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Gabriele Rosano<br />

Silvio Taschieri<br />

Jean-François Gaudy<br />

Tommaso Weinstein<br />

Massimo Del Fabbro<br />

Maxillary sinus vascular anatomy and its<br />

relation to sinus lift surgery<br />

Authors’ affiliations:<br />

Gabriele Rosano, Silvio Taschieri, Tommaso Weinstein,<br />

Massimo Del Fabbro, Dental Clinic, Department of<br />

Health Technologies, Galeazzi Orthopaedic Institute,<br />

University of Milan, Milan, Italy<br />

Jean-François Gaudy, Department of Cranial<br />

Cervicofacial Anatomy, Faculty of Medicine,<br />

University René Descartes–Paris5,Paris,France<br />

Corresponding author:<br />

Dr Gabriele Rosano<br />

Università degli Studi di Milano<br />

Dipartimento di Tecnologie per la Salute<br />

IRCCS Istituto Ortopedico Galeazzi<br />

Via R. Galeazzi, 4<br />

20161 – Milano<br />

Italy<br />

Tel.: þ 39 02 50319950<br />

Fax: þ 39 02 50319960<br />

e-mail: gabriele.rosano@unimi.it<br />

Key words: haemorrhage risk, maxillary sinus vascularisation, sinus lift surgery<br />

Abstract<br />

Objectives: To investigate the prevalence, location, size and course of the anastomosis between the<br />

dental branch of the posterior superior alveolar artery (PSAA), known as alveolar antral artery (AAA),<br />

and the infraorbital artery (IOA).<br />

Material and methods: The first part of the study was performed on 30 maxillary sinuses deriving from<br />

15 human cadaver heads. In order to visualize such anastomosis, the vascular network afferent to the<br />

sinus was injected with liquid latex mixed with green India ink through the external carotid artery. The<br />

second part of the study consisted of 100 CT scans from patients scheduled for sinus lift surgery.<br />

Results: An anastomosis between the AAA and the IOA was found by dissection in the context of the<br />

sinus anterolateral wall in 100% of cases, while a well-defined bony canal was detected<br />

radiographically in 94 out of 200 sinuses (47% of cases).<br />

The mean vertical distance from the lowest point of this bony canal to the alveolar crest was<br />

11.25 2.99 mm (SD) in maxillae examined by CT. The canal diameter was o1 mm in 55.3% of cases,<br />

1–2 mm in 40.4% of cases and 2–3 mm in 4.3% of cases.<br />

In 100% of cases, the AAA was found to be partially intra-osseous, that is between the Schneiderian<br />

membrane and the lateral bony wall of the sinus, in the area selected for sinus antrostomy.<br />

Conclusions: A sound knowledge of the maxillary sinus vascular anatomy and its careful analysis by CT<br />

scan is essential to prevent complications during surgical interventions involving this region.<br />

