Vol. 109 No.

6 June 2010

ORAL AND MAXILLOFACIAL IMPLANTS

Guided bone regeneration using a titanium-reinforced ePTFE

membrane and particulate autogenous bone: the effect of
smoking and membrane exposure
Laura T. Lindfors, DDS,a Ellen A.T. Tervonen, DDS, PhD,b
George K.B. Sándor, MD, DDS, PhD, FRCDC, FRCSC, FACS,c and
Leena P. Ylikontiola, MD, DDS, PhD,d Oulu and Tampere, Finland, and Toronto, Canada
UNIVERSITY OF OULU, OULU UNIVERSITY HOSPITAL, UNIVERSITY OF TORONTO, AND UNIVERSITY
OF TAMPERE

Objectives. The objectives of this study were to describe and evaluate treatment outcomes achieved using guided
bone regeneration (GBR) with autogenous bone grafting, particularly the effect of smoking and membrane exposure.
Study design. Twenty-seven bone augmentations were carried out using intraorally harvested particulate bone grafts
covered by titanium-reinforced ePTFE membranes. Healing events were monitored and treatment outcomes were evaluated.
Results. Twenty-three (85%) augmentations were successful and 4 (15%) were unsuccessful. Augmentations performed
in nonsmokers were successful in 95% of cases, whereas the success rate in smokers was 63%. There were 4 (15%)
cases of membrane exposure, but none affected the final outcome. Signs of soft tissue inflammation were present in 10
(37%) of the augmentation sites, more often in smokers (75%) than in nonsmokers (21%). This difference was
statistically significant (P ⫽ .008).
Conclusions. The results of this study support the use of this technique in the augmentation of resorbed alveolar
processes. Smoking was associated with poor treatment outcomes in this study. Membrane exposures did not seem to
affect outcomes. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;109:825-830)

The alveolar process resorbs following tooth loss, pos-
sibly leading to alveolar defects with insufficient bone
for the placement of dental implants. Localized alveolar
bone defects must be regenerated with reconstructive
surgery to allow the placement of an endosseous im-
plant in an esthetically and functionally favorable po-
sition with good long-term prognosis.1 The combina-
tion of autografts and expanded polytetrafluoroethylene
a
Junior Researcher, Department of Oral and Maxillofacial Surgery
and Department of Periodontology and Geriatric Dentistry, Institute
of Dentistry, University of Oulu, Oulu, Finland.
b
Professor, Department of Periodontology and Geriatric Dentistry,
Institute of Dentistry, University of Oulu, and Oral and Maxillofacial
Department, Oulu University Hospital, Oulu, Finland.
c
Professor and Head of Oral and Maxillofacial Surgery, University of
Toronto, Toronto, Canada; Professor of Tissue Engineering, Regea
Institute for Regenerative Medicine, University of Tampere, Tam-
pere, Finland; and Docent in Oral and Maxillofacial Surgery, Uni-
versity of Oulu, Oulu, Finland.
d
Assistant Professor, Oral and Maxillofacial Surgery, Institute of
Dentistry, University of Oulu, and Oral and Maxillofacial Depart-
ment, Oulu University Hospital, Oulu, Finland.
Received for publication Oct 29, 2009; returned for revision Nov 30,
2009; accepted for publication Dec 23, 2009.
1079-2104/$ - see front matter
© 2010 Mosby, Inc. All rights reserved.
doi:10.1016/j.tripleo.2009.12.035
(ePTFE) membranes is one documented surgical tech-
nique for localized ridge augmentation using block2 or
particulate autografts.3-6 This combination is technique
sensitive, requiring meticulous membrane application
and soft tissue handling.1
Autogenous bone graft material supports the overly-
ing membrane and maintains space beneath the mem-
brane. In addition, the autograft serves as an osteocon-
ductive scaffold for bone matrix deposition, with some
osteoinductive properties, and contains some osteo-
genic cells. New bone formation is induced by osteo-
blasts, osteoblast precursor cells, and growth factors
that are transferred to the augmentation site along with
the grafted bone matrix. The ePTFE membrane serves
as an inert physical barrier preventing the ingrowth of
fibroblasts from the overlying mucosa while allowing
osteogenic and angiogenic cells to migrate into the
defect area.2 The membrane also stabilizes the bone
graft and the blood clot and protects the graft from
resorption.2,7-9 Titanium-reinforced ePTFE membrane
can be adapted to the desired shape above a defect and
has good space-maintaining properties.
The ePTFE membrane is a relatively large foreign
body and therefore it is likely that changes in wound
healing can be expected. This study monitored the

