Guided Bone
Guided Bone
Guided Bone
6 June 2010
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- (ePTFE) membranes is one documented surgical tech-
sibly leading to alveolar defects with insufficient bone nique for localized ridge augmentation using block2 or
for the placement of dental implants. Localized alveolar particulate autografts.3-6 This combination is technique
bone defects must be regenerated with reconstructive sensitive, requiring meticulous membrane application
surgery to allow the placement of an endosseous im- and soft tissue handling.1
plant in an esthetically and functionally favorable po- Autogenous bone graft material supports the overly-
sition with good long-term prognosis.1 The combina- ing membrane and maintains space beneath the mem-
tion of autografts and expanded polytetrafluoroethylene brane. In addition, the autograft serves as an osteocon-
ductive scaffold for bone matrix deposition, with some
a
Junior Researcher, Department of Oral and Maxillofacial Surgery
osteoinductive properties, and contains some osteo-
and Department of Periodontology and Geriatric Dentistry, Institute genic cells. New bone formation is induced by osteo-
of Dentistry, University of Oulu, Oulu, Finland. blasts, osteoblast precursor cells, and growth factors
b
Professor, Department of Periodontology and Geriatric Dentistry, that are transferred to the augmentation site along with
Institute of Dentistry, University of Oulu, and Oral and Maxillofacial
the grafted bone matrix. The ePTFE membrane serves
Department, Oulu University Hospital, Oulu, Finland.
c
Professor and Head of Oral and Maxillofacial Surgery, University of as an inert physical barrier preventing the ingrowth of
Toronto, Toronto, Canada; Professor of Tissue Engineering, Regea fibroblasts from the overlying mucosa while allowing
Institute for Regenerative Medicine, University of Tampere, Tam- osteogenic and angiogenic cells to migrate into the
pere, Finland; and Docent in Oral and Maxillofacial Surgery, Uni- defect area.2 The membrane also stabilizes the bone
versity of Oulu, Oulu, Finland.
d
Assistant Professor, Oral and Maxillofacial Surgery, Institute of
graft and the blood clot and protects the graft from
Dentistry, University of Oulu, and Oral and Maxillofacial Depart- resorption.2,7-9 Titanium-reinforced ePTFE membrane
ment, Oulu University Hospital, Oulu, Finland. can be adapted to the desired shape above a defect and
Received for publication Oct 29, 2009; returned for revision Nov 30, has good space-maintaining properties.
2009; accepted for publication Dec 23, 2009.
1079-2104/$ - see front matter
The ePTFE membrane is a relatively large foreign
© 2010 Mosby, Inc. All rights reserved. body and therefore it is likely that changes in wound
doi:10.1016/j.tripleo.2009.12.035 healing can be expected. This study monitored the
825
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826 Lindfors et al. June 2010
Table I. The reasons for tooth losses Twenty-four (88.9%) augmentations were performed
The reason for tooth loss n % in the esthetic region of the maxilla and 3 (11.1%)
Trauma 14 51.9 augmentations in the mandibular premolar-molar re-
Congenitally missing 5 18.5 gion. In 20 (74.1%) cases the bone graft was placed at
Root resorption 4 14.8 a single tooth augmentation site, in 5 (18.5%) cases
Periapical process 2 7.4 augmentations were performed at sites of 2 missing
Endodontic complication 2 7.4
teeth, and in 2 (7.4%) cases 3 teeth were missing at the
augmentation site.
The cortical bone of the augmentation site was per-
healing-associated events in 26 partially edentulous forated with a bur in 20 cases (74.1%) to improve blood
patients in whom guided bone regeneration (GBR) ther- flow into the graft area. Bone graft material was cov-
apy using titanium-reinforced ePTFE membranes was ered with a titanium-reinforced ePTFE membrane
performed. The aim of this article was to evaluate the (Gore-Tex) that had been cut and formed to the shape
healing process and treatment outcomes. of the future alveolar crest (Fig. 1, C). The membrane
was fixed to the bone with tacks or screws. The mem-
MATERIAL AND METHODS brane was cut so there was a 2- to 3-mm distance
A total of 27 alveolar crest augmentations were per- between it and the neck of the adjacent teeth so as to
formed in the Oral and Maxillofacial Department of the allow the supra-alveolar fibers to adhere (Fig. 1, D).