Date:<br />

Accepted 7 July 2010<br />

To cite this article:<br />

Rosano G, Taschieri S, Gaudy J-F, Weinstein T, Del Fabbro<br />

M. Maxillary sinus vascular anatomy and its relation to sinus<br />

lift surgery.<br />

Clin. Oral Impl. Res. 22, 2011; 711–715.<br />

doi: 10.1111/j.1600-0501.2010.02045.x<br />

Sinus augmentation using autogenous bone or<br />

bone substitutes is a safe procedure with high<br />

predictability (Wallace & Froum 2003; Aghaloo<br />

& Moy 2007; Del Fabbro et al. 2008; Pjetursson<br />

et al. 2008) for the rehabilitation of severely<br />

atrophic posterior maxillae.<br />

However, given the extensiveness of the maxillary<br />

vascular network, it is not infrequent to run<br />

into vascular complications that may compromise<br />

the outcome of surgery. For example, severe<br />

haemorrhage may occur as a result of arterial<br />

injury (Chanavaz 1996).<br />

A sound knowledge of the arterial supply of the<br />

maxillary sinus is mandatory for surgical procedures<br />

involving this area, such as sinus floor<br />

elevation and implantation of grafting materials.<br />

The vascularization of the antero-lateral wall of<br />

the sinus, which is involved in sinus lift surgery<br />

when the lateral approach is carried out, is<br />

characterized by the presence of an intra-osseous<br />

anastomosis between the dental branch of the<br />

posterior superior alveolar artery (PSAA), also<br />

known as alveolar antral artery (AAA) (Gaudy<br />

2003; Rosano et al. 2009), and the infraorbital<br />

artery (IOA).<br />

Such anastomosis, although radiographically<br />

evident in almost 50% of cases (Elian et al.<br />

2005; Mardinger et al. 2007), courses intra-osseously<br />

halfway up the lateral sinus wall and is<br />

reported in the width of the cortical bone of the<br />

lateral wall of the maxillary sinus in 100% of<br />

cases (Solar et al. 1999; Traxler et al. 1999;<br />

Rosano et al. 2009).<br />

The AAA, whose reported diameter is up to<br />

2.5–3 mm (Mardinger et al. 2007; Ella et al.<br />

2008), supplies the sinus membrane and the<br />

antero-lateral wall of the sinus, and as a<br />

consequence, has the potential to cause bleeding<br />

complications during lateral window osteotomies.<br />

Even if the transection of such artery is not life<br />

threatening because its haemorrhage mostly resolves<br />

itself owing to a reactive contraction<br />

(Rosano et al. 2009), impairment in visualization<br />

of the Schneiderian membrane may occur,<br />

especially when the AAA diameter is relevant,<br />

c 2010 John <strong>Wiley</strong> & Sons A/S 711


Rosano et al Haemorrhage risk during sinus surgery<br />

making its elevation far more difficult and interfering<br />

with placement of the graft material.<br />

In such a context, the purpose of this cadaveric<br />

and CT scan study was to investigate the prevalence,<br />

location, size and course of the AAA<br />

located on the anterior lateral wall of the maxillary<br />

sinus, so as to provide indications for<br />

improving the safety of sinus floor elevation<br />

procedure, especially in cases of extreme atrophy<br />

of the alveolar process.<br />

Material and methods<br />

Fig. 1. View of the anterolateral wall of the maxillary sinus by transillumination: the alveolar antral artery dissection is carried<br />

out in the area selected for sinus antrostomy as far as the infraorbital artery (a) and the posterior superior alveolar artery (b) are<br />

visible respectively at its medial and distal extremity. The bony vessel is strictly stick to the Schneiderian membrane.<br />

Fig. 2. Computed tomography scan 3D view of the lateral wall of the maxillary sinus which shows the point of emergence of<br />

the infraorbital artery (IOA) (1), the point of anastomosis between the IOA and the alveolar antral artery (AAA) (2) as well as<br />

