JOMI on CD-ROM (1997 © Quintessence Pub. Co.), 1997 Vol. 12, No.

1 (88 - 94): Histologic and Clinical Observations of Resorbable and Nonresor

Histologic and Clinical Observations of Resorbable

and Nonresorbable Barrier Membranes Used in
Maxillary Sinus Graft Containment
Sean P. Avera , DDS, MS/William A. Stampley/Bradley S. McAllister, DDS, PhD

In this study, clinical and histologic responses to a bioresorbable membrane used to obturate
an osteotomy site in the lateral wall of the maxillary sinus and to facilitate graft containment
were examined. Expanded polytetrafluoroethylene (e-PTFE) membranes were used as a
control to compare biocompatibility and resorption characteristics. Twelve sinus
augmentation procedures were performed to facilitate placement of implants in nine patients
with insufficient bone in the edentulous posterior maxillae. In five procedures, the lateral wall
was obturated to ensure graft containment with an e-PTFE membrane; the other seven were
covered with a bioresorbable barrier (poly[lactic acid]). The presence or absence of
inflammation, dehiscence, suppuration, and encleftation were recorded. All patients healed
without complication or adverse biologic reaction to either barrier material. Biopsy specimens
of the graft site were taken from the lateral wall with overlying soft tissue prior to reflection of
the full-thickness flap at stage 2 surgery. Findings suggest that a poly(lactic acid) membrane
can provide results similar to those with e-PTFE membranes for use in lateral obturation
during sinus augmentation.
(INT J ORAL MAXILLOFAC IMPLANTS 1997;12:88–94)
Key words: encleftation, histology, membrane, sinus augmentation

S ince the breakthrough achievements of implant pioneers P.-I. Brånemark et al 1 and Andre
Schroe der et al2 during the late 1960s and 1970s, numerous advancements have occurred in the
field of implant dentistry. No longer is the surgical specialist forced to place implants into only the
available host bone. Current surgical techniques permit optimal implant placement, not only
facilitating prosthetic concerns, but more importantly improving the accessibility for hygiene. These
techniques often include recipient site augmentation using a variety of approaches and materials.
With the use of these techniques, implants can be placed into sites that were previously deemed
inoperable because of inadequate bony anatomy.

The sinus floor augmentation procedure, as first described by Boyne and James in 1980,3 has given
hope to patients who suffer from severely atrophied maxillae. Inadequate alveolar bone mass and pneu
matization of the sinus are frequent findings in edentulous patients, and they have prevented initial im
plant stabilization, which is mandatory for long-term success. Sinus floor augmentation can provide the
necessary bone mass to place and stabilize implants essential for the initial steps leading toward
osseointegration.4 Common materials currently used for maxillary sinus floor augmentation include
autogenous bone grafts, allografts, alloplasts, and xeno grafts.3-7 These materials have been used with
varied success. Several authors4,8 have discussed incomplete regeneration without the concurrent use of
a barrier membrane. Regardless of the type of material used for maxillary sinus floor augmentation,
dislodgment of the graft material is a possible complication. This can lead to further detrimental sequelae

Article Text 1
JOMI on CD-ROM (1997 © Quintessence Pub. Co.), 1997 Vol. 12, No. 1 (88 - 94): Histologic and Clinical Observations of Resorbable and Nonresor

