Maxillary sinus vascular anatomy and its relation to sinus lift surgery

Gabriele Rosano
Silvio Taschieri
Jean-François Gaudy
Tommaso Weinstein
Massimo Del Fabbro
Maxillary sinus vascular anatomy and its
relation to sinus lift surgery
Authors’ affiliations:
Gabriele Rosano, Silvio Taschieri, Tommaso Weinstein,
Massimo Del Fabbro, Dental Clinic, Department of
Health Technologies, Galeazzi Orthopaedic Institute,
University of Milan, Milan, Italy
Jean-François Gaudy, Department of Cranial
Cervicofacial Anatomy, Faculty of Medicine,
University René Descartes–Paris5,Paris,France
Corresponding author:
Dr Gabriele Rosano
Università degli Studi di Milano
Dipartimento di Tecnologie per la Salute
IRCCS Istituto Ortopedico Galeazzi
Via R. Galeazzi, 4
20161 – Milano
Italy
Tel.: þ 39 02 50319950
Fax: þ 39 02 50319960
e-mail: gabriele.rosano@unimi.it
Key words: haemorrhage risk, maxillary sinus vascularisation, sinus lift surgery
Abstract
Objectives: To investigate the prevalence, location, size and course of the anastomosis between the
dental branch of the posterior superior alveolar artery (PSAA), known as alveolar antral artery (AAA),
and the infraorbital artery (IOA).
Material and methods: The first part of the study was performed on 30 maxillary sinuses deriving from
15 human cadaver heads. In order to visualize such anastomosis, the vascular network afferent to the
sinus was injected with liquid latex mixed with green India ink through the external carotid artery. The
second part of the study consisted of 100 CT scans from patients scheduled for sinus lift surgery.
Results: An anastomosis between the AAA and the IOA was found by dissection in the context of the
sinus anterolateral wall in 100% of cases, while a well-defined bony canal was detected
radiographically in 94 out of 200 sinuses (47% of cases).
The mean vertical distance from the lowest point of this bony canal to the alveolar crest was
11.25 2.99 mm (SD) in maxillae examined by CT. The canal diameter was o1 mm in 55.3% of cases,
1–2 mm in 40.4% of cases and 2–3 mm in 4.3% of cases.
In 100% of cases, the AAA was found to be partially intra-osseous, that is between the Schneiderian
membrane and the lateral bony wall of the sinus, in the area selected for sinus antrostomy.
Conclusions: A sound knowledge of the maxillary sinus vascular anatomy and its careful analysis by CT
scan is essential to prevent complications during surgical interventions involving this region.
Date:
Accepted 7 July 2010
To cite this article:
Rosano G, Taschieri S, Gaudy J-F, Weinstein T, Del Fabbro
M. Maxillary sinus vascular anatomy and its relation to sinus
lift surgery.
Clin. Oral Impl. Res. xx, 2010; 000–000.
doi: 10.1111/j.1600-0501.2010.02045.x
Sinus augmentation using autogenous bone or
bone substitutes is a safe procedure with high
predictability (Wallace & Froum 2003; Aghaloo
& Moy 2007; Del Fabbro et al. 2008; Pjetursson
et al. 2008) for the rehabilitation of severely
atrophic posterior maxillae.
However, given the extensiveness of the maxillary
vascular network, it is not infrequent to run
into vascular complications that may compromise
the outcome of surgery. For example, severe
haemorrhage may occur as a result of arterial
injury (Chanavaz 1996).
A sound knowledge of the arterial supply of the
maxillary sinus is mandatory for surgical procedures
involving this area, such as sinus floor
elevation and implantation of grafting materials.
The vascularization of the antero-lateral wall of
the sinus, which is involved in sinus lift surgery
when the lateral approach is carried out, is
characterized by the presence of an intra-osseous
anastomosis between the dental branch of the
posterior superior alveolar artery (PSAA), also
known as alveolar antral artery (AAA) (Gaudy
2003; Rosano et al. 2009), and the infraorbital
artery (IOA).
Such anastomosis, although radiographically
evident in almost 50% of cases (Elian et al.
2005; Mardinger et al. 2007), courses intra-osseously
halfway up the lateral sinus wall and is
reported in the width of the cortical bone of the
lateral wall of the maxillary sinus in 100% of
cases (Solar et al. 1999; Traxler et al. 1999;
Rosano et al. 2009).