the route of the AAA (3) forming a small concavity (white arrow).<br />

Thefirstpartofthestudywasperformedon30<br />

maxillary sinuses, deriving from 15 human<br />

cadaver heads. The specimens belonged to subjects<br />

with an age range of 59–90 years (mean age<br />

76 years) and equal sex distribution, who had<br />

donated their body for research purpose. The<br />

study obtained ethical approval from the Department<br />

of Anatomy at the Faculty of Medicine<br />

René Descartes of Paris 5 (Paris 5 University,<br />

Paris). Direct visualization of the AAA was<br />

obtained by fenestrating the anterior lateral<br />

wall of the sinus cavity and its dissection was<br />

carried out as far as the IOA and the PSAA were<br />

visible at its extremities (Fig. 1), in order to<br />

determine its course with respect to both the<br />

Schneiderian membrane and the buccal antral<br />

wall.<br />

To detect such an artery, the vascular network<br />

afferent to the sinus was injected with liquid latex<br />

mixed with green India ink through the external<br />

carotid artery.<br />

The second part of the study consisted of 100<br />

CT scans from 100 patients scheduled for sinus<br />

lift surgery at the Dental Clinic of the IRCCS<br />

Istituto Ortopedico Galeazzi, Università degli<br />

Studi di Milano. The age range was 29–78<br />

(mean: 53.5) years.<br />

The CT scans were performed using a 2000<br />

SOMATOM Volume Zoom 4 slice CT scanner<br />

(Siemens AG, Medical Solutions, Forchheim,<br />

Germany) with slices of 0.5 mm thickness. CT<br />

images were investigated for the presence of a<br />

bony canal, housing the AAA, in the context of<br />

the sinus anterolateral wall.<br />

Coronal, axial and sagittal views of the maxillary<br />

sinus were obtained by means of a software<br />

for 3D reconstruction (OneScan 3D, 3D-MED<br />

s.r.l., Brescia, Italy), offering a photorealistic<br />

rendering quality and able to import Dicom<br />

formatted CT images.<br />

The route of the AAA was assessed with<br />

respect to the Schneiderian membrane and to<br />

the bony wall, as well as its diameter and the<br />

distance from its lowest point to the alveolar<br />

crest, with a precision of 0.1 mm. The corresponding<br />

ridge height was measured. The correlation<br />

between the residual ridge height and the<br />

distance between the AAA and the crest was also<br />

analysed.<br />

Only edentulous or partially edentulous maxillae<br />

displaying Class V or VI resorption of<br />

the alveolar process, according to Cawood &<br />

Howell’s classification (1988), were taken into<br />

consideration.<br />

Results<br />

The anatomical dissection confirmed that the<br />

PSAA divides into two branches along its course:<br />

an external (gingival) branch is directed towards<br />

the superior buccal fornix and the maxillary<br />

tuberosity; the other branch is internal (dental)<br />

and, after coursing below the zygomatic process,<br />

was found to point towards the inside of the<br />

orbit making a circular anastomosis with the<br />

IOA.<br />

An intra-osseous anastomosis between the<br />

AAA and the IOA was found by dissection in<br />

100% of the anatomical cases (30/30 sinuses),<br />

while a well-defined bony canal, located in the<br />

context of the sinus anterolateral wall, was detected<br />

radiographically in 94 out of 200 sinuses<br />

examined (47% of cases).<br />

The diameter of such bony canal was o1mm<br />

in 52 sinuses (55.3% of 94 cases), 1–o2mm in<br />

38 sinuses (40.4%) and 2mminfoursinuses<br />

(4.3%).<br />

The AAA displayed three different courses: (1)<br />

within the buccal antral wall cortex; (2) between<br />

the Schneiderian membrane and the lateral bony<br />

wall of the sinus, in which a small concavity was<br />

often visible (Figs 2 and 3); and (3) under the<br />

periosteum of the sinus lateral wall.<br />

In particular, the AAA course was found to be<br />

(1) completely intra-osseous at its extremities in<br />

100% of cases (Fig. 4); (2) partially intra-osseous<br />

in the area usually involved with sinus antrostomy<br />

(from second premolar to second molar) in<br />

100% of cases (Fig. 4). In such an area, the AAA<br />

was strictly close to the Schneiderian membrane<br />

and partially encased in the lateral sinus wall<br />

in all specimens. No bony layer interposed<br />

between the AAA and the sinus membrane<br />

could be identified by dissection (Figs 1 and 5);<br />

and (3) variable (either intra-osseous or intra-<br />

712 | Clin. Oral Impl. Res. 22, 2011 / 711–715 c 2010 John <strong>Wiley</strong> & Sons A/S