825

826 Lindfors et al.
Table I. The reasons for tooth losses
The reason for tooth loss n %
Trauma 14 51.9
Congenitally missing 5 18.5
Root resorption 4 14.8
Periapical process 2 7.4
Endodontic complication 2 7.4
healing-associated events in 26 partially edentulous
patients in whom guided bone regeneration (GBR) ther-
apy using titanium-reinforced ePTFE membranes was
performed. The aim of this article was to evaluate the
healing process and treatment outcomes.
MATERIAL AND METHODS
A total of 27 alveolar crest augmentations were per-
formed in the Oral and Maxillofacial Department of the
Oulu University Hospital between 1998 and 2008 on 26
consecutive partially edentulous patients. One subject
had 2 augmentations performed at separate sites during
the same surgery. There were 18 females and 8 males,
ranging in age from 17 to 68 years at the time of
surgery. Subjects were classified as ASA I or II status
(American Society of Anesthesiologists Classification).
The reasons for tooth loss are presented in Table I. The
augmentations were performed using a GBR technique
in which particulate bone graft was harvested in-
traorally using a round bur and a bone suction trap
(CSMT, Mississauga, Ontario, Canada) and covered
with a titanium-reinforced ePTFE membrane (Gore-
Tex; W. L. Gore & Associates, Inc., Flagstaff, AZ).
Bone substitute materials were not used. Seven subjects
with 8 augmentation sites (29.6%) admitted to being
smokers.
The data were gathered retrospectively from patient
records in the Oulu University Hospital. Statistical
analyses were performed using chi-square tests with
SPSS 16.0 for Windows (SPSS Inc., Chicago, IL). The
augmentation procedures were performed under local
anesthesia with preoperative oral sedation using mida-
zolam (7.5 mg). In one case nitrous oxide sedation was
used as well.
The amount of bone required and the shape of the
atrophic alveolar crest had been estimated clinically
and radiologically before the operation. A mucoperios-
teal flap was first raised at the site of augmentation (Fig.
1, A) and then at the donor site. The required amount of
particulate bone autograft was harvested from mandib-
ular donor sites using a round bur and a bone suction
trap (Fig. 1, B). The augmentation sites were allowed to
heal before implantation in 24 (88.9%) cases. In the
other 3 (11.1%) cases implantation was done synchro-
nously with augmentation.
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June 2010
Twenty-four (88.9%) augmentations were performed
in the esthetic region of the maxilla and 3 (11.1%)
augmentations in the mandibular premolar-molar re-
gion. In 20 (74.1%) cases the bone graft was placed at
a single tooth augmentation site, in 5 (18.5%) cases
augmentations were performed at sites of 2 missing
teeth, and in 2 (7.4%) cases 3 teeth were missing at the
augmentation site.
The cortical bone of the augmentation site was per-
forated with a bur in 20 cases (74.1%) to improve blood
flow into the graft area. Bone graft material was cov-
ered with a titanium-reinforced ePTFE membrane
(Gore-Tex) that had been cut and formed to the shape
of the future alveolar crest (Fig. 1, C). The membrane
was fixed to the bone with tacks or screws. The mem-
brane was cut so there was a 2- to 3-mm distance
between it and the neck of the adjacent teeth so as to
allow the supra-alveolar fibers to adhere (Fig. 1, D).
The periosteum was released to allow tension-free clo-
sure of the flap over the augmentation area.
Postoperatively, ibuprofen 400 to 800 mg ⫻ 3 to 4
was prescribed for analgesia in most cases. Addition-
ally, some patients received a combination of acetamin-
ophen 500 mg and codeine 30 mg. After the operation,
chlorhexidine-rinsing with Corsodyl 0.2% (SmithKline
Beecham Consumer Healthcare, Maidenhead, England)
was recommended twice a day until the first follow-up
visit. Thereafter, subjects with membrane exposures or
signs of soft tissue inflammation rinsed as required.
Antibiotics were prescribed pre- and postoperatively to
prevent wound infection and promote healing.
Patients had follow-up visits at 10 days after surgery
and as required by individual patients afterward. In 20
(74.1%) augmentations missing teeth were replaced
during the bone graft healing with a temporary pros-
thesis designed to avoid loading of the bone graft.
The treatment was considered successful if an im-
plant could be placed in the augmentation area in an
esthetically and functionally acceptable position (Fig.
1, E).
RESULTS
Twenty-three (85.2%) augmentations were success-
ful and 4 (14.8%) were unsuccessful. Augmentations
performed in nonsmokers were successful in 94.7%,
whereas the success rate in smokers was 62.5% (Table
II). The difference in the success rates between smokers
and nonsmokers was statistically significant (chi-square
test, P ⫽ .031).
Membranes were removed on average 6.3 months
postoperatively. Healing of the augmented sites was
uneventful in 13 (48.1%) cases. Membranes became
exposed in 4 (14.8%) cases (Fig. 2), 2 exposures
being associated with a thin tissue phenotype. Two
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Volume 109, Number 6 Lindfors et al. 827

