DENTAL IMPLANTS

J Oral Maxillofac Surg

70:141-148, 2012

Trans-Sinus Dental Implants, Bone

Morphogenetic Protein 2, and Immediate
Function for All-on-4 Treatment of Severe
Maxillary Atrophy
Ole T. Jensen, DDS, MS,* Jared Cottam, DDS, MD,†
Jason Ringeman, DDS, MD,‡ and Mark Adams, DDS, MS§

Purpose: The aim of this study was to evaluate the clinical outcomes of trans-sinus dental implant placement by
use of bone morphogenetic protein 2 (BMP-2) grafting and immediate functional loading by the all-on-4 scheme.
Patients and Methods: After bone reduction to create the all-on-4 shelf or because of severe maxillary
atrophy and prominent sinus anatomy, 10 patients were selected to undergo trans-sinus implant
placement and simultaneous BMP-2 sinus floor grafting for immediate provisional loading. Insertion
torque was measured upon implant placement. Patients were followed up for at least 1 year after final
restoration when either a computed tomography scan or panoramic radiograph was obtained and analyzed
for the presence of trans-sinus peri-implant bone. Hounsfield units were recorded mid sinus graft.
Results: Of 19 trans-sinus implants, 18 remained integrated at the 1-year follow-up, for a 5.2% failure
rate. All sinus grafts formed bone, with a mean of 460 Hounsfield units. Final fixed prostheses were
completed for all 10 patients.
Conclusion: Trans-sinus dental implant placement with BMP-2 grafting to gain anterior-posterior spread
for immediate function by use of all-on-4 treatment appears to be a viable alternative to the use of
zygomatic implants in the presence of severe maxillary atrophy.
© 2012 American Association of Oral and Maxillofacial Surgeons
J Oral Maxillofac Surg 70:141-148, 2012

Severe maxillary atrophy, in the presence of promi-
nent sinus anatomy, is a significant surgical challenge
for all-on-4 immediate function. We report a new
technique in which posterior implants are angled
forward, passing trans-sinus, to fixate into the lateral
nasal wall. The trans-sinus implants are then grafted
with bone morphogenetic protein 2 (BMP-2) and
placed into immediate function.
Received from ClearChoice Dental Implant Center, Greenwood
Village, CO.
*Oral and Maxillofacial Surgeon.
†Oral and Maxillofacial Surgeon.
‡Fellow.
§Prosthodontist.
Address correspondence and reprint requests to Dr Jensen:
Department of Oral and Maxillofacial Surgery, 8200 East Belleview
Ave, Suite 520E, Greenwood Village, CO 80111; e-mail: ole.
jensen@clearchoice.com
© 2012 American Association of Oral and Maxillofacial Surgeons
0278-2391/12/7001-0$36.00/0
doi:10.1016/j.joms.2011.03.045
Immediate function of trans-sinus dental implants is
facilitated in part by the simultaneous BMP-2 grafting to
the sinus floor.1,2 When atrophy is severe, with less than
5 mm of vertical height, often in the presence of only 2
to 4 mm of alveolar width and prominent sinus cavities,
zygomatic implants or combined alveolar/sinus floor
grafting by use of a delayed loading protocol have been
prescribed.3-8 These patients are often elderly and may
not have adequate bone volume available from maxillo-
facial sites for implant fixation except in the zygoma.9,10
Common use of the zygomatic implant for immediate
function, however, is still lacking, with relatively few
surgeons experienced with the technique.11
Because of this, the question arises— could implants
be placed trans-sinus, bone grafted at the same time, and
then be functionally loaded? The development of BMP-2
as a grafting material known to form de novo bone in
the sinus was tested in this setting over a 2-year period.
The use of BMP-2 for sinus bone grafting is well
established for use in a delayed–implant placement pro-
tocol but has not been well studied for simultaneous
implant placement.12-15 If BMP-2 could be depended on

