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Gabriele Rosano Maxillary sinus vascular anatomy and its

Silvio Taschieri
Jean-François Gaudy
relation to sinus lift surgery
Tommaso Weinstein
Massimo Del Fabbro

Authors’ affiliations: Key words: haemorrhage risk, maxillary sinus vascularisation, sinus lift surgery
Gabriele Rosano, Silvio Taschieri, Tommaso Weinstein,
Massimo Del Fabbro, Dental Clinic, Department of
Health Technologies, Galeazzi Orthopaedic Institute, Abstract
University of Milan, Milan, Italy Objectives: To investigate the prevalence, location, size and course of the anastomosis between the
Jean-François Gaudy, Department of Cranial dental branch of the posterior superior alveolar artery (PSAA), known as alveolar antral artery (AAA),
Cervicofacial Anatomy, Faculty of Medicine,
University René Descartes – Paris 5, Paris, France and the infraorbital artery (IOA).
Material and methods: The first part of the study was performed on 30 maxillary sinuses deriving from
Corresponding author: 15 human cadaver heads. In order to visualize such anastomosis, the vascular network afferent to the
Dr Gabriele Rosano
Università degli Studi di Milano sinus was injected with liquid latex mixed with green India ink through the external carotid artery. The
Dipartimento di Tecnologie per la Salute second part of the study consisted of 100 CT scans from patients scheduled for sinus lift surgery.
IRCCS Istituto Ortopedico Galeazzi
Results: An anastomosis between the AAA and the IOA was found by dissection in the context of the
Via R. Galeazzi, 4
20161 – Milano sinus anterolateral wall in 100% of cases, while a well-defined bony canal was detected
Italy radiographically in 94 out of 200 sinuses (47% of cases).
Tel.: þ 39 02 50319950
The mean vertical distance from the lowest point of this bony canal to the alveolar crest was
Fax: þ 39 02 50319960
e-mail: gabriele.rosano@unimi.it 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.

Sinus augmentation using autogenous bone or 2003; Rosano et al. 2009), and the infraorbital
bone substitutes is a safe procedure with high artery (IOA).
predictability (Wallace & Froum 2003; Aghaloo Such anastomosis, although radiographically
& Moy 2007; Del Fabbro et al. 2008; Pjetursson evident in almost 50% of cases (Elian et al.
et al. 2008) for the rehabilitation of severely 2005; Mardinger et al. 2007), courses intra-os-
atrophic posterior maxillae. seously halfway up the lateral sinus wall and is
However, given the extensiveness of the max- reported in the width of the cortical bone of the
illary vascular network, it is not infrequent to run lateral wall of the maxillary sinus in 100% of
into vascular complications that may compro- cases (Solar et al. 1999; Traxler et al. 1999;
mise the outcome of surgery. For example, severe Rosano et al. 2009).
haemorrhage may occur as a result of arterial The AAA, whose reported diameter is up to
injury (Chanavaz 1996). 2.5–3 mm (Mardinger et al. 2007; Ella et al.
A sound knowledge of the arterial supply of the 2008), supplies the sinus membrane and the
maxillary sinus is mandatory for surgical proce- antero-lateral wall of the sinus, and as a
dures involving this area, such as sinus floor consequence, has the potential to cause bleeding
elevation and implantation of grafting materials. complications during lateral window osteo-
The vascularization of the antero-lateral wall of tomies.
Date: the sinus, which is involved in sinus lift surgery Even if the transection of such artery is not life
Accepted 7 July 2010
when the lateral approach is carried out, is threatening because its haemorrhage mostly re-
To cite this article: characterized by the presence of an intra-osseous solves itself owing to a reactive contraction
Rosano G, Taschieri S, Gaudy J-F, Weinstein T, Del Fabbro
M. Maxillary sinus vascular anatomy and its relation to sinus anastomosis between the dental branch of the (Rosano et al. 2009), impairment in visualization
lift surgery.
Clin. Oral Impl. Res. 22, 2011; 711–715.
posterior superior alveolar artery (PSAA), also of the Schneiderian membrane may occur,
doi: 10.1111/j.1600-0501.2010.02045.x known as alveolar antral artery (AAA) (Gaudy especially when the AAA diameter is relevant,

c 2010 John Wiley & Sons A/S


 711
Rosano et al  Haemorrhage risk during sinus surgery

making its elevation far more difficult and inter-


fering with placement of the graft material.
In such a context, the purpose of this cadaveric
and CT scan study was to investigate the pre-
valence, location, size and course of the AAA
located on the anterior lateral wall of the max-
illary 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.
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.
Material and methods