Fig. 1. A, Mucoperiosteal flap elevated at the augmentation site. B, Bone graft harvested from mandibular donor site using a bur
and a bone suction trap. C, Particulated bone autograft harvested from mandible adapted to the augmentation site. D, Bone graft
covered with a titanium-reinforced ePTFE membrane anchored to the bone with fixation tacks. Notice the 2- to 3-mm distance
between the edge of the membrane and the necks of the adjacent teeth. E, Dental implant in place.

exposed membranes were managed with chlorhexi-
dine-rinsing or brushing with chlorhexidine gel
throughout the healing period. One exposed mem-
brane was covered with a connective tissue graft and
the exposed edges of another membrane were
trimmed. Regardless of the exposures, none of the
membranes were removed prematurely and in all
cases dental implant placement was successful. The
surgical site did not become clinically inflamed in
any of these cases. None of the subjects with exposed
membrane were smokers.
Signs of soft tissue inflammation including redness,
exudate formation, or fistula were present in 10 (37.0%)
augmentation sites (Fig. 3). The rate of inflammation
was greater in smokers than in nonsmokers and this
difference was statistically significant (75.0% versus
21.1%, P ⫽ .008) (Table III).
Resolution of inflammation occurred in 7 cases and
in all of these there was sufficient bone for implanta-
tion. Augmentations were unsuccessful in 4 cases. In 3
of these the membrane was removed prematurely be-
cause of infection of the surgical site. In the remaining

828 Lindfors et al.
Table II. Cross-tabulation of smoking and treatment
success
Treatment success, n (%)
Unsuccessful Successful
Nonsmoker 1 (5.3) 18 (94.7)
Smoker 3 (37.5) 5 (62.5)
Total 4 (14.8) 23 (85.2)
Chi-square test P ⫽ .031.
Fig. 2. Small palatal exposure of an ePTFE membrane.
case the bone graft did not mature. The patients were
smokers in 3 of the 4 unsuccessful cases.
Two of the 4 unsuccessful cases had a temporary
bridge that did not load the grafted area. The 2 other
unsuccessful cases had no temporary prosthesis at all.
A total of 29 implants were inserted in the 23 suc-
cessfully augmented sites. The time between augmen-
tation and implant placement averaged 8.7 months,
excluding the 3 cases where the implant had been
placed concurrently with the augmentation operation.
DISCUSSION
One of the main findings in this study was that
smoking influences the healing of GBR. All except one
augmentation (94.7%) performed in nonsmokers were
successful, whereas the success rate in smokers was
only 62.5%. This difference was statistically significant
(P ⫽ .031). Toxic by-products, including nicotine, car-
bon monoxide, and hydrogen cyanide, have been im-
plicated as risk factors for impaired wound healing.10
Smoking is known to hinder bone revascularization
because of its increasing effect on vasoconstriction.10
Smoking also disturbs the function and metabolism of
fibroblasts11 and polymorphonuclear leukocytes.12 Fur-
thermore, nicotine affects bone metabolism by slowing
the formation of osteoblasts and decreasing the number
of osteoclasts.13 Smoking also increases the likelihood
of subgingival infection with certain periodontal patho-
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June 2010
Total
19 (100.0)
8 (100.0)
27 (100.0)
Fig. 3. Inflammation localized to an area overlying a loos-
ened fixation tack.
Table III. Cross-tabulation of smoking and inflamma-
tion of the surgical site
Inflammation of the surgical site, n (%)
Absent Present Total
Nonsmoker 15 (78.9) 4 (21.1) 19 (100.0)
Smoker 2 (25.0) 6 (75.0) 8 (100.0)
Total 17 (63.0) 10 (37.0) 27 (100.0)
Chi-square test P ⫽ .008.
gens.14 Cigarette smoking is a potentially controllable
risk factor, but no data exist on the length of time
before patients should stop smoking and what effect the
timing of smoking cessation has on healing. Although
clinical experience seems to support smoking cessation
months before surgery, in periodontal tissues the half-
life of smoking effects has been estimated to be 1.5
years (95% confidence interval [CI] 0.5-2.5 years).15
Smoking was recorded as a dichotomous variable
(smoker/nonsmoker) and the history of smoking was
not registered. Therefore, in this study the dose-depen-
dence between smoking and wound healing could not
be assessed. In view of our results with poorer out-
comes in smokers, the authors feel that specific atten-
tion should be focused on patient selection by counsel-
ing smokers to quit.
Healing was eventful in 14 (51.9%) cases. Even
slight changes in healing were recorded, which could
be one reason why more events were associated with
the GBR technique in this study than reported in earlier
studies.2-4 However, in most cases mucosal inflamma-
tion or membrane exposure did not lead to definite
failure of the augmentation and insertion of an implant
to an esthetic and functional position could still be
attained. In these cases partial or complete removal of
the membrane, removal of a fixation tack, and/or anti-
microbial treatment was performed.
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Volume 109, Number 6 Lindfors et al. 829