Oulu University Hospital between 1998 and 2008 on 26 The periosteum was released to allow tension-free clo-
consecutive partially edentulous patients. One subject sure of the flap over the augmentation area.
had 2 augmentations performed at separate sites during Postoperatively, ibuprofen 400 to 800 mg ⫻ 3 to 4
the same surgery. There were 18 females and 8 males, was prescribed for analgesia in most cases. Addition-
ranging in age from 17 to 68 years at the time of ally, some patients received a combination of acetamin-
surgery. Subjects were classified as ASA I or II status ophen 500 mg and codeine 30 mg. After the operation,
(American Society of Anesthesiologists Classification). chlorhexidine-rinsing with Corsodyl 0.2% (SmithKline
The reasons for tooth loss are presented in Table I. The Beecham Consumer Healthcare, Maidenhead, England)
augmentations were performed using a GBR technique was recommended twice a day until the first follow-up
in which particulate bone graft was harvested in- visit. Thereafter, subjects with membrane exposures or
traorally using a round bur and a bone suction trap signs of soft tissue inflammation rinsed as required.
(CSMT, Mississauga, Ontario, Canada) and covered Antibiotics were prescribed pre- and postoperatively to
with a titanium-reinforced ePTFE membrane (Gore- prevent wound infection and promote healing.
Tex; W. L. Gore & Associates, Inc., Flagstaff, AZ). Patients had follow-up visits at 10 days after surgery
Bone substitute materials were not used. Seven subjects and as required by individual patients afterward. In 20
with 8 augmentation sites (29.6%) admitted to being (74.1%) augmentations missing teeth were replaced
smokers. during the bone graft healing with a temporary pros-
The data were gathered retrospectively from patient thesis designed to avoid loading of the bone graft.
records in the Oulu University Hospital. Statistical The treatment was considered successful if an im-
analyses were performed using chi-square tests with plant could be placed in the augmentation area in an
SPSS 16.0 for Windows (SPSS Inc., Chicago, IL). The esthetically and functionally acceptable position (Fig.
augmentation procedures were performed under local 1, E).
anesthesia with preoperative oral sedation using mida-
zolam (7.5 mg). In one case nitrous oxide sedation was RESULTS
used as well. Twenty-three (85.2%) augmentations were success-
The amount of bone required and the shape of the ful and 4 (14.8%) were unsuccessful. Augmentations
atrophic alveolar crest had been estimated clinically performed in nonsmokers were successful in 94.7%,
and radiologically before the operation. A mucoperios- whereas the success rate in smokers was 62.5% (Table
teal flap was first raised at the site of augmentation (Fig. II). The difference in the success rates between smokers
1, A) and then at the donor site. The required amount of and nonsmokers was statistically significant (chi-square
particulate bone autograft was harvested from mandib- test, P ⫽ .031).
ular donor sites using a round bur and a bone suction Membranes were removed on average 6.3 months
trap (Fig. 1, B). The augmentation sites were allowed to postoperatively. Healing of the augmented sites was
heal before implantation in 24 (88.9%) cases. In the uneventful in 13 (48.1%) cases. Membranes became
other 3 (11.1%) cases implantation was done synchro- exposed in 4 (14.8%) cases (Fig. 2), 2 exposures
nously with augmentation. 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- Signs of soft tissue inflammation including redness,
dine-rinsing or brushing with chlorhexidine gel exudate formation, or fistula were present in 10 (37.0%)
throughout the healing period. One exposed mem- augmentation sites (Fig. 3). The rate of inflammation
brane was covered with a connective tissue graft and was greater in smokers than in nonsmokers and this
the exposed edges of another membrane were difference was statistically significant (75.0% versus
trimmed. Regardless of the exposures, none of the 21.1%, P ⫽ .008) (Table III).
