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J Neurosurg 106:151–156, 2007
Anatomical study of the superior orbital fissure as seen
during a pterional approach
MARIO AMMIRATI, M.D.,1 AND ANTONIO BERNARDO, M.D.2
Department of Neurological Surgery, The Ohio State University, Columbus, Ohio; and 2Department of
Neurological Surgery, Weill Medical College of Cornell University, New York, New York
1
Object. The superior orbital fissure (SOF) is an important landmark in the neurosurgical pterional approach, but the
anatomical features of the SOF and the procedures necessary to fully expose it and its contents have not been detailed.
Although the pterional approach is commonly used during skull base or vascular surgery by neurosurgeons who may
already be familiar with its nuances and anatomical relationships to the SOF, this knowledge may also be useful to the
wider neurosurgical community. The authors describe the spatial relationships of the contents of the SOF and suggest
a specific sequence of steps for exposing the SOF region in a pterional approach.
Methods. Using standard microsurgical equipment and instruments, the authors performed 20 pterional approaches
in 10 embalmed cadaver heads in which the vascular systems had been injected with colored material.
Five sequential steps were delineated for approaching and dissecting the SOF and its contents: 1) drilling the sphenoidal ridge, anterior clinoidal process, and part of the greater and lesser wings of the sphenoid; 2) resecting the dural
bridge; 3) detaching the hemispheric dura mater, thereby exposing the anterior portion of the cavernous sinus and the
neural component entering the SOF; 4) identifying and dissecting the extraanular structures; and 5) opening the anulus
of Zinn and identifying its neural constituents.
Conclusions. Knowing the 3D relationships of the contents of the SOF encountered in the pterional approach enables
safe neurosurgical access to the area. The proposed sequence of steps allows a controlled exposure of the SOF and surrounding areas. Untethering the frontotemporal lobe by transecting the dural bridge connecting the dura to the periorbita allows good exposure of the basal frontotemporal lobes, both intra- and extradurally, and reduces brain retraction.
KEY WORDS • cavernous sinus • orbit • superior orbital fissure •
microsurgical anatomy • pterional approach
pterional approach to intracranial surgery, popularized by Yaşargil for aneurysm surgery,10 is one of
the most widely used approaches, either singly or as
a building block of more complex approaches.1 The SOF is
an important anatomical landmark encountered while executing this approach. It has a complex anatomy because of
the abundant neurovascular structures running through or
near it, and there are many changes in the anatomical relationships of these structures as they pass from one compartment to another within a very confined space (Fig. 1).3,8
Although this complexity is well documented in most anatomy textbooks,9 little information on the appearance of the
SOF and its components during a pterional approach is
available to the surgeon. During this approach, the SOF is
within the surgeon’s extradural pterional field of vision,
and therefore knowledge of the anatomical presentation of
the region is extremely important, regardless of whether the
T
HE
Abbreviations used in this paper: ON = optic nerve; SOF = superior orbital fissure; SOV = superior ophthalmic vein.
J. Neurosurg. / Volume 106 / January, 2007
SOF is an anatomical landmark en route to the target of the
procedure or is itself the target. Additionally, although the
pterional approach is commonly used for skull base or vascular procedures by neurosurgeons who are familiar with
the nuances of this approach, including its relationships to
the SOF, knowledge of these relationships may be useful to
the wider neurosurgical community. We describe the spatial
relationships of the various components of the SOF and of
the surrounding structures as they are encountered during a
pterional approach, and we enumerate the sequential surgical steps to expose the region fully using this approach.
Materials and Methods
We performed 20 pterional approaches using standard microsurgical equipment and instruments (such as operating microscopes and
high-speed drills) in 10 adult cadaver heads fixed in formalin. The
vascular systems were injected with colored silicone material to
facilitate visualization and identification of constituent vessels during surgery. The specimens were maintained in surgical position using a table-mounted Mayfield head clamp.
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FIG. 1. Illustration of the SOF from the pterional perspective, showing the relationship of the paraclinoidal internal
carotid artery to its rings (A) and the ON (B).
Results
Five sequential surgical steps were used to approach and
dissect the SOF, and are detailed below.
the anterior portion of the cavernous sinus and the third and
fourth cranial nerves as well as the first division of the fifth
cranial nerve (Fig. 4).