resulting in failure. For example, graft migration and dispersion into the soft tissues can cause scarring
and connective tissue invagination or encleftation.8 Encleftation of connective tissue occurs following
graft displacement. The migrating graft material becomes infiltrated by connective tissue and, as such, is
useless as a site for implant placement (Fig 1).
Encleftation of the sinus can result in possible exposure of the implants, rendering them useless as a
load-bearing entity. In addition, it has been speculated that epithelial remnants trapped in the wound have
caused postoperative maxillary cysts.9 To ensure graft stabilization and minimal loss of osseous volume,
barrier membranes have been utilized to obturate the osteotomy and to confine the graft material to the
sinus cavity until progressive wound healing events can stabilize the graft particles. This prevents graft
displacement and possible soft tissue encleftation into the sinus.
Currently, expanded polytetrafluoroethylene (e-PTFE) membranes are commonly used for this
procedure. For graft stabilization and exclusion of soft tissue during bone regeneration, this material has
its own inherent problems. A second surgical procedure is required for its removal, and removal of this
material by dissection from the reflected flap can at times be laborious and time consuming. Flap
fenestration and consequent maintenance of the e-PTFE membrane for prolonged periods may
compromise the result by bacterial contamination of the site.10 This is especially true with sinus
augmentation.
An alternative material that could negate these obstacles would seem desirable. A bioresorbable
membrane could alleviate these disadvantages, although it is not known what effect a resorbable material
could have on the healing process of a sinus augmentation procedure. The purpose of the present study
was to determine the clinical feasibility of using a bioresorbable poly(lactic acid) (PLA) membrane to
obturate an osteotomy in the lateral wall of the maxillary sinus following augmentation. Histologic and
clinical evaluation and comparison to results from control subjects treated with a non-resorbable e-PTFE
membrane were performed.
Materials and Methods
Patient Selection. Patients were selected for this study from Oregon Health Science University (OHSU)
residency clinics. This project followed OHSU IRB guidelines (IRB approval No. 3859). The patients
presented with edentulous posterior maxillae having bone insufficient to place implants without sinus
augmentation. Patients were free from current sinus pathology as determined by computerized
tomography (CT), clinical examinations, and health questionnaires. Computerized tomography was used
with a radiographic template designed with radiopaque markers that related strategic implant sites to
future prosthetic demands. This radiographic survey was also used to identify possible septa present in
the antrum. All patients were healthy nonsmokers. Nine patients (six women and three men) with a mean
age of 66 years (range, 50 to 78 years) were included in the study (Table 1). Twelve maxillary sinus
augmentation procedures were performed either prior to or concomitant with implant placement. A total
of 30 screw-type endosseous implants were placed. A blinded randomization was performed to decide
which barrier treatment was performed for each of the sinus lift procedures. In two patients, bilateral
procedures were completed with an e-PTFE membrane placed on one osteotomy site and a bioresorbable
membrane placed on the contralateral side.
Surgical Procedure. The surgical technique used in the present study was similar to that de scribed
by Hirsh and Ericsson,11 and the grafting techniques were similar to those described by Smiler et al.4
Two hours preoperatively, patients were given 250 mg of amoxicillin and 125 mg of clavulanic acid

Article Text 2
JOMI on CD-ROM (1997 © Quintessence Pub. Co.), 1997 Vol. 12, No. 1 (88 - 94): Histologic and Clinical Observations of Resorbable and Nonresor