The first part of the study was performed on 30


maxillary sinuses, deriving from 15 human
cadaver heads. The specimens belonged to sub-
jects 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 Depart-
ment 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.
Fig. 2. Computed tomography scan 3D view of the lateral wall of the maxillary sinus which shows the point of emergence of
To detect such an artery, the vascular network the infraorbital artery (IOA) (1), the point of anastomosis between the IOA and the alveolar antral artery (AAA) (2) as well as
afferent to the sinus was injected with liquid latex the route of the AAA (3) forming a small concavity (white arrow).
mixed with green India ink through the external
carotid artery.
The second part of the study consisted of 100 lation between the residual ridge height and the context of the sinus anterolateral wall, was de-
CT scans from 100 patients scheduled for sinus distance between the AAA and the crest was also tected radiographically in 94 out of 200 sinuses
lift surgery at the Dental Clinic of the IRCCS analysed. examined (47% of cases).
Istituto Ortopedico Galeazzi, Università degli Only edentulous or partially edentulous max- The diameter of such bony canal was o1 mm
Studi di Milano. The age range was 29–78 illae displaying Class V or VI resorption of in 52 sinuses (55.3% of 94 cases), 1–o2 mm in
(mean: 53.5) years. the alveolar process, according to Cawood & 38 sinuses (40.4%) and  2 mm in four sinuses
The CT scans were performed using a 2000 Howell’s classification (1988), were taken into (4.3%).
SOMATOM Volume Zoom 4 slice CT scanner consideration. The AAA displayed three different courses: (1)
(Siemens AG, Medical Solutions, Forchheim, within the buccal antral wall cortex; (2) between
Germany) with slices of 0.5 mm thickness. CT the Schneiderian membrane and the lateral bony
images were investigated for the presence of a Results wall of the sinus, in which a small concavity was
bony canal, housing the AAA, in the context of often visible (Figs 2 and 3); and (3) under the
the sinus anterolateral wall. The anatomical dissection confirmed that the periosteum of the sinus lateral wall.
Coronal, axial and sagittal views of the max- PSAA divides into two branches along its course: In particular, the AAA course was found to be
illary sinus were obtained by means of a software an external (gingival) branch is directed towards (1) completely intra-osseous at its extremities in
for 3D reconstruction (OneScan 3D, 3D-MED the superior buccal fornix and the maxillary 100% of cases (Fig. 4); (2) partially intra-osseous
s.r.l., Brescia, Italy), offering a photorealistic tuberosity; the other branch is internal (dental) in the area usually involved with sinus antrost-
rendering quality and able to import Dicom and, after coursing below the zygomatic process, omy (from second premolar to second molar) in
formatted CT images. was found to point towards the inside of the 100% of cases (Fig. 4). In such an area, the AAA
The route of the AAA was assessed with orbit making a circular anastomosis with the was strictly close to the Schneiderian membrane
respect to the Schneiderian membrane and to IOA. and partially encased in the lateral sinus wall
the bony wall, as well as its diameter and the An intra-osseous anastomosis between the in all specimens. No bony layer interposed
distance from its lowest point to the alveolar AAA and the IOA was found by dissection in between the AAA and the sinus membrane
crest, with a precision of 0.1 mm. The corre- 100% of the anatomical cases (30/30 sinuses), could be identified by dissection (Figs 1 and 5);
sponding ridge height was measured. The corre- while a well-defined bony canal, located in the and (3) variable (either intra-osseous or intra-

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

Rosano et al  Haemorrhage risk during sinus surgery

sinusal or sub-periosteal) in the maxillary tuber- Discussion teeth play a relevant role in determining the
osity area. location of the vessel.
The vertical distance from the lowest point of The anastomosis between PSAA and IOA pro- In the present study, the average distance of the
the vessel, corresponding to the first molar area, vides blood supply to the sinus membrane, to the AAA from the alveolar ridge in atrophic maxillae
to the alveolar crest averaged 11.25  2.99 (SD) periosteal tissues, and especially, to the antero- of Cawood & Howell class V and VI was
mm (range between 7.2 and 17.7 mm). lateral wall of the sinus (Solar et al. 1999; Rosano 11.25 mm. For the most atrophic cases, in which
The residual ridge height ranged from 0.7 to et al. 2009). the ridge height is inferior to 3 mm, such a
5.1 mm (mean height 3.60  1.28 mm). A slight The scientific literature reports that this vessel distance was significantly lower with respect to
positive correlation between such a distance and is located at an average distance of 19 mm (Solar lesser atrophic cases. This would confirm that
the ridge height was observed (r ¼ 0.38). When et al. 1999; Traxler et al. 1999), 16.4 mm (Elian the more resorbed the bone crest, the higher the
considering a threshold of 3 mm for the residual et al. 2005) and 16.9 mm (Mardinger et al. 2007) risk of violation of such a vessel during sinus
ridge height, the AAA-to-alveolar crest distance from the alveolar crest of the posterior maxilla. augmentation procedure.
averaged 9.33  2.41 (n ¼ 39) and 12.45  2.71 Nevertheless, such data can be misleading These results are substantially in agreement
(n ¼ 55) for cases with ridge height o3 mm and because the height of the residual bony ridge, with the study by Mardinger et al. (2007), which
 3 mm, respectively. the maxillary atrophy class and the presence of 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
greater than 15 mm in classes A, B and C.
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 inclu-
sion 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 anasto-
Fig. 3. Internal view of the maxillary sinus: the arrow A shows the alveolar antral artery, the endosseous branch of the
mosis and the maxillary sinus has never been
posterior superior alveolar artery (PSAA), partially encased in the lateral sinus wall, while the arrow B shows the infraorbital found by anatomic dissection (Fig. 1), it could be
artery deriving from the maxillary artery and forming a vascular arcade with the PSAA. 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