Bone Stage
Detaching the Hemispheric Dura
The first step of the dissection consists of an anterior clinoidectomy,7 executed after a standard pterional flap2 is
formed. The neurovascular structures of the SOF are exposed and mobilized by drilling the sphenoidal ridge, unroofing the ON, and removing the anterior clinoidal process
and part of the greater and lesser wings of the sphenoid. At
this point, the microscope is angled toward the most lateral
aspect of the SOF, encountering the periorbital continuation
of the intracranial dura mater, the dural bridge.
After dural bridge resection, the anterior half of the cavernous sinus can be exposed extradurally by carefully peeling the dura from the neural structures closest to crossing
the SOF. As the dura is elevated from the anterior portion of
the cavernous sinus, the cranial nerves are visible through
the thin and semitransparent veil of connective tissue covering them. Near the SOF, the cranial nerves are wrapped by
a common meningeal sheath, which is continuous anteriorly with the periosteum of the orbit and allows mobilization
of the dura without disruption of the venous channels of the
cavernous sinus.4 Changing the angle of the microscope at
this stage enables identification of most of the nerves crossing the SOF, including the frontal and lacrimal nerves;
branches of the ophthalmic division of the fifth cranial
nerve; and the third, fourth, and sixth cranial nerves (Fig. 5).
Dural Bridge Resection
The dural bridge is located on the lateral side of the SOF,
between the greater and lesser wings of the sphenoidal
bone.7 It is very short (usually 2–3 mm) and contains a small
bridging vessel, the orbitomeningeal artery, that needs to be
transected (Fig. 2). This vessel was present in all our specimens, and in eight, it was more than half the size of the middle meningeal artery. Sometimes the border between the dural bridge and the nerves crossing the lateral portion of the
SOF is not easily identifiable. Therefore, careful retraction
of the dura while resecting the dural bridge is advised so
that once separated from the bridge, the dura can provide a
well-defined cleavage plane between itself and the cranial
nerves of the anterior portion of the cavernous sinus, and
entry into the lateral aspect of the SOF can be controlled to
avoid risks to its neural structures (Fig. 3). Resecting the
dural bridge allows further detachment of the dura from the
surrounding structures and enables extradural exposure of
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Identifying and Dissecting Extraanular Structures
The extraanular structures are the trochlear, lacrimal, and
frontal nerves, and the SOV, which provides the main venous drainage from the orbit to the cavernous sinus. The
lacrimal nerve is the most lateral nerve in the SOF, and
therefore is the first nerve encountered by the surgeon during a pterional approach. The frontal nerve is immediately
medial to the lacrimal nerve, and the fourth cranial nerve is
inferior and medial to the frontal nerve (Fig. 6). The SOV
is located inferomedially to the lacrimal nerve. Because
these structures need to be carefully mobilized to access the
most medial (and deeper, from the pterional perspective)
J. Neurosurg. / Volume 106 / January, 2007
Superior orbital fissure anatomy in a pterional approach
FIG. 4. Photograph demonstrating the exposure of the anterior
portion of the cavernous sinus after the dura has been peeled off.
III = oculomotor nerve; IV = trochlear nerve; VI = abducent nerve.
Opening the Anulus of Zinn and Exposing the Intraanular
Structures
FIG. 2. Photograph of the opening of the dural bridge (upper) and
the dissection of the orbitomeningeal artery (asterisk; lower).
structures of the SOF, an incision is made just lateral to the
lacrimal nerve and continued forward into the periorbita
approximately 3 to 4 mm. This incision allows the surgeon
access to the area containing the nerves, allowing further
identification and dissection of these nerves that will need
to be gently retracted to expose the deeper intraanular structures (Fig. 7).
FIG. 3. Photograph showing the transection of the dural bridge.
ica = paraclinoidal internal carotid artery.
J. Neurosurg. / Volume 106 / January, 2007
The anulus of Zinn is an important anatomical landmark
in the SOF. It is a fibrous ring at the orbital apex in front of
the upper half of the medial part of the SOF, and is attached
to the lateral margin of the fissure near the junction of its lateral and medial parts. Four rectus muscles arise from the anulus and form a cone around the neural and vascular structures passing through the anulus. The intraanular structures
are the nasociliary nerve, the third and sixth cranial nerves,
sympathetic nerve fibers, the ciliary root, and the inferior
ophthalmic vein.