The significance of membrane exposure on the out-

come in GBR procedures is somewhat controversial.
Several studies have shown better responses when the
membranes remained submerged compared with those
that became exposed during healing,16-18 whereas ac-
cording to some results membrane exposures had no
influence on the healing of the surgical site.19 In the
current study, implantation could be performed at all
sites, despite membrane exposures. The removal of the
membrane after wide exposure has been recommended
to avoid infection.20 Bacteria have been shown to be
able to penetrate through an exposed ePTFE membrane
within 4 weeks despite the use of daily chlorhexidine
application.21 In this study the exposure of ePTFE
membrane did not lead to clinically observed inflam-
mation at the surgical site. Two of the 4 exposed
membranes remained exposed to the oral cavity until
the end of the planned augmentation phase. Both of the
exposures were detected 2 weeks after the operation.
Both these patients used chlorhexidine throughout the
healing period to avoid inflammation of the site. In the
other 2 exposures, 1 membrane was partially removed
and 1 was covered with a palatal connective tissue
graft. None of the 4 subjects were smokers.
Resolution of inflammation in the augmentation site
occurred in 7 cases and in all of these there was
Fig. 4. A, Titanium-reinforced ePTFE membrane overlying
sufficient bone for implantation. Some inflammatory
the alveolar crest giving the underlying bone graft support to
reactions may have been the result of a foreign body produce an ideal ridge form. B, Titanium-reinforced ePTFE
reaction induced by the membrane itself or the result of membrane has been removed and resulted in an ideally
a loosened fixation tack. In 3 cases a fistula at the shaped alveolar process.
surgical site was located over the area of a loosened or
detached fixation tack. To reduce the risk for surgical
site infection and membrane exposure, the membrane
was cut and fixed so that there was a 2- to 3-mm pregnant, which postponed the implantation and in an-
distance between it and the neck of the adjacent teeth so other case the patient missed follow-up appointments
as to allow the supra-alveolar fibers to adhere. and postponed the implantation time repeatedly.
Of the 4 failed cases, 2 patients wore fixed temporary The results of this study support the use of the GBR
prostheses that did not load the reconstructed sites. The technique combining particulate bone graft with a tita-
other 2 failed cases did not have any temporary pros- nium-reinforced ePTFE membrane in the augmentation
thesis. The failed cases were not statistically related to of resorbed alveolar processes. Smoking was associated
temporary prosthesis wear. with poor treatment outcomes in this study. Membrane
Titanium-reinforced ePTFE membranes were used to exposures did not seem to affect outcomes.
maintain the space under the membrane and provide a
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Reprint requests:
Laura Lindfors, DDS
University of Oulu
Department of Oral and Maxillofacial Surgery
PL 5281
FIN-90014 Oulun yliopisto, Finland
lauralindf@gmail.com