membranes were removed prematurely and in all Resolution of inflammation occurred in 7 cases and
cases dental implant placement was successful. The in all of these there was sufficient bone for implanta-
surgical site did not become clinically inflamed in tion. Augmentations were unsuccessful in 4 cases. In 3
any of these cases. None of the subjects with exposed of these the membrane was removed prematurely be-
membrane were smokers. cause of infection of the surgical site. In the remaining
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828 Lindfors et al. June 2010
case the bone graft did not mature. The patients were
smokers in 3 of the 4 unsuccessful cases. gens.14 Cigarette smoking is a potentially controllable
Two of the 4 unsuccessful cases had a temporary risk factor, but no data exist on the length of time
bridge that did not load the grafted area. The 2 other before patients should stop smoking and what effect the
unsuccessful cases had no temporary prosthesis at all. timing of smoking cessation has on healing. Although
A total of 29 implants were inserted in the 23 suc- clinical experience seems to support smoking cessation
cessfully augmented sites. The time between augmen- months before surgery, in periodontal tissues the half-
tation and implant placement averaged 8.7 months, life of smoking effects has been estimated to be 1.5
excluding the 3 cases where the implant had been years (95% confidence interval [CI] 0.5-2.5 years).15
placed concurrently with the augmentation operation. Smoking was recorded as a dichotomous variable
(smoker/nonsmoker) and the history of smoking was
DISCUSSION not registered. Therefore, in this study the dose-depen-
One of the main findings in this study was that dence between smoking and wound healing could not
smoking influences the healing of GBR. All except one be assessed. In view of our results with poorer out-
augmentation (94.7%) performed in nonsmokers were comes in smokers, the authors feel that specific atten-
successful, whereas the success rate in smokers was tion should be focused on patient selection by counsel-
only 62.5%. This difference was statistically significant ing smokers to quit.
(P ⫽ .031). Toxic by-products, including nicotine, car- Healing was eventful in 14 (51.9%) cases. Even
bon monoxide, and hydrogen cyanide, have been im- slight changes in healing were recorded, which could
plicated as risk factors for impaired wound healing.10 be one reason why more events were associated with
Smoking is known to hinder bone revascularization the GBR technique in this study than reported in earlier
because of its increasing effect on vasoconstriction.10 studies.2-4 However, in most cases mucosal inflamma-
Smoking also disturbs the function and metabolism of tion or membrane exposure did not lead to definite
fibroblasts11 and polymorphonuclear leukocytes.12 Fur- failure of the augmentation and insertion of an implant
thermore, nicotine affects bone metabolism by slowing to an esthetic and functional position could still be
the formation of osteoblasts and decreasing the number attained. In these cases partial or complete removal of
of osteoclasts.13 Smoking also increases the likelihood the membrane, removal of a fixation tack, and/or anti-
of subgingival infection with certain periodontal patho- microbial treatment was performed.
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Volume 109, Number 6 Lindfors et al. 829
4. Simion M, Jovanovic SA, Trisi P, Scarano A, Piattelli A. Vertical 16. Moses O, Pitaru S, Artzi Z, Nemcovsky CE. Healing of dehis-
ridge augmentation around dental implants using a membrane cence-type defects in implants placed together with different
technique and autogenous bone or allografts in humans. Int J barrier membranes: a comparative clinical study. Clin Oral Im-
Periodontics Restorative Dent 1998;18:8-23. plants Res 2005;16:210-9.
5. Parma-Benfenati S, Tinti C, Albrektsson T, Johansson C. Histo- 17. Machtei EE. The effect of membrane exposure on the outcome of
logic evaluation of guided vertical ridge augmentation around regenerative procedures in humans: a meta-analysis. J Periodon-
implants in humans. Int J Periodontics Restorative Dent tol 2001;72:512-6.