The next step in exposing the SOF is to open the anulus
of Zinn and identify the neural components that cross it,
which are the nasociliary nerve and the sixth cranial nerve,
the two branches of the third cranial nerve, and the sympathetic nerve fibers. An incision is made in the anulus of Zinn
along the medial aspect of the nasociliary nerve, which lies
outside the anulus. Once the nasociliary nerve has been exposed inside the anulus, the sixth cranial nerve located me-
FIG. 5. Photograph demonstrating further detachment of the dura
to allow clear visualization of the components of the SOF.
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M. Ammirati and A. Bernardo
FIG. 8. Photograph showing the exposure of the nasociliary
nerve after the initial opening of the anulus of Zinn. Asterisk indicates the nasociliary nerve; double asterisk, a remnant of the anulus
of Zinn.
FIG. 6. Photograph showing the identification of the extraanular
structures. II = ON.
dially to the nasociliary nerve can be identified. The third
cranial nerve and its superior and inferior divisions are located deep and medial to the nasociliary nerve and the sixth
cranial nerve. Between the sixth cranial nerve laterally and
the inferior oculomotor division medially is the sensory root
of the ciliary ganglion (Fig. 8). Deep in the surgical field,
just medial and inferior to the third cranial nerve, lies the
ophthalmic artery (Fig. 9).
Appropriate manipulation of the microscope allows visualization of the posterior section of the contents of the orbit.
Further removal of the orbital roof and incision of the periorbita fully exposes the orbit, which is entered from the
SOF portal as well as the orbital roof (Fig. 10). Throughout the dissection of the SOF, variously developed venous
structures are encountered, which represent the drainage of
the SOV and inferior ophthalmic vein into the veins of the
cavernous sinus.
FIG. 7. Photograph demonstrating the gentle retraction of the
extraanular structures to allow exposure of the anulus of Zinn and
the nerves passing through it.
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Discussion
The anatomy of the SOF is well described in most anatomy textbooks.3 Exploration of the SOF in recent studies has
focused primarily on determining the surgical anatomy of
different approaches to the orbit through the orbital roof and
making craniometric measurements.3,7,8 Although the pterional approach is one of the most fundamental and widely
used neurosurgical approaches, and the SOF and its contents are within the extradural pterional field of vision, little
information is available on the surgical anatomy of the SOF
during a pterional approach. The foundations of the current
pterional approach can be traced to Wagner at the end of the
nineteenth century, and Yaşargil refined and popularized the
approach in the microneurosurgical era. 5
The SOF is a complex anatomical structure at the junction of two areas of surgical complexity, the anterior cavernous sinus and orbital apex. Consistent with all skull base
anatomical junctions, the SOF has an intricate anatomy,
containing multiple neurovascular structures whose anatomical relationships change as they pass from one compartment to another within a very confined space. The results of our study suggest that a simple pterional approach
in combination with an anterior clinoidectomy, unroofing
of the ON canal, and extensive removal of the lesser and
greater sphenoidal wings leads to excellent extradural visualization of the contents of the SOF and its related topography (such as the anterior cavernous sinus and orbital apex).
As other investigators have done,7 we describe the exposure of the components of the SOF beginning with the anterior cavernous sinus. However, if operative circumstances
require a different starting point, a thorough knowledge of
the neural topography of the region will enable safe and
effective choices. If dissection requires beginning further
back on the superolateral wall of the cavernous sinus due to
the pathological involvement of the anterior cavernous sinus area, the veins of the cavernous sinus do not need to be
disturbed, because the third and fourth cranial nerves and
the first division of the fifth cranial nerve can be identified
in between the two layers of the superolateral wall of the
sinus. Alternatively, beginning dissection by incising the
posterior periorbita6 is more dangerous and requires knowledge of the extraanular nerves located just beneath the periorbita, which are not always visible through it.
For these reasons, we emphasize the importance of idenJ. Neurosurg. / Volume 106 / January, 2007
Superior orbital fissure anatomy in a pterional approach
FIG. 9. Photographs demonstrating the extensive opening of the
anulus of Zinn to allow identification of the intraanular structures.
IIIi = inferior branch of the oculomotor nerve; IIIs = superior branch
of the oculomotor nerve; asterisk indicates the nasociliary nerve;
double asterisk, the ophthalmic artery.
tifying the nerves in the anterior cavernous sinus when feasible. The ophthalmic nerve lies in the superolateral part of
the anterior cavernous sinus, dividing into its lacrimal, frontal, and nasociliary branches 2 to 3 mm prior to the SOF.
