Sinus membrane elevation and simultaneous insertion of dental

Periodontology 2000, Vol. 47, 2008, 193–205
Printed in Singapore. All rights reserved
2008 The Authors.
Journal compilation 2008 Blackwell Munksgaard
PERIODONTOLOGY 2000
Sinus membrane elevation and
simultaneous insertion of dental
implants: a new surgical
technique in maxillary sinus
floor augmentation
S T E F A N L U N D G R E N , G I O V A N N I C R I C C H I O , V I N I C I U S C. P A L M A ,
L U I Z A. S A L A T A & L A R S S E N N E R B Y
Endosseous implants are frequently used for prosthetic reconstruction in the edentulous patient.
Sufficient volume and density of the alveolar bone
for implant integration and load bearing are prerequisites for good clinical outcome. Bone resorption
following the extraction of posterior maxillary teeth
sometimes results in severe loss of bone in vertical
and ⁄ or horizontal dimensions, which may compromise the use of dental implants. Various grafting
procedures have been used to establish an adequate
bone volume for the placement of endosseous implants in atrophic posterior maxillae. The most
common technique is augmentation of the maxillary
sinus floor, a technique introduced by Tatum (28)
and modified by Boyne & James (2) and Wood &
Moore (34). Access to the maxillary sinus is obtained
by drilling a bone window in the lateral sinus wall
using a small round bur, while ensuring that the sinus
membrane remains intact. The sinus membrane is
then carefully elevated, mobilized together with the
attached bone window and rotated medially. Maxillary sinus elevation surgery is usually performed in
conjunction with a variety of bone grafting material,
including autogenous bone from the iliac crest (1,
21), the mandibular chin (16, 19, 22, 34), the mandibular ramus (3) or the calvarium (31), as well as
bone substitutes used alone (8, 10) or in combination
with autogenous bone (18, 24, 32, 35).
Summers (26) described an alternative surgical
technique to increase the available bone volume in
the posterior maxilla. Access to the maxillary sinus
floor was achieved through the alveolar ridge, using
various instruments to form and shape a socket. The
sinus membrane was subsequently elevated and a
bone graft was placed prior to the immediate insertion of a titanium implant.
Even if new bone can be obtained after placing
bone grafts in the maxillary sinus, it might not be a
prerequisite for bone formation per se. The mere
lifting of the sinus membrane and the establishment
of a void space with a blood clot may yield new bone,
following the principles of guided tissue regeneration
(4). This concept was supported by a study in which
bone formation was detected at the apical part of
implants protruding into the sinus cavity (5). Spontaneous bone formation at the floor of the maxillary
sinus has also been observed 3 months following the
removal of an intrasinusal cyst (14).
The present article presents the development and
the clinical and histological evaluation of a new
clinical technique for maxillary floor augmentation,
which does not include bone grafting.
Development of a surgical
technique
Bone reformation after sinus membrane elevation is
a novel technique for maxillary sinus floor augmentation and the rationale behind it originated from the
experience with a patient who was referred for augmentation of the right maxillary sinus and a delayed
193
Lundgren et al.
A
B
C
D
E
F
Fig. 1. (A) Orthopantomogram of a
patient planned for removal of a
sinus cyst at 3 months before a sinus
floor augmentation procedure in the
left maxilla. (B) Tomographic section of a showing a sinus cyst. (C) A
replaceable bone window has been
cut with a saw. (D) The sinus cyst is
visible and has been removed. (E)
The lacerated membrane is repaired
using resorbable sutures. (F) The
bone window is placed in position.
placement of implants. During the pre-operative
examination, a mucosal intrasinusal cyst was diagnosed (Fig. 1A,B). As the patient had symptoms of
nasal congestion, the cyst was removed in a separate
session 3 months before sinus floor augmentation
surgery. The 3-month time period was chosen to
ensure healing of the sinus membrane prior to the
bone grafting procedure.
