain of 3.33 ± 0.83 mm, and measured histomorphometrically.80
the combination group 3.09 ± 0.63 mm.75 Cordaro et al81 used bone blocks harvested from the
Fontana et al76 conducted a study in which the test mandibular ramus or symphysis, which were placed as
group was grafted using titanium-reinforced e-PTFE lateral or vertical onlay grafts fixed with titanium
and allogeneic graft, and the control group with titan- screws. The lateral augmentation areas showed a graft
ium-reinforced e-PTFE membrane and autogenous resorption by the time of implant placement from a
graft. Tenting screws were placed vertically and left to mean of 6.5 ± 0.33 mm to a mean of 5.0 ± 0.23 mm
protrude 3 to 6 mm from the alveolar crest. The results (23.5% resorption). The vertical augmentation areas
yielded bone regeneration of 4.7 mm in the test group showed a graft resorption by the time of implant place-
with 1.26 mm marginal bone loss around implants. In ment from 3.4 ± 0.66 mm to 2.2 ± 0.66 mm (42%
the control group, the mean bone regeneration was resorption). Mandibular sites showed higher graft
found to be 4.1 mm with marginal bone loss around resorption than the maxillary sites.81
implants being 0.84 mm. Histologic findings showed Machtei82 showed that membrane exposure during
trabecular bone formation with varying degrees of GBR had six times more detrimental effect compared to
maturation and mineralization in both groups.76 membrane exposure during GTR. These results are
Urban et al77 treated 35 patients with 36 three-di- based on two clinical studies only. The membranes
mensional defects, ranging from 2 to 12 mm, using were not trimmed as desired for close adaptation to the
e-PTFE membranes and combination of particulate bone, and they were placed in close proximity to the
autografts with anorganic bovine bone. Patients were adjacent teeth not leaving enough space for reattach-
divided in three groups: (i) single missing teeth (group ment of the flap. The second concern has to do with
A), (ii) multiple missing teeth (group B), and (iii) combi- the expected regeneration around polished titanium
nation of sinus and vertical augmentations procedures surfaces.82
performed simultaneously (group C). Six to nine

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Donos et al7 evaluated implant outcomes following to use. The most common complication of the nonre-
lateral bone augmentation In the staged approach, 2 to sorbable membranes is exposure, which can lead to
5 years after the placement of the final restoration the infection and subsequent premature removal of the
survival rate ranged between 93.3% and 98%. For membrane. In both types of membranes, exposure has
implant placement with simultaneous GBR, the survival a detrimental effect on the final outcome, and there-
rate ranged between 76.8% and 96.1% after 5 years, fore tension-free closure such as buccal periosteal and
with the maxilla showing significantly lower survival mylohyoid releases should be considered when per-
rates. All graft materials demonstrated a percentage of forming these procedures. In combination defects,
resorption which did not prevent the placement of the both types of membranes may result in a successful
implants.7 outcome as long as the space is maintained either via
Esposito et al,6 in a Cochrane systematic review, tenting screws or the membrane itself.
concluded that for horizontal or vertical augmentation
procedures, (i) complications are common, (ii) various
techniques are available with distraction osteogenesis
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doi: 10.3290/j.qi.a37133 17

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