(Aug mentin, SmithKline Beecham, Philadelphia, PA). 12 Immed iately prior to surgery, patients were
instructed to rinse with 0.12% chlorhexidine gluconate for 90 seconds. All patients were treated under
conscious intravenous sedation and local anesthetic. An incision just palatal to the crest of the ridge was
made from the tuberosity, and it was continued anteriorly beyond the anterior border of the sinus. A
vertical releasing incision in the canine fossa facilitated flap reflection and sinus wall access. The
full-thickness mucoperiosteal flap was reflected to the level of the malar buttress, exposing the lateral
wall of the maxilla. A fiberoptic light source was placed against the palate and was angled laterally to
illuminate the antrum. An oval osteotomy was performed using a No. 6 round bur with copious sterile
saline irrigation.
The inferior border of the osteotomy was initiated 2 mm superior to the sinus floor and was continued
through the cortical bone without perforating the schneiderian membrane. Once mobility of the bony
window was achieved, Tatum sinus membrane elevators (Walter Lorenz, Jacksonville, FL) were used to
position the bony window medially and to dissect the schneiderian membrane away from the inferior and
medial wall of the sinus (Fig 2). If implants were to be placed, the recommended drilling sequence was
performed at this time. Graft material consisting of 50% porous resorbable hydroxyapatite (Bio-Oss,
Osteohealth, Shirley, NY) and 50% decalcified freeze-dried bone (Michigan tissue bank, 300 to 500
µm)4 was hydrated with saline and was placed into the sinus under the schneiderian membrane until the
lateral contours of the maxilla were restored (Fig 3). Prior to flap closure, either an e-PTFE membrane
(Gore-Tex, WL Gore, Flagstaff, AZ) or a PLA re sorbable barrier membrane (Guidor USA, Bensen ville,
IL) was placed over the osteotomy site (Fig 4). Interrupted polyglactin 910 sutures were used to achieve
primary closure of the flap.
Postoperatively, patients were given Augmentin three times a day for 10 days, nonsteroidal
anti-inflammatory drugs as needed for pain (200 mg of ketoprofen), and nasal decongestants for 14 days
postoperatively. Sutures were removed after 7 to 10 days, and patients were instructed not to wear any
prosthesis for a minimum of 2 weeks.
Patients were recalled weekly for the first month, every 2 weeks for the second month, and once a
month until stage 2 surgery. Stage 2 surgery was performed 10 to 12 months after sinus augmentation. A
biopsy specimen was taken from the center of the osteotomy site at this time. Subsequently, a
full-thickness flap was reflected to expose the lateral wall for evaluation and membrane removal.
Clinical Evaluation. The surgical sites were evaluated for pain, inflammation, suppuration,
dehiscence, and encleftation. Inflammation was graded as none (0), mild (+), moderate (++), or severe
(+++). Suppuration, dehiscence, and encleftation were ranked dichotomously (+ or –). Although not
graded, presence or absence of pain was recorded.
Histologic Evaluation. The biopsy specimen taken at stage 2 surgery employed a 2-mm diameter
tissue punch (Acuderm, Fort Lauderdale, FL) or a bone marrow biopsy needle (Manan Medical Pro
ducts, Northbrook, IL) and was made through the epithelium over the lateral maxillary wall osteotomy
site, perpendicular to the cortical plate and into the graft site. A core of graft material at least 5 mm in
length with overlying mucosa was taken. This technique provided a histologic view of the osseous
graft–soft tissue interface with minimal distortion (Fig 5). The specimens were then placed in 10%
buffered formalin until histologic preparation was initiated. The samples were decalcified in Kristen
son’s solution for 4 days and were then embedded in paraffin substitute; 4-µm-step serial sections were
stained with either hematoxylin and eosin stain or Masson trichrome stain.

Article Text 3
JOMI on CD-ROM (1997 © Quintessence Pub. Co.), 1997 Vol. 12, No. 1 (88 - 94): Histologic and Clinical Observations of Resorbable and Nonresor