In order to reposition the bone window after the
removal of the cyst, an oblique osteotomy was made
using a microreciprocating saw (Fig. 1C). The osteotomized window was detached by careful dissection
from the sinus membrane and stored in saline. The
sinus membrane around the created window was
dissected free from the sinus wall before a vertical
incision was made in the membrane to reach and
remove the cyst (Fig. 1D). After removal of the cyst,
194
the sinus membrane was lifted from the sinus floor to
make the mucosa as tension-free as possible before
closing with three resorbable sutures (Fig. 1E). The
bone window was then repositioned and the oral
mucosa sutured with single resorbable sutures
(Fig. 1F). Healing of the bone window was completed
within 3 months of the time of the bone grafting
procedure. During preparation of a new bone
window for the sinus floor augmentation, extensive
new bone formation was visible in the area
where the sinus membrane had been elevated
from the floor of the sinus in order to remove the
cyst (14).
Encouraged by this observation, a decision was
made to study, in greater detail, the bone-forming
potential of a sinus membrane elevation technique.
A patient referred for maxillary sinus augmentation
Sinus membrane elevation and simultaneous insertion of dental implants
A
B
C
D
E
F
G
prior to the placement of a single implant was found
to have an alveolar bone height of 7 mm in the future
implant site (Fig. 2A). A mucoperiosteal flap was
raised to expose the lateral wall of the maxillary sinus.
Five holes were drilled using a round bur in order to
outline the planned window, and an oblique osteotomy was made (Fig. 2B). The bone window was detached from the underlying sinus membrane and
stored in saline (Fig. 2C). The sinus membrane was
dissected around the margins of the window and
extended inferiorly to expose the floor of the sinus in
Fig. 2. (A) Orthopantomogram of a
patient planned for a sinus membrane elevation procedure for a
single tooth implant in the right
maxilla. (B) Preparation of a
replaceable bone flap. (C) The bone
flap. (D) An intact sinus membrane.
(E) The membrane is carefully dissected and lifted. (F) Insertion of an
implant that protrudes some 6 mm
into the sinus. (G) Repositioning of
the bone flap.
the edentulous area (Fig. 2D,E). Finally, using a drill
with a diameter of 2.85 mm (without use of a countersink), a 13 · 3.75 mm machined surface implant
(MK III; Nobel Biocare AB, Gothenburg, Sweden) was
inserted into the residual bone (Fig. 2F). The implant
protruded 6 mm into the prepared cavity in the sinus.
Care was taken not to lacerate the elevated sinus
membrane with the tip of the implants during the
insertion. The bone window was re-attached and the
oral mucosa was re-adapted and sutured with single
sutures (Fig. 2G).
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Lundgren et al.
A
A
B
B
Fig. 4. (A) Orthopantomogram of the patient in Fig. 1
after 6 months of healing. (B) Before and after tomography, showing bone formation at the level of the apex of the
implant.
C
drill diameter of 2.85 mm (without use of a countersink) (Fig. 3B). The bone window was replaced and
the surgical site was closed by sutures (Fig. 3C).
Post-operative radiographs of these two patients
showed bone formation around all placed implants
(Fig. 4). Figure 4 is from the first patient; Figure 7 is
from the second patient.
Clinical experience
Fig. 3. (A) Orthopantomogram of a patient planned for
sinus membrane elevation and simultaneous placement
of three implants. (B) Placement of three, 13-mm-long
implants. (C) Repositioning of the bone flap.
The same technique was tested in a second patient,
who received three implants (Fig. 3A). The three
implants, each 13 · 3.75 mm, were placed with a final
196
The satisfactory clinical and radiographic results
obtained prompted a study of 10 additional patients
who received a total of 19 implants (13). The protocol
included sinus membrane elevation and simultaneous placement of implants with an oxidized surface (TiUnite; Nobel Biocare AB) (Fig. 5). The residual
alveolar bone height was measured in situ. Initial
implant stability was optimized by using an underpreparation technique; drilling through the residual
alveolar process using a 2.0 mm twist drill followed
by a 3 mm pilot drill, just enough to enable the
introduction of the implant in the drill canal, followed drilling using a 2.85 mm twist drill, with no use
Sinus membrane elevation and simultaneous insertion of dental implants
Fig. 5. An oxidized implant placed in a membrane elevation site.
of a countersink bur. In patients with low bone
density, implants were placed after the initial preparation using the 2 mm drill. Implant stability was
measured using resonance frequency analysis
(Osstell; Integration Diagnostics AB, Gothenburg,
Sweden). Radiographic bone formation was evident
in all 10 patients, and all 19 implants were stable after
12 months of loading (Figs 6, 8, 9, 10).