The AAA, whose reported diameter is up to
2.5–3 mm (Mardinger et al. 2007; Ella et al.
2008), supplies the sinus membrane and the
antero-lateral wall of the sinus, and as a
consequence, has the potential to cause bleeding
complications during lateral window osteotomies.
Even if the transection of such artery is not life
threatening because its haemorrhage mostly resolves
itself owing to a reactive contraction
(Rosano et al. 2009), impairment in visualization
of the Schneiderian membrane may occur,
especially when the AAA diameter is relevant,
c 2010 John Wiley & Sons A/S 1

Rosano et al Haemorrhage risk during sinus surgery
making its elevation far more difficult and interfering
with placement of the graft material.
In such a context, the purpose of this cadaveric
and CT scan study was to investigate the prevalence,
location, size and course of the AAA
located on the anterior lateral wall of the maxillary
sinus, so as to provide indications for
improving the safety of sinus floor elevation
procedure, especially in cases of extreme atrophy
of the alveolar process.
Material and methods
Fig. 1. View of the anterolateral wall of the maxillary sinus by transillumination: the alveolar antral artery dissection is carried
out in the area selected for sinus antrostomy as far as the infraorbital artery (a) and the posterior superior alveolar artery (b) are
visible respectively at its medial and distal extremity. The bony vessel is strictly stick to the Schneiderian membrane.
Fig. 2. Computed tomography scan 3D view of the lateral wall of the maxillary sinus which shows the point of emergence of
the infraorbital artery (IOA) (1), the point of anastomosis between the IOA and the alveolar antral artery (AAA) (2) as well as
the route of the AAA (3) forming a small concavity (white arrow).
Thefirstpartofthestudywasperformedon30
maxillary sinuses, deriving from 15 human
cadaver heads. The specimens belonged to subjects
with an age range of 59–90 years (mean age
76 years) and equal sex distribution, who had
donated their body for research purpose. The
study obtained ethical approval from the Department
of Anatomy at the Faculty of Medicine
René Descartes of Paris 5 (Paris 5 University,
Paris). Direct visualization of the AAA was
obtained by fenestrating the anterior lateral
wall of the sinus cavity and its dissection was
carried out as far as the IOA and the PSAA were
visible at its extremities (Fig. 1), in order to
determine its course with respect to both the
Schneiderian membrane and the buccal antral
wall.
To detect such an artery, the vascular network
afferent to the sinus was injected with liquid latex
mixed with green India ink through the external
carotid artery.
The second part of the study consisted of 100
CT scans from 100 patients scheduled for sinus
lift surgery at the Dental Clinic of the IRCCS
Istituto Ortopedico Galeazzi, Università degli
Studi di Milano. The age range was 29–78
(mean: 53.5) years.
The CT scans were performed using a 2000
SOMATOM Volume Zoom 4 slice CT scanner
(Siemens AG, Medical Solutions, Forchheim,
Germany) with slices of 0.5 mm thickness. CT
images were investigated for the presence of a
bony canal, housing the AAA, in the context of
the sinus anterolateral wall.
Coronal, axial and sagittal views of the maxillary
sinus were obtained by means of a software
for 3D reconstruction (OneScan 3D, 3D-MED
s.r.l., Brescia, Italy), offering a photorealistic
rendering quality and able to import Dicom
formatted CT images.
The route of the AAA was assessed with
respect to the Schneiderian membrane and to
the bony wall, as well as its diameter and the
distance from its lowest point to the alveolar
crest, with a precision of 0.1 mm. The corresponding
ridge height was measured. The correlation
between the residual ridge height and the
distance between the AAA and the crest was also
analysed.
Only edentulous or partially edentulous maxillae
displaying Class V or VI resorption of
the alveolar process, according to Cawood &
Howell’s classification (1988), were taken into
consideration.
Results
The anatomical dissection confirmed that the
PSAA divides into two branches along its course:
an external (gingival) branch is directed towards
the superior buccal fornix and the maxillary
tuberosity; the other branch is internal (dental)
and, after coursing below the zygomatic process,
was found to point towards the inside of the
orbit making a circular anastomosis with the
IOA.