Results
Clinical Findings. Postoperative observation ranged from 10 to 19 months for both groups (Table 1). All
patients experienced uneventful healing during this time period. Slight inflammation was observed at all
sites for the first 2 weeks of healing. This was especially apparent at the wound margins. At stage 2
surgery, after the biopsy had been performed, the full-thickness flap exposing the lateral wall of the
maxillary sinus revealed no evidence of soft tissue encleftation in any of the patients. In no patient was
dehiscence or suppuration observed throughout the healing period. The survival rate of the implants was
90% for the duration of the study.
Histologic Findings. Histologic findings were evaluated with emphasis on the soft tissue–hard tissue
interface. No quantitative histomorphometry was performed; however, a descriptive qualitative
evaluation of the findings for each type of barrier follows:
Samples of e-PTFE Membranes. Biopsy specimens of the e-PTFE samples separated at the
membrane–connective tissue interface during histologic preparation. Tissue samples from the e-PTFE
group showed no appreciable inflammation on either side of the membrane. The membrane was
surrounded on both surfaces by connective tissue. Fibroblasts were present within the stroma. Some
ingrowth of fibrous connective tissue was evident. The fibrous connective tissue observed between the
membrane and the graft material was devoid of inflammatory cells. Fine cancellous bone was present,
and fragments of nonvital bone were seen interspersed within new bone, which exhibited osteocytes
within their lacunae and secondary osteon formation. Osteoblasts surrounded some of the vital bone
fragments; however, they were sparse. Small blood vessels were also apparent. Figure 6 shows a
representative histologic view of this group.
Bioresorbable Samples. These samples were similar to the e-PTFE group in graft and soft tissue
characteristics. The PLA membrane was absent, indicating complete degradation of the device. Fibrous
connective tissue was present with fibroblasts. The graft–connective tissue interface showed no
inflammatory infiltrate. Qualitative evaluation of the specimens revealed a slight invasion of the fibrous
connective tissue into the graft material at the microscopic level, and this appeared to be more extensive
than what was observed in the e-PTFE samples. Fragments of vital and nonvital bone surrounded by
connective tissue were seen at the graft surface. Small blood vessels were also evident. Although few in
number, vital bone fragments were seen with lining cells. Small deposits of osteoid were present, and
giant cells were sparse. Figure 7 shows a representative histologic view of this group.
Discussion
The concept of guided tissue regeneration is a well-established mode of treatment.13,14 Since the first
human trials in the 1980s, there has been widespread use of this technique for the regeneration of tissue
destroyed by periodontal disease. Recently, this technology has been used for additional applications
such as the regeneration of bony defects associated with implant dentistry. 15
The most common material employed for maxillary sinus augmentation, e-PTFE, is nonresorbable,
mandating the eventual removal of the material. However, it has some disadvantages so that it would
seem beneficial to use a resorbable material to possibly eliminate these disadvantages. In the present
study, a comparison between a nonresorbable membrane and a bioresorbable membrane was made in
conjunction with maxillary sinus augmentation. Both the e-PTFE and the PLA materials performed
without negative sequela. Only one site showed persistent clinical signs of inflammation during the
study. This site was in the e-PTFE group, and inflammation was still apparent at the wound margin 3

Article Text 4
JOMI on CD-ROM (1997 © Quintessence Pub. Co.), 1997 Vol. 12, No. 1 (88 - 94): Histologic and Clinical Observations of Resorbable and Nonresor

weeks after surgery. Although histomorphometry was not done on our samples, a slight tendency for
more connective tissue infiltration into the graft material was seen in the PLA samples. The difference
was noticeable only with high magnification, and it was not apparent clinically. This increase in fibrous
connective tissue could result from early dissolution of the PLA membrane, relative to the e-PTFE
membrane. There was no clinical evidence of soft tissue encleftation with either material.
Sinus lift augmentation without the use of barrier membranes may result in soft tissue encleftation.
This can lead to ultimate implant failure. With no large long-term studies evaluating the efficacy of the
sinus augmentation procedure, it is imperative that chances for long-term success be maximized. Place
ment of a membrane over the lateral wall oste otomy site is one technique that will likely enhance bone
quality in this area and, thus, overall long-term success.
It is likely that the lateral wall osteotomy site is one of the last areas to mineralize. Thus, it is a likely
area for immature and poorly mineralized bone during the stage 2 surgical procedure. For this reason, the
lateral wall is the optimal site for biopsy and evaluation of the quality of bone prior to the initiation of
prosthetic procedures. If the quality of bone is sufficient in this location, one might assume that near the
sinus floor (the site most biopsy specimens have been taken as reported in the literature to date) the
quality would be superior. In recent animal sinus lift studies utilizing the chimpanzee in our laboratories,
the bone mineral density was observed to be greater near the floor as compared to the lateral wall
osteotomy. 16 In a preliminary animal study evaluating the PLA membrane for the lateral wall osteotomy
after sinus augmentation in the Rhesus monkey, we observed no significant soft tissue encleftation,
further supporting the findings described in the present study.
The potential for graft displacement external to the sinus exists, even when a membrane is used. For
further stabilization, the membrane may be fixated to bone. If a nonresorbable barrier is desired,
utilization of TefGen membranes (TefGen-USA, Sacramento, CA) or the center of e-PTFE Oval 9
membrane (Gore-Tex, WL Gore, Flagstaff, AZ) makes the dissection process at removal easier. Use of
titanium-reinforced e-PTFE membranes may be employed in cases where the residual ridge is narrow.
Lateral wall osteotomy coverage and ridge augmentation can be accomplished simultaneously with this
technique. Ultimately, we intend to use more robust grafting materials, such as the bone morphogenetic
proteins for the sinus augmentation procedure, which may alleviate the need for membranes altogether. 17
The potential carriers for these recombinant factors may add an additional positive guided bone
regeneration influence and minimize the phenomena of encleftation and graft containment problems.
Extensive studies on bioresorbable barriers indicate that most of the current materials have inherent
problems. The resorptive process will, by definition, have associated with it some inflammatory cellular
response in the surrounding tissue, regardless of whether the material is degraded by hydrolysis or
through enzymatic mechanisms. This inflammatory response should be minimal and reversible, and it
must not be detrimental to the process of regeneration. The process should be controlled so that the
design of the material is maintained during the initial healing period and the function for tissue guidance
is maintained for a sufficient length of time. The membranes made of PLA appear to fit these criteria.
Conclusion
The present study illustrates clinically and histologically that a membrane made of PLA can provide
results similar to those with e-PTFE membranes for use in lateral obturation during sinus augmentation.
The fact that the membrane completely resorbed and no adverse clinical reaction was apparent from our
specimens gives credence to the use of this material in the sinus augmentation procedure. In addition,
patient acceptance and comfort is increased by the fact that a second surgical procedure is negated.