These results were confirmed in two other publications, which also obtained bone augmentation in
the maxillary sinus floor by the mere elevation of the
Schneiderian membrane and the simultaneous
placement of endosseous implants beneath the
membrane without adding a graft material. In six
patients with an average of 5 mm residual alveolar
bone, Hatano et al. (9) placed 14 implants (TiUnite
MK III; Nobel Biocare AB) protruding into the sinus
cavity. The cavity produced beneath the sinus
membrane was filled with venous blood drawn from
Fig. 7. Tomography of a patient 6 months after treatment
with three implants in conjunction with a sinus membrane elevation procedure. The section is taken at the
apical level of the implants and shows bone formation
around the implants.
a remote site, and the bone window was repositioned. Bone formation was evident in all six patients,
and the average height of newly formed bone around
the implants was 10 mm. One implant was lost
during the initial healing period, but was immediately replaced by another implant, which then experienced a successful healing (9). Thor et al. (29)
placed 44 endosseous implants (Astra Tech ST Implants; Astra Tech Company, Mölndahl, Sweden) in
20 patients, who presented with an average of 5 mm
residual bone at the floor of the maxillary sinus. One
implant failed to integrate. During a follow-up period
averaging 28 months, no additional implant failed
and new bone formation averaged 7 mm. The
authors found that the greater the length of the
Fig. 6. Tomography of a single implant placement 2 weeks and
6 months after a sinus membrane
elevation procedure. Left: a greyish
area, probably corresponding to a
blood clot, is seen around the implant. Right: evidence of ossification
is seen around the implant.
197
Lundgren et al.
A
B
Fig. 8. (A) Intra-oral radiographs of
a single implant case immediately
(left) and 6 months (right) after a
sinus membrane elevation procedure. Note bone formation. (B)
Computed tomography scans show
evidence of bone formation around
the implant.
implants (i.e. the further the implants protruded into
the secluded space between the floor of the sinus and
the elevated sinus membrane), the more new bone
that was formed (29). They also found that the less
residual bone that was present, the more new bone
was formed (29).
Histological findings from sinus
membrane elevation
The mechanism of bone formation underneath the
elevated sinus membrane is not fully understood.
Because autogenous bone has been considered to be
the gold standard for bone grafting, the clinical
findings of the novel technique presented here need
198
to be supported by histological investigations. Palma
et al. (20) compared the histological outcome of sinus
membrane elevation and simultaneous placement of
implants with and without adjunctive autogenous
bone graft. Each of four tufted capuchin primates
underwent two surgical procedures. Initial surgery
involved bilateral extraction of the maxillary first,
second and third premolars and of the first molar.
The sinus floor augmentation surgery took place after
a dental socket healing of 4 months. A mucoperiosteal flap was raised and a window was prepared in
the lateral wall of the sinus. The window was removed and, after carefully elevating the sinus membrane, two different 3.75 · 8.5 mm Brånemark
(Nobel Biocare AB) implants were placed in each jaw
side, namely a MK III implant with a machined
Sinus membrane elevation and simultaneous insertion of dental implants
Fig. 9. Tomography carried out immediately (above) and
6 months (below) after a sinus membrane elevation,
showing bone formation.
Fig. 10. Tomography of a patient treated bilaterally with
autogenous bone grafting on the left side and membrane
elevation on the right side, after 6 months of healing.
Bone formation is seen at both sides with no apparent
differences.
surface and a TiUnite MK III implant with a titanium
surface enlarged by oxidation (Fig. 11). One sinus was
left to be filled with a coagulum alone, whereas the
contralateral sinus was sacrificed with autogenous
bone harvested from the tibia. The bone windows
were repositioned and the surgical site was closed
with the mucoperisteal flap and sutured. Six months
post-surgery, the animals were sacrificed and the
maxilla was retrieved en bloc for preparation of
ground sections for light microscopy.
Fig. 11. One oxidized and one machined implant placed
into a sinus membrane elevated sinus in a primate.