 713 | Clin. Oral Impl. Res. 22, 2011 / 711–715
Rosano et al  Haemorrhage risk during sinus surgery

with the placement of bone graft and constituting


a true surgical complication.
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 rele-
vant haematomas of the cheek area causing
discomfort to patients and creating an ideal ‘‘pa-
bulum’’ for bacteria growth and consequent in-
fection.
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.
Fig. 5. Macro-anatomical dissection of the sinus lateral wall: the alveolar antral artery is close to the Schneiderian membrane In fact, if the maxillary sinus is, even partly,
and no bony layer between such vessel and the membrane is visible after antrostomy. filled up by mucosal oedema, haematoma or
seroma, a delay of maxillary sinus clearance
could often be completely adherent to the sinus means of both CT scan analysis and anatomical may occur because of the reduction of maxillary
membrane (that means not radiographically visi- dissection in the maxillary tuberosity area but ostium patency, and maxillary sinusitis may
ble) instead of being located inside the buccal wall never in the area usually selected for sinus develop as well, compromising the success of
cortex. antrostomy. the grafting procedure (Timmenga et al. 2003).
This would justify the contradiction between a When carrying out sinus lift surgery, the bony The preservation of such anastomosis is im-
100% prevalence of this artery found by dissec- window height should be almost 13 mm from the portant not only to avoid bleeding complications
tion and an only 47% prevalence detected by CT ridge if the purpose is to place 11–13 mm dental but also to support bone graft neoangiogenesis
scan in the present study. implants. Thus, in patients with severely (Taschieri & Rosano 2010); in this perspective,
The authors’ opinion is that such contradiction atrophic posterior maxillae (classes V, VI), the its concomitant reflection with the Schneiderian
may not depend on the AAA small diameter, possibility of lacerating the AAA must be con- membrane during sinus augmentation proce-
which makes it radiographically undetectable in sidered, especially when the residual ridge is dures, if possible and especially when its dia-
some cases, as suggested by Elian et al. (2005) o3 mm high. meter is consistent, should be seriously
and Mardinger et al. (2007), but on an entirely The diameter of the anastomosis was considered.
intra-sinusal location of the vessel.  2 mm in a very few cases (3.3% by dissection In conclusion, the authors recommend to rely
The course of the AAA, as identified in this and 2% by CT scan); anyway, this eventuality, upon CT scan imaging, which has been proved to
study, is in agreement with the CT study by Ella even if infrequent, is worthy to be taken into be the most appropriate radiographic method for
et al. (2008) where intra-osseous, intra-sinusal serious consideration. detecting any anatomical variation within the
and sub-periosteal courses of this artery were As a matter of fact, if the damage of a bony sinus (Schwarz et al. 1987; Quirynen et al.
detected. vessel o2 mm can be barely relevant under a 1990; Alder et al. 1995; Dula et al. 2001), before
As stated by Ella et al. (2008), a ‘‘superficial’’ clinical point of view, the transection of an AAA sinus lift surgery is performed, in order to pre-
location of such anastomosis, which is under with a diameter over 2 mm is likely to produce surgically evaluate the location, size and thus the
the periosteum of the sinus lateral wall bleeding and impairment of vision, which may clinical relevance of this anastomotic vessel.
should also be considered. In the present study, lead to a potential membrane perforation, thus Extreme caution should be taken when the re-
such sub-periosteal course was identified by prolonging the overall operation time, interfering sidual ridge height is o3 mm.