Rosano et al Haemorrhage risk during sinus surgery<br />

sinusal or sub-periosteal) in the maxillary tuberosity<br />

area.<br />

The vertical distance from the lowest point of<br />

the vessel, corresponding to the first molar area,<br />

to the alveolar crest averaged 11.25 2.99 (SD)<br />

mm (range between 7.2 and 17.7 mm).<br />

The residual ridge height ranged from 0.7 to<br />

5.1 mm (mean height 3.60 1.28 mm). A slight<br />

positive correlation between such a distance and<br />

the ridge height was observed (r ¼ 0.38). When<br />

considering a threshold of 3 mm for the residual<br />

ridge height, the AAA-to-alveolar crest distance<br />

averaged 9.33 2.41 (n ¼ 39) and 12.45 2.71<br />

(n ¼ 55) for cases with ridge height o3mm and<br />

3 mm, respectively.<br />

Discussion<br />

The anastomosis between PSAA and IOA provides<br />

blood supply to the sinus membrane, to the<br />

periosteal tissues, and especially, to the anterolateral<br />

wall of the sinus (Solar et al. 1999; Rosano<br />

et al. 2009).<br />

The scientific literature reports that this vessel<br />

is located at an average distance of 19 mm (Solar<br />

et al. 1999; Traxler et al. 1999), 16.4 mm (Elian<br />

et al. 2005) and 16.9 mm (Mardinger et al. 2007)<br />

from the alveolar crest of the posterior maxilla.<br />

Nevertheless, such data can be misleading<br />

because the height of the residual bony ridge,<br />

the maxillary atrophy class and the presence of<br />

Fig. 3. Internal view of the maxillary sinus: the arrow A shows the alveolar antral artery, the endosseous branch of the<br />

posterior superior alveolar artery (PSAA), partially encased in the lateral sinus wall, while the arrow B shows the infraorbital<br />

artery deriving from the maxillary artery and forming a vascular arcade with the PSAA.<br />

teeth play a relevant role in determining the<br />

location of the vessel.<br />

In the present study, the average distance of the<br />

AAA from the alveolar ridge in atrophic maxillae<br />

of Cawood & Howell class V and VI was<br />

11.25 mm. For the most atrophic cases, in which<br />

the ridge height is inferior to 3 mm, such a<br />

distance was significantly lower with respect to<br />

lesser atrophic cases. This would confirm that<br />

the more resorbed the bone crest, the higher the<br />

risk of violation of such a vessel during sinus<br />

augmentation procedure.<br />

These results are substantially in agreement<br />

with the study by Mardinger et al. (2007), which<br />

found that this vessel was located at a mean<br />

distance of 10.9 mm from the crest in classes<br />

D, E (Lekholm & Zarb 1985) and at a distance<br />

greaterthan15mminclassesA,BandC.<br />

Differences concerning the mean distance from<br />

the vessel to the crest, with the studies by Solar<br />

et al. (1999), Traxler et al. (1999) and Elian et al.<br />

(2005) are probably due to the more strict inclusion<br />

criteria considered in the present study,<br />

where only highly atrophic ridges have been<br />

examined.<br />

Moreover, because a well-distinguished bony<br />

wall between the intra-osseous maxillary anastomosis<br />

and the maxillary sinus has never been<br />

found by anatomic dissection (Fig. 1), it could be<br />

speculated that the lowest border of such a vessel<br />

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)<br />

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<br />

the maxillary tuberosity area.<br />

c 2010 John <strong>Wiley</strong> & Sons A/S 713 | Clin. Oral Impl. Res. 22, 2011 / 711–715


Rosano et al Haemorrhage risk during sinus surgery<br />

Fig. 5. Macro-anatomical dissection of the sinus lateral wall: the alveolar antral artery is close to the Schneiderian membrane<br />

and no bony layer between such vessel and the membrane is visible after antrostomy.<br />