Fig. 12. Histological section of an oxidized implant
6 months after a sinus membrane elevation procedure.
New bone formation is seen around the implant, which is
lined by a sinus membrane.
The histological examination revealed that the
floor of the sinus provided approximately 2.2 mm
(SD ± 1.1 mm) of cortical bone for primary stability,
while the rest of the implant projected into the sinus
cavity, which after healing was filled with new bone
(Fig. 12). The sinus membrane appeared morphologically intact in most cases and in contact with the
apical surface of the implant (Fig. 13). The membrane-elevated sites showed most new bone at the
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Lundgren et al.
Fig. 13. Light micrograph showing a healthy sinus membrane lining the apex of a titanium implant placed with
simultaneous membrane elevation 6 months earlier.
µm
Fig. 15. Light micrograph showing bone formation towards the surface of a machined implant.
µm
Fig. 14. Light micrograph showing an oxidized implant
placed with sinus membrane elevation. Bone formation is
associated with the sinus membrane and occurs at the
implant surface.
periphery, in contact with the membrane and
sometimes extending downwards towards the centre
of the augmented area (Fig. 14). In grafted sites, bone
tissue was seldom seen lining the sinus membrane at
the uppermost part of the implant. Different patterns
of implant integration could be distinguished for
oxidized and machined implants. While the bone
200
200 µm
Fig. 16. Light micrograph showing bone formation directly at the surface of an oxidized implant.
contact with the machined surface seemed to be a
consequence of bone growth from the periphery onto
the implants (Fig. 15), the oxidized surface showed
Sinus membrane elevation and simultaneous insertion of dental implants
A
B
Fig. 17. (A) Fluoroscopy of an oxidized implant. Calcein staining
demonstrates bone formation directly at the surface of an oxidized
implant at 50 days after insertion.
(B) Staining is mainly seen at a
distance from the surface of a
machined implant.
Bone-to-Implant Contact
(%)
plant surface modification increases the potential for
bone integration of implants placed with no primary
bone contact (Fig. 19A,B).
70
60
50
Animals
Mean
Maintaining an elevated sinus
membrane without the use of
implants
40
30
20
10
0
Machined
Oxidized
Membrane elevation
Machined
Oxidized
Bone Graft
Fig. 18. Bone–implant contacts at machined and oxidized
implants placed with sinus membrane elevation only or
with an adjunctive autogenous bone graft.
direct bone formation without evidence of trabeculae
projection from the surroundings (Fig. 16). The
dynamics of the bone formation process was assessed by using calcein staining and fluoroscopy. For
instance, bone labeling after 50 days was detected
mainly at the implant interface for oxidized implants
(Fig. 17A), but at a distance from the surface of machined implants (Fig. 17B). This was irrespective of
the implants being placed in membrane elevated
sites only or in bone grafted sites. Morphometric
measurements also showed a markedly higher degree
of bone–implant contacts for oxidized than for machined implants. The findings thus indicate that im-
A prerequisite for the present technique is that dental
implants can be placed to serve as tent poles for the
sinus membrane. However, the residual alveolar crest
of many patients is too thin or has too low density to
allow a firm primary stability of implants. It is well
known that bone can be formed in secluded spaces
on a bone surface by using various types of barrier
membranes or other space-making devices. It is
possible that a space-making device can be used also
for bone formation in the maxillary sinus. This
hypothesis was tested in two patients (Cricchio G,
Sennerby L, Lundgren S, unpublished data). A
replaceable bone window was prepared at the lateral
aspect of the maxillary sinus followed by careful
dissection and elevation of the sinus membrane (Fig.
20A–D). A space-making device of about 8 mm, made
using a bioresorbable polymer, was introduced into
the maxillary sinus floor in order to keep up the
elevated membrane. Six months later it was evident
that new bone, 5–6 mm in height, had been formed
at the floor of sinuses in both patients (Fig. 21A–C).
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Lundgren et al.
A
B
Fig. 19. (A) Light micrograph of a
machined implant showing almost
no contacts with the newly formed
bone. (B) An oxidized implant
showing bone formation directly on
the surface.