141
142
FIGURE 1. An axial view taken in the premaxillary area can some-
times show anterior sinus deflections subnasally that present on the CT
scan as round central alveolar defects. (The so-called bullet sign is well
shown in this dentate patient not included in the study.)
Jensen et al. Severe Maxillary Atrophy Treatment. J Oral Maxillofac
Surg 2012.
to form osseointegration, then implant placement with
minimal osseous contact could be performed. However,
the major problem with implant placement in the highly
atrophic maxilla for immediate function is the difficulty
FIGURE 2. Panoramic radiograph of sinus extending forward below nasal fossa into canine lateral region. (This patient is not included in the study.)
Jensen et al. Severe Maxillary Atrophy Treatment. J Oral Maxillofac Surg 2012.
SEVERE MAXILLARY ATROPHY TREATMENT
in gaining any primary stability even if BMP-2 grafting is
done as an adjunct.16
The purpose of this article is to describe the use of
trans-sinus application of posteriorly angled implants for
maxillary all-on-4 immediate function by use of simulta-
neous BMP-2 grafting in the sinus floor and around
exposed implants. The technique is an alternative to the
placement of zygomatic implants.
Patients and Methods
We identified 10 maxillary edentulous Cawood Class
V patients who presented with maxillary sinus pneuma-
tization subnasally.17 Patients were sometimes classified
as having extreme vertical atrophy after alveolar bone
leveling from creation of the all-on-4 shelf.18 Premaxil-
lary pneumatization was observed on cross-sectional
computed tomography (CT) scans as an often circular
sinus defect, described as the “bullet sign” (Fig 1). (This
occurs when the anterior sinus wall extends subnasally,
sometimes even to the central incisor location. The
bullet sign, when present on CT scan, usually extends
just past the canine fossa into the lateral incisor posi-
tion.) Of the 10 patients selected, 3 had extension to the
lateral incisor, 2 had extension distal to the central
incisor, and 5 had extension to the canines (Fig 2).
Other radiographic selection criteria included suf-
ficient pyriform bone mass (ⱖ3 mm in thickness) in
order for apical fixation to be obtained.
JENSEN ET AL 143

All patients underwent the use of the M-4 all-on-4

technique previously described, in which anterior
and posterior implants converge apically, engaging
bone above the nasal floor in the lateral nasal wall (Fig
3).19 (This configuration of implant placement makes
an “M” shape when viewed on orthopantomography,
therefore designating the all-on-4 technique, “M-4.”
The point at which implants converge is designated
the M point, a reference point determined by CT scan
analysis of maximum paranasal bone mass available
for apical implant fixation—an area of bone often left
relatively unresorbed in long-term maxillary atrophy.)
All patients selected for the study had at least 3 ⫻ 3
mm of M-point bone mass available for implant fixa-
tion.19,20
Implants used were internal hex implants (Nobel
Active TiUnite; Noble Biocare, Zurich, Switzerland) or
external hex implants (Nobel Speedy TiUnite; Noble
Biocare) with angled abutments placed the day of
surgery for immediate provisional loading. Implant
diameters were all 4.3 mm except in 1 case where a
3.5-mm diameter was used. Implant lengths ranged
from 15 to 18 mm. All patients had 4 implants placed
with efforts made to gain adequate spacing and ante-
rior-posterior spread.21
Surgery was performed in an outpatient setting
with intravenous anesthesia, all patients being classi- FIGURE 3. A, B, C, Once the sinus is elevated and the membrane
reflected posteriorly, the trans-sinus implant can be placed, engag-
fied as American Society of Anesthesiologists status I ing lateral nasal bone.
or II. We used a crestal incision with a posterior Jensen et al. Severe Maxillary Atrophy Treatment. J Oral Maxil-
lateral release permitting lateral access to the sinus lofac Surg 2012.
cavity for sinus membrane elevation along the ante-
rior sinus wall. Results
Implants were placed with bicortical stabilization
to engage the M point with exposed trans-sinus im- Table 1 describes the radiographic and clinical
plant threads grafted with 1.5 mg of recombinant findings at 6 weeks (periapical radiographs) and 12
human BMP-2 bovine collagen, generally by use of a months (panoramic radiographs or CT scans) post-
small kit divided in half for each sinus but sometimes operatively. In some cases follow-up CT scans were
expanded with particulated autograft or demineral- not obtained. The CT scans indicated that sinus
bone formed in every case and osseointegration
ized allograft by 20% to 25%. (Only the anterior-most
appeared to be present except in 1 patient in whom
portion of the sinus is elevated, leaving a relatively
1 implant failed in the presence of well-formed
small site to graft such that minimal graft material is
bone.
required.) After wound closure, abutments were
When CT scans were obtained (7 of 10 patients),
torqued at 10 to 15 N-cm and the provisional restora- bone density appeared to be at a relatively high level.
tion placed according to the all-on-4 protocol for Recorded Hounsfield units taken mid graft ranged
immediate loading. (The BMP-2 does not participate from 280 to 641 (mean, 460)—a value consistent with
in providing primary implant stability until bone type 2 bone.22,23 One case was not immediately
forms after 4 to 6 months). loaded because of Huntington disease. A total of 19
Six to nine months later, the final restorations were trans-sinus implants were placed (all at second pre-
placed and a follow-up CT scan or panoramic radio- molar sites), with 1 failure by use of the trans-sinus
graph was taken at the 1-year recall appointment, protocol, for a success rate of 94.8%. The failed im-
which was analyzed for the presence of bone, includ- plant never had good primary stability, with an inser-
ing peri-implant Hounsfield units. No core biopsy tion torque of 5 to 10 N-cm.
specimens were taken to verify bone quantity or qual- Although registered periapical radiographs were
ity by histologic analysis. not obtained, it was difficult to find any bone loss in
144 SEVERE MAXILLARY ATROPHY TREATMENT