The lacrimal and frontal nerves are in close apposition as
they enter the most lateral section of the SOF, and the fourth
cranial nerve lies medially to them. Once these extraanular
structures are identified and partially mobilized, they can be
gently retracted, and the nasociliary nerve can be visualized
as it enters the anulus of Zinn. Making a 2- to 3-mm incision
medial to the nasociliary nerve and parallel to its long axis permits it to be mobilized, allows the identification of
the third cranial nerve and its two branches medial to the
nasociliary nerve, and facilitates the identification of the
sixth cranial nerve.
Partial or extensive dissection of the SOF components
may be valuable not only when approaching a pathology involving the fissure itself, but also for extra- and intradural
pathology of the sellar–parasellar area.7 Although execution
J. Neurosurg. / Volume 106 / January, 2007
FIG. 10. Photographs revealing a full exposure of the contents of
the orbit after removal of the orbital roof and opening of the periorbita. Asterisk indicates the nasociliary nerve.
of all the steps described is necessary only when the pathology is considered completely resectable and crosses the
orbit and anterior cavernous sinus, a detailed anatomical
knowledge of the 3D relationships of the SOF components
encountered is invaluable to all neurosurgeons using a pterional approach. Simple maneuvers made possible by a
detailed knowledge of the anatomical construct described
may be significantly helpful during a routine pterional approach.
We have found that transecting the dural bridge consistently leads to untethering the frontotemporal lobe from the
SOF. This extradural untethering is particularly helpful because it increases the operative space between the frontal
and temporal lobes, allowing a more basal exposure, both
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extra- and intradurally, with limited retraction of the brain.
This basal exposure is achieved using a rather simple and
routine neurosurgical approach and may be helpful in a routine pterional approach. With experience this dural bridge
resection may be performed quickly and expeditiously. We
have now incorporated this dural bridge resection in all our
pterional approaches.
Conclusions
Controlled surgical exposure of the SOF and surrounding
areas during a pterional approach is facilitated by an accurate knowledge of the 3D relationships of the neurovascular
structures in the area, and the proposed series of surgical
steps will allow safe exposure of this region. The extradural untethering of the frontotemporal dura by transecting the
dural bridge connecting the dura to the periorbita is particularly helpful in achieving a more basal exposure of the basal frontotemporal lobe intra- and extradurally with minimal retraction of the brain.
3. Govsa F, Kayalioglu G, Erturk M, Ozgur T: The superior orbital
fissure and its contents. Surg Radiol Anat 21:181–185, 1999
4. Kawase T, van Loveren H, Keller JT, Tew JM: Meningeal architecture of the cavernous sinus: clinical and surgical implications.
Neurosurgery 39:527–536, 1996
5. Ljunggren B, Fox JL: History of the pterional approach, in Fox JL
(ed): Atlas of Neurosurgical Anatomy. The Pterional Perspective. New York: Springer-Verlag, 1989, pp 1–10
6. Morard M, Tcherekayev V, de Tribolet N: The superior orbital fissure: a microanatomical study. Neurosurgery 35:1087–1093,
1994
7. Natori Y, Rhoton AL Jr: Microsurgical anatomy of the superior
orbital fissure. Neurosurgery 36:762–775, 1995
8. Natori Y, Rhoton AL Jr: Transcranial approach to the orbit: microsurgical anatomy. J Neurosurg 81:78–86, 1994
9. Pernkopf E (ed): Pernkopf Anatomy: Atlas of Topographic and
Human Anatomy: Thorax, Abdomen and Extremities, Vol 1.
Munich: Urban and Schwarzenberg, 1989, Vol 1, p 93
10. Yaşargil MG: Microneurosurgery, Vol 1. Stuttgart: Georg
Thieme Verlag, 1984, pp 208–271
References
1. Ammirati M, Kim H, Cho Y: Anatomo-radiological evaluation of
lateral approaches to the skull base. Skull Base 8:105–117, 1998
2. Fox JL: Cranial anatomy and the cranial flap, in Fox JL (ed): Atlas
of Neurosurgical Anatomy. The Pterional Perspective. New
York: Springer-Verlag, 1989, pp 37–54
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Manuscript received March 8, 2006.
Accepted in final form August 1, 2006.
Address reprint requests to: Mario Ammirati, M.D., Department
of Neurological Surgery, 410 West Tenth Avenue, N1025 Doan
Hall, Columbus, Ohio 43210. email: [email protected].
J. Neurosurg. / Volume 106 / January, 2007