Sinus Membran Elevation

Sinus membrane elevation andsimultaneous insertion of dentalimplants: a new surgicaltechnique in maxillary sinusfloor augmentation

ST E F A N LU N D G R E N, GI O V A N N I CR I C C H I O, VI N I C I U S C. PA L M A,LU I Z A. SA L A T A & LA R S SE N N E R B Y

Endosseous implants are frequently used for pros-

thetic reconstruction in the edentulous patient.

Sufficient volume and density of the alveolar bone

for implant integration and load bearing are prereq-

uisites 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 compro-

mise the use of dental implants. Various grafting

procedures have been used to establish an adequate

bone volume for the placement of endosseous im-

plants 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. Maxil-

lary 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 man-

dibular 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 inser-

tion 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). Spon-

taneous 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 surgicaltechnique

Bone reformation after sinus membrane elevation is

a novel technique for maxillary sinus floor augmen-

tation and the rationale behind it originated from the

experience with a patient who was referred for aug-

mentation of the right maxillary sinus and a delayed

193

Periodontology 2000, Vol. 47, 2008, 193–205

Printed in Singapore. All rights reserved

� 2008 The Authors.

Journal compilation � 2008 Blackwell Munksgaard

PERIODONTOLOGY 2000

placement of implants. During the pre-operative

examination, a mucosal intrasinusal cyst was diag-

nosed (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 osteo-

tomized 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,

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

C

A

E

F

D

B

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 sec-

tion 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.

194

Lundgren et al.

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 osteot-

omy was made (Fig. 2B). The bone window was de-

tached 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

the edentulous area (Fig. 2D,E). Finally, using a drill

with a diameter of 2.85 mm (without use of a coun-

tersink), 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).

A

C

E

G

B

D

F

Fig. 2. (A) Orthopantomogram of a

patient planned for a sinus mem-

brane 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 dis-

sected and lifted. (F) Insertion of an

implant that protrudes some 6 mm

into the sinus. (G) Repositioning of

the bone flap.

195

Sinus membrane elevation and simultaneous insertion of dental implants

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

drill diameter of 2.85 mm (without use of a counter-

sink) (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

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 simulta-

neous placement of implants with an oxidized sur-

face (TiUnite; Nobel Biocare AB) (Fig. 5). The residual

alveolar bone height was measured in situ. Initial

implant stability was optimized by using an under-

preparation 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, fol-

lowed drilling using a 2.85 mm twist drill, with no use

A

B

C

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.

A

B

Fig. 4. (A) Orthopantomogram of the patient in Fig. 1

after 6 months of healing. (B) Before and after tomogra-

phy, showing bone formation at the level of the apex of the

implant.

196

Lundgren et al.

of a countersink bur. In patients with low bone

density, implants were placed after the initial prep-

aration 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 publi-

cations, 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

a remote site, and the bone window was reposi-

tioned. 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 immedi-

ately replaced by another implant, which then expe-

rienced a successful healing (9). Thor et al. (29)

placed 44 endosseous implants (Astra Tech ST Im-

plants; Astra Tech Company, Molndahl, 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. 5. An oxidized implant placed in a membrane eleva-

tion site.

Fig. 6. Tomography of a single im-

plant 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 im-

plant. Right: evidence of ossification

is seen around the implant.

Fig. 7. Tomography of a patient 6 months after treatment

with three implants in conjunction with a sinus mem-

brane elevation procedure. The section is taken at the

apical level of the implants and shows bone formation

around the implants.

197


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 sinusmembrane 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

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 mucoperio-

steal flap was raised and a window was prepared in

the lateral wall of the sinus. The window was re-

moved and, after carefully elevating the sinus mem-

brane, two different 3.75 · 8.5 mm Branemark

(Nobel Biocare AB) implants were placed in each jaw

side, namely a MK III implant with a machined

A

B

Fig. 8. (A) Intra-oral radiographs of

a single implant case immediately

(left) and 6 months (right) after a

sinus membrane elevation proce-

dure. Note bone formation. (B)

Computed tomography scans show

evidence of bone formation around

the implant.

198

Lundgren et al.

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.

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 morpho-

logically intact in most cases and in contact with the

apical surface of the implant (Fig. 13). The mem-

brane-elevated sites showed most new bone at the

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.

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.

199


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

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

Fig. 13. Light micrograph showing a healthy sinus mem-

brane lining the apex of a titanium implant placed with

simultaneous membrane elevation 6 months earlier.

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.

µm

Fig. 15. Light micrograph showing bone formation to-

wards the surface of a machined implant.

200 µm

Fig. 16. Light micrograph showing bone formation di-

rectly at the surface of an oxidized implant.

200

Lundgren et al.

direct bone formation without evidence of trabeculae

projection from the surroundings (Fig. 16). The

dynamics of the bone formation process was as-

sessed 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 ma-

chined 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 ma-

chined implants. The findings thus indicate that im-

plant surface modification increases the potential for

bone integration of implants placed with no primary

bone contact (Fig. 19A,B).

Maintaining an elevated sinusmembrane without the use ofimplants

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).

A B

Fig. 17. (A) Fluoroscopy of an oxi-

dized implant. Calcein staining

demonstrates bone formation di-

rectly 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

Animals

0

10

20

30

40

50

60

70

Machined Oxidized

Membrane elevation Bone Graft

Machined Oxidized

(%)

Mean

Fig. 18. Bone–implant contacts at machined and oxidized

implants placed with sinus membrane elevation only or

with an adjunctive autogenous bone graft.

201


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 addi-

tional 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 disap-

pointing 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 pro-

cess.

Hypotheses on bone formation insinus 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 ossi-

fication 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,

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 win-

dow. 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 si-

nus membrane and the underlying blood clot, the

bone window replacement technique may help to re-

establish proper pneumatic conditions (30). Third, it

is possible that the surface of the bone window

contributes to a prolonged period of healing, pas-

sively by serving as a stabilizing surface for the blood

clot and actively by promoting bone formation

beneath the elevated sinus membrane.

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.

202

Lundgren et al.

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 predomi-

nates 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 lim-

ited 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

A

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.

A

B

C

D

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.

203


in bone formation and osseointegration. The amount

of bone formation does not seem to differ when

performing sinus membrane elevation with or with-

out bone grafts. Histologically, the de novo bone

tends to be deposited in contact with the sinus

membrane after its elevation, pointing to the osseo-

inductive potential of the sinus membrane. Surface-

modified implants showed a stronger bone response

than machined implants in maxillary sites receiving

sinus floor augmentation.

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