Table 1. TRANSSINUS BMP-2 GRAFTED ALL ON 4 IMMEDIATE FUNCTION IMPLANTS

Insertion Torque of Sinus

Trans-Sinus Implant Bone Graft
Patient Upper Left Second Upper Right Second Sinus Graft Immediate Consolidation Crestal Bone Crestal Bone
No. Bicuspid Premolar Bicuspid Premolar Material Loading at 12 mo Loss at 6 wk Loss at 12 mo

1 25 N-cm 25 N-cm BMP-2/allograft L, 446

R, 618
2 40 N-cm 30 N-cm BMP-2/allograft L, Yes L, 401
R, Yes R, 463
3 40 N-cm 10 N-cm BMP-2 L, Yes L, 280 1-mm implant
R, Yes R, 459 failed
4 50 N-cm 30 N-cm BMP-2 L, Yes Patient L, 0
R, Yes refused R, 0
another CT
scan
5 50 N-cm 50 N-cm BMP-2/autogenous L, Yes Patient did L, 0
R, Yes not return R, 0
for CT scan
6 10 N-cm 10 N-cm BMP-2/autogenous No No CT scan
Puros (Zimmer due to
Dental, Huntington
Carlsbad, CA) disease
7 15 N-cm 15 N-cm BMP-2/autogenous L, Yes L, 408
Puros R, Yes R, 428
8 40 N-cm 30 N-cm BMP-2/Puros L, Yes L, 522
R, Yes R, 494
9 50 N-cm BMP-2 L, Yes L, 416 L, 0 L, 0
10 50 N-cm 30 N-cm BMP-2/autogenous L, Yes L, 376 L, 0
Puros R, Yes R, 447 R, 0
Jensen et al. Severe Maxillary Atrophy Treatment. J Oral Maxillofac Surg 2012.