could often be completely adherent to the sinus<br />

membrane (that means not radiographically visible)<br />

instead of being located inside the buccal wall<br />

cortex.<br />

This would justify the contradiction between a<br />

100% prevalence of this artery found by dissection<br />

and an only 47% prevalence detected by CT<br />

scan in the present study.<br />

The authors’ opinion is that such contradiction<br />

may not depend on the AAA small diameter,<br />

which makes it radiographically undetectable in<br />

some cases, as suggested by Elian et al. (2005)<br />

and Mardinger et al. (2007), but on an entirely<br />

intra-sinusal location of the vessel.<br />

The course of the AAA, as identified in this<br />

study, is in agreement with the CT study by Ella<br />

et al. (2008) where intra-osseous, intra-sinusal<br />

and sub-periosteal courses of this artery were<br />

detected.<br />

As stated by Ella et al. (2008), a ‘‘superficial’’<br />

location of such anastomosis, which is under<br />

the periosteum of the sinus lateral wall<br />

should also be considered. In the present study,<br />

such sub-periosteal course was identified by<br />

means of both CT scan analysis and anatomical<br />

dissection in the maxillary tuberosity area but<br />

never in the area usually selected for sinus<br />

antrostomy.<br />

When carrying out sinus lift surgery, the bony<br />

window height should be almost 13 mm from the<br />

ridge if the purpose is to place 11–13 mm dental<br />

implants. Thus, in patients with severely<br />

atrophic posterior maxillae (classes V, VI), the<br />

possibility of lacerating the AAA must be considered,<br />

especially when the residual ridge is<br />

o3mmhigh.<br />

The diameter of the anastomosis was<br />

2 mm in a very few cases (3.3% by dissection<br />

and 2% by CT scan); anyway, this eventuality,<br />

even if infrequent, is worthy to be taken into<br />

serious consideration.<br />

As a matter of fact, if the damage of a bony<br />

vessel o2 mm can be barely relevant under a<br />

clinical point of view, the transection of an AAA<br />

with a diameter over 2 mm is likely to produce<br />

bleeding and impairment of vision, which may<br />

lead to a potential membrane perforation, thus<br />

prolonging the overall operation time, interfering<br />

with the placement of bone graft and constituting<br />

atruesurgicalcomplication.<br />

In addition, the haemorrage from this artery (a)<br />

may displace the grafting material due to a<br />

‘‘washing’’ effect caused by the blood pressure,<br />

thus reducing or compromising the filling of the<br />

space below the Schneiderian membrane after<br />

sinus floor elevation, and (b) may produce relevant<br />

haematomas of the cheek area causing<br />

discomfort to patients and creating an ideal ‘‘pabulum’’<br />

for bacteria growth and consequent infection.<br />

It is the authors’ opinion that the excision of a<br />

large diameter AAA in combination with the<br />

inadvertent tearing of the sinus membrane has<br />

the potential to induce sinus mucosa swelling,<br />

extrusion of blood into the sinus cavity as<br />

well as a postoperative sinusitis as a major<br />

drawback.<br />

In fact, if the maxillary sinus is, even partly,<br />

filled up by mucosal oedema, haematoma or<br />

seroma, a delay of maxillary sinus clearance<br />

may occur because of the reduction of maxillary<br />

ostium patency, and maxillary sinusitis may<br />

develop as well, compromising the success of<br />

the grafting procedure (Timmenga et al. 2003).<br />

Thepreservationofsuchanastomosisisimportant<br />

not only to avoid bleeding complications<br />

but also to support bone graft neoangiogenesis<br />

(Taschieri & Rosano 2010); in this perspective,<br />

its concomitant reflection with the Schneiderian<br />

membrane during sinus augmentation procedures,<br />

if possible and especially when its diameter<br />

is consistent, should be seriously<br />

considered.<br />

In conclusion, the authors recommend to rely<br />

upon CT scan imaging, which has been proved to<br />

be the most appropriate radiographic method for<br />

detecting any anatomical variation within the<br />

sinus (Schwarz et al. 1987; Quirynen et al.<br />

1990; Alder et al. 1995; Dula et al. 2001), before<br />

sinus lift surgery is performed, in order to presurgically<br />

evaluate the location, size and thus the<br />

clinical relevance of this anastomotic vessel.<br />

Extreme caution should be taken when the residual<br />

ridge height is o3mm.<br />

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c 2010 John <strong>Wiley</strong> & Sons A/S 715 | Clin. Oral Impl. Res. 22, 2011 / 711–715

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