An intra-osseous anastomosis between the
AAA and the IOA was found by dissection in
100% of the anatomical cases (30/30 sinuses),
while a well-defined bony canal, located in the
context of the sinus anterolateral wall, was detected
radiographically in 94 out of 200 sinuses
examined (47% of cases).
The diameter of such bony canal was o1mm
in 52 sinuses (55.3% of 94 cases), 1–o2mm in
38 sinuses (40.4%) and 2mminfoursinuses
(4.3%).
The AAA displayed three different courses: (1)
within the buccal antral wall cortex; (2) between
the Schneiderian membrane and the lateral bony
wall of the sinus, in which a small concavity was
often visible (Figs 2 and 3); and (3) under the
periosteum of the sinus lateral wall.
In particular, the AAA course was found to be
(1) completely intra-osseous at its extremities in
100% of cases (Fig. 4); (2) partially intra-osseous
in the area usually involved with sinus antrostomy
(from second premolar to second molar) in
100% of cases (Fig. 4). In such an area, the AAA
was strictly close to the Schneiderian membrane
and partially encased in the lateral sinus wall
in all specimens. No bony layer interposed
between the AAA and the sinus membrane
could be identified by dissection (Figs 1 and 5);
and (3) variable (either intra-osseous or intra-
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Rosano et al Haemorrhage risk during sinus surgery
sinusal or sub-periosteal) in the maxillary tuberosity
area.
The vertical distance from the lowest point of
the vessel, corresponding to the first molar area,
to the alveolar crest averaged 11.25 2.99 (SD)
mm (range between 7.2 and 17.7 mm).
The residual ridge height ranged from 0.7 to
5.1 mm (mean height 3.60 1.28 mm). A slight
positive correlation between such a distance and
the ridge height was observed (r ¼ 0.38). When
considering a threshold of 3 mm for the residual
ridge height, the AAA-to-alveolar crest distance
averaged 9.33 2.41 (n ¼ 39) and 12.45 2.71
(n ¼ 55) for cases with ridge height o3mm and
3 mm, respectively.
Discussion
The anastomosis between PSAA and IOA provides
blood supply to the sinus membrane, to the
periosteal tissues, and especially, to the anterolateral
wall of the sinus (Solar et al. 1999; Rosano
et al. 2009).
The scientific literature reports that this vessel
is located at an average distance of 19 mm (Solar
et al. 1999; Traxler et al. 1999), 16.4 mm (Elian
et al. 2005) and 16.9 mm (Mardinger et al. 2007)
from the alveolar crest of the posterior maxilla.
Nevertheless, such data can be misleading
because the height of the residual bony ridge,
the maxillary atrophy class and the presence of
Fig. 3. Internal view of the maxillary sinus: the arrow A shows the alveolar antral artery, the endosseous branch of the
posterior superior alveolar artery (PSAA), partially encased in the lateral sinus wall, while the arrow B shows the infraorbital
artery deriving from the maxillary artery and forming a vascular arcade with the PSAA.
teeth play a relevant role in determining the
location of the vessel.
In the present study, the average distance of the
AAA from the alveolar ridge in atrophic maxillae
of Cawood & Howell class V and VI was
11.25 mm. For the most atrophic cases, in which
the ridge height is inferior to 3 mm, such a
distance was significantly lower with respect to
lesser atrophic cases. This would confirm that
the more resorbed the bone crest, the higher the
risk of violation of such a vessel during sinus
augmentation procedure.
These results are substantially in agreement
with the study by Mardinger et al. (2007), which
found that this vessel was located at a mean
distance of 10.9 mm from the crest in classes
D, E (Lekholm & Zarb 1985) and at a distance
greaterthan15mminclassesA,BandC.
Differences concerning the mean distance from
the vessel to the crest, with the studies by Solar
et al. (1999), Traxler et al. (1999) and Elian et al.
(2005) are probably due to the more strict inclusion
criteria considered in the present study,
where only highly atrophic ridges have been
examined.