References

Aghaloo, T.L. & Moy, P.K. (2007) Which hard tissue Cawood, J.I. & Howell, R.A. (1988) A classification of Dula, K., Mini, R., Van der Stelt, P.F. & Buser, D.
augmentation techniques are the most successful in the edentulous jaws. The International Journal of (2001) The radiographic assessment of implant pa-
furnishing bony support for implant placement? The Oral and Maxillofacial Surgery 17: 232–236. tients: decision making criteria. The International
International Journal of Oral & Maxillofacial Im- Chanavaz, M. (1996) Sinus grafting related to implan- Journal of Oral & Maxillofacial Implants 16: 80–89.
plants 22 (Suppl.): 49–70. tology. Statistical analysis of 15 years of surgical Elian, N., Wallace, S., Cho, S.C., Jalbout, Z.N. &
Alder, M.E., Deahl, S.T. & Matteson, S.R. (1995) experience (1979–1994). Journal of Oral Implantol- Froum, S. (2005) Distribution of the maxillary artery
Clinical usefulness of two dimensional refor- ogy 22: 119–130. as it relates to sinus floor augmentation. The Inter-
matted and three dimensionally rendered computer- Del Fabbro, M., Rosano, G. & Taschieri, S. (2008) national Journal of Oral & Maxillofacial Implants
ized tomographic images: literature review and Implant survival rates after maxillary sinus aug- 20: 784–787.
a survey of surgeons’opinions. Journal of Oral and mentation. European Journal of Oral Sciences 116: Ella, B., Sédarat, C., Da Costa Noble, R., Normand, E.,
Maxillofacial Surgery 53: 375–386. 497–506. Lauverjat, Y., Siberchicot, F., Caix, P. & Zwetyenga,

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

Rosano et al  Haemorrhage risk during sinus surgery

N. (2008) Vascular connections of the lateral wall of combination with sinus floor elevation. Journal of procedures. Clinical Oral Implants Research 10:
the sinus: surgical effect in sinus augmentation. The Clinical Periodontology 35: 216–240. 34–44.
International Journal of Oral & Maxillofacial Im- Quirynen, M., Lamoral, Y., Dekeyser, C., Peene, P., Taschieri, S. & Rosano, G. (2010) Management of the
plants 23: 1047–1052. van Steenberghe, D., Bonte, J. & Baert, AL. (1990) alveolar antral artery during sinus floor augmentation
Gaudy, J.-F. (2003) Anatomie Clinique. Rueil-Malmai- The CT scan standard reconstruction technique for procedures. The International Journal of Oral and
son Cedex: Groupe Liaisons, Editions CdP, 11pp. reliable jaw bone volume determination. The Inter- Maxillofacial Surgery 68: 230.
Lekholm, U. & Zarb, G.A. (1985) Patient selection. national Journal of Oral & Maxillofacial Implants 5: Timmenga, N.M., Raghoebar, G.M., Liem, R.S.B., van
In: Brånemark, P.-I., Zarb, G.A. & Albrektsson, T., 384–389. Weissenbruch, R., Manson, W.L. & Vissink, A.
eds. Tissue Integrated Prosthesis. Osseointegration Rosano, G., Taschieri, S., Gaudy, J.-F. & Del Fabbro, M. (2003) Effects of maxillary sinus floor elevation sur-
in Clinical Dentistry, 199–209. Chicago: Quintes- (2009) Maxillary sinus vascularization: a cada- gery on maxillary sinus physiology. European Journal
sence. veric study. Journal of Craniofacial Surgery 20: of Oral Sciences 111: 189–197.
Mardinger, O., Abba, M., Hirshberg, A. & Schwartz- 940–943. Traxler, H., Windisch, A., Geyerhofer, U., Surd, R.,
Arad, D. (2007) Prevalence, diameter and course of Schwarz, M.S., Rothman, S.L.G., Rhodes, M.L. & Solar, P. & Firbas, W. (1999) Arterial blood supply
the maxillary intraosseous vascular canal with rela- Chafetz, N. (1987) Computed tomography: part II. of the maxillary sinus. Clinical Anatomy 12: 417–
tion to sinus augmentation procedure: a radiographic Preoperative assessment of the maxilla for endosseous 421.
study. The International Journal of Oral and Max- implant surgery. Journal of Oral & Maxillofacial Wallace, S.S. & Froum, S.J. (2003) Effect of maxillary
illofacial Surgery 36: 735–738. Implants 2: 143–148. sinus augmentation on the survival of endosseous
Pjetursson, B.E., Tan, W.C., Zwahlen, M. & Lang, N.P. Solar, P., Geyerhofer, U., Traxler, H., Windisch, A., dental implants. A systematic review. Annals of
(2008) A systematic review of the success of sinus Ulm, C. & Watzek, G. (1999) Blood supply to the Periodontology 8: 328–343.
floor elevation and survival of implants inserted in maxillary sinus relevant to sinus floor elevation

c 2010 John Wiley & Sons A/S


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