Although the new bone did not allow for placement
of 10-mm implants with full bone coverage, the 3–
4 mm of new bone made it possible to place implants
with sufficient primary stability to perform a second
sinus membrane-elevation procedure to gain additional bone (13). The results from these two patients
demonstrated that bone can form in a secluded space
in the maxillary sinus without the presence of a
dental implant. However, the findings were disappointing with regard to the amount of bone formed.
It is possible that the space-making polymer material
had in some way inhibited the bone-formation process.
Hypotheses on bone formation in
sinus sites
The studies presented have revealed the formation of
a blood clot around titanium implants placed in the
maxillary sinus. Examinations at 6 to 12 months
post-implant placement showed shrinkage and ossification of the blood clot and the formation of a new
sinus floor. The mechanism of the observed bone
formation in the maxillary sinus remains to be
determined. Knowledge about bone healing has
mainly been gained from studies of healing fractures
and bone defects. However, the maxillary sinus is
unique as it requires bone to be formed beyond the
skeletal contour and not in a bone fracture or defect.
Nonetheless, irrespective of the bone-forming site,
bone formation and healing require the recruitment,
202
migration and differentiation of osteogenic cells. The
lifting of the periosteum may have initiated a
resorption process, exposure of the bone marrow and
access of stem cells to the sinus cavity, a sequence of
events that has been described in animal studies (15,
23). Gruber et al. (6) revealed that the sinus mucosa
contains mesenchymal progenitor cells and cells
committed to the osteogenic lineage, which may
constitute another source of bone-forming cells with
sinus membrane elevation.
One factor contributing to the successful outcome
of the membrane elevation procedure was probably
the use of a replaceable bone window. Technically,
this was achieved by using an oscillating saw with a
thin blade. The margin of the window was first
marked by four to five drill holes. The cutting by the
oscillating saw was then performed in an oblique
direction, resulting in a flanged bone window capable
of being replaced in a stable position. There are
several advantages of using a replaceable bone window. First, soft tissue from the overlaying intra-oral
mucosa does not gain access to the sinus space.
Second, because air cannot pass through the bone
window, which reduces the risk of disturbing the sinus membrane and the underlying blood clot, the
bone window replacement technique may help to reestablish proper pneumatic conditions (30). Third, it
is possible that the surface of the bone window
contributes to a prolonged period of healing, passively by serving as a stabilizing surface for the blood
clot and actively by promoting bone formation
beneath the elevated sinus membrane.
Sinus membrane elevation and simultaneous insertion of dental implants
A
A
B
B
C
Fig. 21. Series of tomographies of the patient in Fig. 20,
(A) immediately after, (B) after 3 months and (C) after
6 months of placement. Note bone formation after 3 and
6 months.
C
D
In sum, these observations described here suggest
that, in spite of an ongoing bone remodelling, bone
deposition is the net outcome of a sinus mucosa
elevation without the use of bone grafts, while a
resorptive process of bone graft particles predominates in bone-grafted sites. The tissue regeneration
field (4, 5, 11–13, 17, 25, 27) has firmly established the
importance of the coagulum and its endogenous
growth factors for bone formation, and it seems that
the osteoinductive properties of a coagulum is limited mainly by lack of a properly maintained space.
While several authors (5, 7, 13, 14, 33) have observed
bone formation after sinus floor augmentation with
no use of bone grafts, Palma et al. (20) were the first
to describe the process histologically and to evaluate
the integration potential of implants with different
surfaces in sinus sites.
Conclusions
The mere elevation of the maxillary sinus membrane
and the simultaneous placement of implants results
Fig. 20. (A) Orthopantomogram of a patient with a very
thin alveolar crest in the left second premolar region. (B)
Preparation of a replaceable bone window. (C) Dissection
and lifting of the sinus membrane in order to place a
space-maintaining device at the floor of the sinus. (D)
Repositioning of the bone window.
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Lundgren et al.
in bone formation and osseointegration. The amount
of bone formation does not seem to differ when
performing sinus membrane elevation with or without bone grafts. Histologically, the de novo bone
tends to be deposited in contact with the sinus
membrane after its elevation, pointing to the osseoinductive potential of the sinus membrane. Surfacemodified implants showed a stronger bone response
than machined implants in maxillary sites receiving
sinus floor augmentation.
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