Moreover, because a well-distinguished bony
wall between the intra-osseous maxillary anastomosis
and the maxillary sinus has never been
found by anatomic dissection (Fig. 1), it could be
speculated that the lowest border of such a vessel
Fig. 4. Computed tomography scan transversal views of the anterior lateral wall of a sinus where it is possible to evidence the course of the alveolar antral artery from the infraorbital artery (1)
to the posterior superior alveolar artery (2): completely intra-osseous at its extremities, between the Schneiderian membrane and the bony wall in the sinus antrostomy area, sub-periosteal in
the maxillary tuberosity area.
c 2010 John Wiley & Sons A/S
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Rosano et al Haemorrhage risk during sinus surgery
Fig. 5. Macro-anatomical dissection of the sinus lateral wall: the alveolar antral artery is close to the Schneiderian membrane
and no bony layer between such vessel and the membrane is visible after antrostomy.
could often be completely adherent to the sinus
membrane (that means not radiographically visible)
instead of being located inside the buccal wall
cortex.
This would justify the contradiction between a
100% prevalence of this artery found by dissection
and an only 47% prevalence detected by CT
scan in the present study.
The authors’ opinion is that such contradiction
may not depend on the AAA small diameter,
which makes it radiographically undetectable in
some cases, as suggested by Elian et al. (2005)
and Mardinger et al. (2007), but on an entirely
intra-sinusal location of the vessel.
The course of the AAA, as identified in this
study, is in agreement with the CT study by Ella
et al. (2008) where intra-osseous, intra-sinusal
and sub-periosteal courses of this artery were
detected.
As stated by Ella et al. (2008), a ‘‘superficial’’
location of such anastomosis, which is under
the periosteum of the sinus lateral wall
should also be considered. In the present study,
such sub-periosteal course was identified by
means of both CT scan analysis and anatomical
dissection in the maxillary tuberosity area but
never in the area usually selected for sinus
antrostomy.
When carrying out sinus lift surgery, the bony
window height should be almost 13 mm from the
ridge if the purpose is to place 11–13 mm dental
implants. Thus, in patients with severely
atrophic posterior maxillae (classes V, VI), the
possibility of lacerating the AAA must be considered,
especially when the residual ridge is
o3mmhigh.
The diameter of the anastomosis was
2 mm in a very few cases (3.3% by dissection
and 2% by CT scan); anyway, this eventuality,
even if infrequent, is worthy to be taken into
serious consideration.
As a matter of fact, if the damage of a bony
vessel o2 mm can be barely relevant under a
clinical point of view, the transection of an AAA
with a diameter over 2 mm is likely to produce
bleeding and impairment of vision, which may
lead to a potential membrane perforation, thus
prolonging the overall operation time, interfering
with the placement of bone graft and constituting
atruesurgicalcomplication.
In addition, the haemorrage from this artery (a)
may displace the grafting material due to a
‘‘washing’’ effect caused by the blood pressure,
thus reducing or compromising the filling of the
space below the Schneiderian membrane after
sinus floor elevation, and (b) may produce relevant
haematomas of the cheek area causing
discomfort to patients and creating an ideal ‘‘pabulum’’
for bacteria growth and consequent infection.
It is the authors’ opinion that the excision of a
large diameter AAA in combination with the
inadvertent tearing of the sinus membrane has
the potential to induce sinus mucosa swelling,
extrusion of blood into the sinus cavity as
well as a postoperative sinusitis as a major
drawback.
In fact, if the maxillary sinus is, even partly,
filled up by mucosal oedema, haematoma or
seroma, a delay of maxillary sinus clearance
may occur because of the reduction of maxillary
ostium patency, and maxillary sinusitis may
develop as well, compromising the success of
the grafting procedure (Timmenga et al. 2003).
Thepreservationofsuchanastomosisisimportant
not only to avoid bleeding complications
but also to support bone graft neoangiogenesis
(Taschieri & Rosano 2010); in this perspective,
its concomitant reflection with the Schneiderian
membrane during sinus augmentation procedures,
if possible and especially when its diameter
is consistent, should be seriously
considered.
In conclusion, the authors recommend to rely
upon CT scan imaging, which has been proved to
be the most appropriate radiographic method for
detecting any anatomical variation within the
sinus (Schwarz et al. 1987; Quirynen et al.
1990; Alder et al. 1995; Dula et al. 2001), before
sinus lift surgery is performed, in order to presurgically
evaluate the location, size and thus the
clinical relevance of this anastomotic vessel.
Extreme caution should be taken when the residual
ridge height is o3mm.
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