Article Text 5
JOMI on CD-ROM (1997 © Quintessence Pub. Co.), 1997 Vol. 12, No. 1 (88 - 94): Histologic and Clinical Observations of Resorbable and Nonresor

Acknowledgments
Partial funding for this project provided by Guidor USA, Ben sen ville, IL.

Sean P. Avera

Assistant Professor, Department of

Periodontology, Oregon Health Sciences
University, Portland, Oregon.

William A. Stampley

Histotech, Department of Oral Pathology, Oregon

Health Sciences University, Portland, Oregon.

Bradley S. McAllister

Director of Research, Departments of

Periodontology and Oral Molecular Biology,
Oregon Health Sciences University, Portland,
Oregon.

FIGURES

Footnotes 6
Figure 1

Fig. 1 Lack of placement of a barrier membrane has contributed to graft migration and an
encleftation of connective tissue into the maxillary sinus. The result can be insufficient bone
quality for implant placement.

Figure 2

Fig. 2 Osteotomy site with sinus membrane reflected and elevated above the sinus floor.

Figures 7
JOMI on CD-ROM (1997 © Quintessence Pub. Co.), 1997 Vol. 12, No. 1 (88 - 94): Histologic and Clinical Observations of Resorbable and Nonresor

Figure 3

Fig. 3 Graft material and implants in place within the maxillary sinus.

Figure 4

Fig. 4 Bioresorbable membrane in place, obturating the osteotomy site created in the lateral
wall of the maxillary sinus.

Figures 8
JOMI on CD-ROM (1997 © Quintessence Pub. Co.), 1997 Vol. 12, No. 1 (88 - 94): Histologic and Clinical Observations of Resorbable and Nonresor

Figure 5

Fig. 5 Gross specimen obtained from biopsy punch illustrating the presence of graft material
(arrows) and soft tissue (Mu = mucosa) (Masson trichrome stain; magnification u 12).

Figure 6

Fig. 6 Photomicrograph of the membrane–soft tissue junction (arrows) in an e-PTFE sample.

Note lack of inflammatory response (M = membrane; CT = connective tissue; G = graft
material) (Masson trichrome stain; magnification u 125).

Figures 9
JOMI on CD-ROM (1997 © Quintessence Pub. Co.), 1997 Vol. 12, No. 1 (88 - 94): Histologic and Clinical Observations of Resorbable and Nonresor

Figure 7

Fig. 7 Photomicrograph of the junction (arrows) between the bioresorbable membrane and the
graft material (G). Fragments of nonvital bone can be seen immediately adjacent to the
junction. Note the lack of inflammatory response, and the slight infiltration of connective tissue
(CT) in the graft area with lack of inflammatory cells (Masson trichrome stain; magnification u
125).