any of the implants placed, with 2 implants graded
as having lost 1 mm over the 1-year study period.
Figure 4 shows post-placement periapical radio-
graphs with implants passing through the sinus to
engage lateral paranasal bone mass. In all 19 trans-
sinus implants, insertion torque was relatively low
but still at least 15 N-cm to load. Implants were
immediately loaded with a screw-retained fixed
provisional appliance. All the trans-sinus implants
were angled at 30° and then corrected with 30°
angled abutments.
Twelve-month follow-up CT scans or panoramic
radiographs indicated good bone fill in the trans-
sinus grafting locations (Fig 5), with favorable
Hounsfield units indicating adequate consolida-
tion.24 Continuity of density was excellent at
grafted sites (Fig 6, occlusal view). Trans-sinus in-
tegration appeared to be present radiographically.
Resonance frequency analysis was not performed.
There were no infections, there was 1 case of
implant loss, and there were no sinus complications;
however, implant apices sometimes perforated 1 to 2
mm into the nasal fossa but remained covered with
mucosa. There was no instance of nasolacrimal duct
dysfunction.
Discussion
The use of BMP-2 as simultaneous sinus grafting
material appears to show that a delayed implant place-
ment strategy is not absolutely necessary even when
implants have a relatively poor insertion torque. Im-
mediate function of sinus grafted implants with min-
imal bone available for fixation has not previously
been reported by use of the all-on-4 treatment strat-
egy.25,26 The trans-sinus approach described in this
report provides early evidence that implants grafted
in the sinus with minimal cortical fixation can still be
immediately loaded provided that anterior implants
are well fixed and a cross-arch–stabilized prosthesis is
made. It appears that a minimum of 15 N-cm of
insertion torque is required for loading, as previously
described for single implants.26 To diminish potential
overload of a fragile osseous fixation, anterior occlu-
sion from canine to canine is recommended with the
JENSEN ET AL
FIGURE 4. Once trans-sinus im-
plants are well fixed at the M
point, exposed implant threads
are grafted with BMP-2–impreg-
nated collagen sponge. A, Clin-
ical view of trans-sinus implant.
B, Trans-sinus implants immedi-
ately after grafting with BMP-2
and autograft bone chips. C,
Trans-sinus implant placement on
opposite side with implants well
fixed at M point. D, Postoperative
radiograph obtained on day of
placement showing loaded trans-
sinus implant, which engages
minimal available bone.
Jensen et al. Severe Maxillary At-
rophy Treatment. J Oral Maxillo-
fac Surg 2012.
posterior (premolar) teeth left out of occlusion.27 The
provisional appliances should be made without can-
tilevers. A soft diet is prescribed for 6 weeks to allow
for early osseointegration.
BMP-2 graft material is slow to mineralize, taking 6
months or longer to consolidate.12 In addition, the initial
effect of BMP-2 is osteoclastic, followed by an angioblas-
tic/osteoblastic response.28 Therefore the use of BMP-2
may in some settings provide enough of an early demin-
eralization response in conjunction with the regional
acceleratory phenomenon effect that precarious im-
plants could fail to maintain primary stability.29,30 This,
however, did not occur in our 10 patients. The great
advantage of BMP-2 is its ease of use, well-studied pro-
tocol, and minimal morbidity. For the highly atrophic,
often elderly patient, BMP-2 appears to induce highly
vascularized bone lacking in scar formation or foreign-
body response sometimes observed by the use of alter-
natives.31 The 1 unknown question is, Will osseointegra-
tion develop?
The use of BMP-2 adsorbed onto the implant sur-
face itself has not shown dependable osseointegration
in animal studies.32 The use of BMP-2 to cover ex-
posed implant threads has only been used experimen-
tally until recently.33,34 Clinicians are now reporting
their use of BMP-2 to cover exposed titanium surfaces
with success (J. Berger, oral communication, April 15,
2011).
145
The important factor to stress is the conventional
advantage of not having to go to the zygoma for
fixation in a Class V maxilla because trans-sinus
placement derives about the same anterior-poste-
rior spread as zygomatic implant placement and
often equivalent quantity of bone for osseointegra-
tion. Figure 7 shows a stereolithic model workup of
prospective zygomatic and trans-sinus implant loca-
tions and surgical placement. The model workup
indicates that there is almost no difference in the
position of the posterior implant from trans-sinus
and zygomatic placement. In this case, we found
that the trans-sinus approach developed adequate
anterior-posterior spread and adequate insertion
torque for loading by use of conventional lateral-
access sinus grafting. This has also been the finding
in the vast majority of Class V maxillas treated with
an all-on-4 technique.
In addition, there is a great advantage of using
BMP-2 in the sinus floor because of its prolific
osteogenesis that develops around the implant,
something not shown with allograft or xenograft
alone.30 Although the use of iliac marrow bone has
been shown to develop osseointegration in ex-
posed implant settings such as with “tent-pole”
vertical augmentation of the mandible, the conve-
nient use of BMP-2 permits the operator to avoid
the morbidity of a distant secondary harvest site.35
146 SEVERE MAXILLARY ATROPHY TREATMENT

FIGURE 5. BMP-2 almost always consolidates in the sinus and appears to “osseointegrate” implants. A, Preoperative axial view at site of
implant entry at alveolar crest of residual alveolus toward trans-sinus fixation. B, Six months later, after immediate function, the implant can
be seen passing through the alveolar crest within the sinus with BMP-2–induced bone consolidation. C, Mid–trans-sinus view suggestive of
osseointegration. D, The apical portion passes slightly through the nasal fossa but without mucosa perforation and well within the forming
graft. E, A well-formed nasal floor cortex slightly encroached upon by the implant fixed right at the M point.
Jensen et al. Severe Maxillary Atrophy Treatment. J Oral Maxillofac Surg 2012.

In summary, the treatment of highly resorbed maxil- does need require the use of zygomatic implants in the
las, or those maxillas with reduced bone stock after vast majority of cases. Trans-sinus implants grafted with
creation of the all-on-4 shelf for immediate function, BMP-2 appear to show promise as an alternative tech-
JENSEN ET AL 147

FIGURE 6. An occlusal view, mid sinus, showing the trans-sinus implant well encased in newly formed bone. The implant anterior-posterior
spread at the crest is 14 mm.
Jensen et al. Severe Maxillary Atrophy Treatment. J Oral Maxillofac Surg 2012.

nique to zygomatic implant placement or the use of a Although the approach is technique sensitive and
delayed implant placement strategy as observed in this may not be readily accomplished by every clinician,
short-term study. experience teaches best. For clinicians who rarely

FIGURE 7. A, B, Medical model showing zygomatic implant about half a tooth more posterior than trans-sinus placed fixture (arrow), a
difference that is considered clinically inconsequential.
Jensen et al. Severe Maxillary Atrophy Treatment. J Oral Maxillofac Surg 2012.
148
perform zygomatic fixture placement, this becomes
a reasonable alternative.
It should be emphasized that this is a short-term
follow-up of a limited number of cases performed at a
single center; as such, longer-term study and more
broad use are required to fully validate the technique.
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