1999;19:424-37. 18. Simion M, Baldoni M, Rossi P, Zaffe D. A comparative study of
6. Trombelli L, Farina R, Marzola A, Itro A, Calura G. GBR and the effectiveness of e-PTFE membranes with and without early
autogenous cortical bone particulate by bone scraper for alveolar exposure during the healing period. Int J Periodontics Restorative
ridge augmentation: a 2-case report. Int J Oral Maxillofac Im- Dent 1994;14:166-80.
plants 2008;23:111-6. 19. Assenza B, Piattelli M, Scarano A, Lezzi G, Petrone G, Piattelli
7. Antoun H, Sitbon JM, Martinez H, Missika P. A prospective A. Localized ridge augmentation using titanium micromesh.
randomized study comparing two techniques of bone augmenta- J Oral Implantol 2001;27:287-92.
tion: onlay graft alone or associated with a membrane. Clin Oral 20. Verardi S, Simion M. Management of the exposure of e-PTFE
Implants Res 2001;12:632-9. membranes in guided bone regeneration. Pract Proced Aesthet
8. Jensen OT, Greer RO Jr, Johnson L, Kassebaum D. Vertical Dent 2007;19:111-7.
guided bone-graft augmentation in a new canine mandibular 21. Simion M, Trisi P, Maglione M, Piattelli A. Bacterial penetration
model. Int J Oral Maxillofac Implants 1995;10:335-44. in vitro through GTAM membrane with and without topical
9. Jardini MA, De Marco AC, Lima LA. Early healing pattern of chlorhexidine application. A light and scanning electron micro-
autogenous bone grafts with and without e-PTFE membranes: a scopic study. J Clin Periodontol 1995;22:321-31.
histomorphometric study in rats. Oral Surg Oral Med Oral Pathol 22. Merli M, Migani M, Esposito M. Vertical ridge augmentation
Oral Radiol Endod 2005;100:666-73. with autogenous bone grafts: resorbable barriers supported by
10. Li J, Wang HL. Common implant-related advanced bone grafting ostheosynthesis plates versus titanium-reinforced barriers. A pre-
complications: classification, etiology, and management. Implant liminary report of a blinded, randomized controlled clinical trial.
Dent 2008;17:389-401. Int J Oral Maxillofac Implants 2007;22:373-82.
11. Wong LS, Martins-Green M. Firsthand cigarette smoke alters 23. Gielkens PF, Bos RR, Raghoebar GM, Stegenga B. Is there
fibroblast migration and survival: implications for impaired heal- evidence that barrier membranes prevent bone resorption in
ing. Wound Repair Regen 2004;12:471-84. autologous bone grafts during the healing period? A systematic
12. Corberand J, Laharrague P, Nguyen F, Dutau G, Fontanilles M, review. Int J Oral Maxillofac Implants 2007;22:390-8.
Gleizes B, et al. In vitro effect of tobacco smoke components on 24. Hürzeler MB, Quiñones CR, Hutmacher D, Schüpbach P.
the functions of normal human polymorphonuclear leukocytes. Guided bone regeneration around dental implants in the atrophic
Infect Immun 1980;30:649-55. alveolar ridge using a bioresorbable barrier. An experimental
13. Yuhara S, Kasagi S, Inoue A, Otsuka E, Hirose S, Hagiwara H. study in the monkey. Clin Oral Implants Res 1997;8:323-31.
Effects of nicotine on cultured cells suggest that it can influence
the formation and resorption of bone. Eur J Pharmacol 1999;
383:387-93. Reprint requests:
14. Zambon JJ, Grossi SG, Machtei EE, Ho AW, Dunford R, Genco RJ. Laura Lindfors, DDS
Cigarette smoking increases the risk for subgingival infection with University of Oulu
periodontal pathogens. J Periodontol 1996;67(suppl):1050-4. Department of Oral and Maxillofacial Surgery
15. Dietrich T, Hoffmann K. A comprehensive index for the mod- PL 5281
eling of smoking history in periodontal research. J Dent Res FIN-90014 Oulun yliopisto, Finland
2004;83:859-63. lauralindf@gmail.com