TABLES

Figures 10
JOMI on CD-ROM (1997 © Quintessence Pub. Co.), 1997 Vol. 12, No. 1 (88 - 94): Histologic and Clinical Observations of Resorbable and Nonresor

Table 1

Histologic and Clinical Observations of Resorbable and Nonresorbable Barrie

1. Brånemark P-I, Breine U, Adell R, Hansson BO, Lindström J, Ohlsson A. Intra-osseous anchorage of dental
prostheses. I. Experimental studies. Scand J Plast Reconstr Surg 1969;3:81–100.
2. Schroeder A, Pohler O, Sutter F. Gewebsreaktion auf ein Titan-Hohlzylinderimplantat mit
Titan-Spritzschichtoberflache. Schweiz Monatsschr Zahnheilk 1976;86:713–727.
3. Boyne P, James R. Grafting of the maxillary sinus floor with autogenous marrow and bone. J Oral Surg
1980;38:613–616.
4. Smiler D, Johnson PW, Lazoda JL, Misch C, Rosnelicht JL, Tatum OH, Wagner JR. Sinus lift grafts and
endosseous implants. Treatment of the atrophic posterior maxilla. Dent Clin North Am 1992;36:151–186.
5. Hürzeler M, Kirsch A, Ackermann K, Quiñones C. Reconstruction of the severely resorbed maxilla with dental
implants in the augmented maxillary sinus: A 5-year clinical investigation. Int J Oral Maxillofac Implants
1996;11:466–475.
6. Moy PK, Lundgren S, Holmes RE. Maxillary sinus augmentation: Histomorphometric analysis of graft
materials for maxillary sinus floor augmentation. J Oral Maxillofac Surg 1993;51:857–862.
7. Wallace S, Froum S, Tarnow D. Histologic evaluation of sinus elevation procedure: A clinical report. Int J
Periodont Rest Dent 1996;16:47–51.

References 11
JOMI on CD-ROM (1997 © Quintessence Pub. Co.), 1997 Vol. 12, No. 1 (88 - 94):

8. Jensen OT. Guided bone graft augmentation. In: Buser D, Dahlin C, Schenk RK (eds). Guided Bone
Regeneration in Implant Dentistry. Chicago: Quintessence, 1994:235–264.
9. Misch CM, Misch CE, Resnik RR, Ismail YH, Appel B. Post-operative maxillary cyst associated with a
maxillary sinus elevation procedure: A case report. J Oral Implantol 1991;17:432–437.
10. Augthun M, Spiekermann H, Stean B. Healing of bone defects in combination with immediate implants using
the membrane technique. Int J Oral Maxillofac Implants 1985;10:421–428.
11. Hirsch JM, Ericsson I. Maxillary sinus augmentation using mandibular bone grafts and simultaneous
installation of implants. A surgical technique. Clin Oral Implants Res 1991;2(2):91–96.
12. Classen DC, Evans RS, Pestotnik SL, Horn SD, Menlove RL, Burke JP. The timing of prophylactic
administration of antibiotics and the risk of surgical-wound infection. N Engl J Med 1992;326:281–286.
13. Nyman S, Lindhe J, Karring T, Rylander H. New attachment following surgical treatment of human
periodontal disease. J Clin Periodontol 1982;9:290–296.
14. Mendieta C, Williams R. Periodontal regeneration with bioresorbable membranes. Curr Opin Periodontol
1994;2:157–167.
15. Lundgren D, Sennerby L, Falk H, Friberg B, Nyman S. The use of a new bioresorbable barrier for guided bone
regeneration in connection with implant installation. Case reports. Clin Oral Implants Res 1994;5:177–184.
16. McAllister B, Margolin M, Taylor M, Cogan A, Diana K. Bone formation following sinus augmentation with
rhOP-1 in the chimpanzee. 1997 (in press).
17. Margolin M, Taylor M, Cogan A, McAllister B. Residual lateral wall defects following sinus augmentation
with rhOP-1. J Dent Res 1997;76(special issue):1232.

References 12