Keywords anterior clinoidectomy - posterior clinoidectomy - third nerve mobilization - basilar
apex - opticocarotid triangle - carotidoculomotor triangle
Aneurysms of the upper basilar artery (BA), which arise from the basilar bifurcation,
posterior cerebral artery (PCA), superior cerebellar artery (SCA) junction, and proximal
P1 segment, represent some of the most difficult and technically challenging to clip
directly. These aneurysms constitute 5 to 15% of all intracranial aneurysms and approximately
50% of all vertebrobasilar aneurysms.[1 ] Both the pterional (transsylvian) approach of Yasargil[2 ] and subtemporal approach of Drake[3 ] have traditionally been used with great success to treat these lesions. The pterional
approach has the advantages of bilateral visualization of the basilar tip perforators,
PCA and SCA, less temporal lobe retraction, less oculomotor nerve injury and is more
familiar to most surgeons compared with the subtemporal approach. With the pterional
approach, dissection of upper BA aneurysms is usually performed through a space on
either the medial (opticocarotid triangle) or lateral (carotidoculomotor triangle)
side of the internal carotid artery (ICA). In an early article, Yasargil noted that
dissection through the opticocarotid triangle is sometimes limited when the ICA and
optic nerve (ON) are closely opposed, and as such dissection lateral to the ICA is
preferable.[1 ] In some circumstances, however, this corridor can also be limited and can be overcome
by incising and laterally retracting the tentorial edge. In addition, aneurysms located
below the level of the posterior clinoid process may be inaccessible with this approach.
These limitations have prompted others to supplement the standard pterional craniotomy
with removal of the zygoma,[4 ]
[5 ] and anterior[6 ]
[7 ] and/or posterior clinoidectomy,[1 ] in addition to mobilization of the carotid artery from the distal dural ring.[8 ]
The decision to use each or any of these surgical maneuvers is often determined preoperatively,
and alterations in the surgical plan may become necessary intraoperatively if exposure
is not optimal. Variables that are commonly thought to impact this decision include
the positional relationship between the basilar apex and the posterior clinoids,[9 ] as well as the length of the carotid artery.[10 ] Youssef et al have recently published the effect of anterior and posterior clinoidectomies
and ICA mobilization on the dimension of the carotidoculomotor window and rostracaudal
exposure of the BA.[11 ] In this study, we employed a frameless stereotactic system to quantitatively measure
the surgical area of the opticocarotid and carotidoculomotor triangle and the upper
BA together with the surgical freedom before and after anterior and posterior clinoidectomies
and finally after mobilization of the third cranial nerve from its tentorial insertion.
Methods
Cadaveric Preparation
This study was performed on six cadaveric head specimens bilaterally and two unilaterally,
yielding a total of 14 datasets.
The cadaver preparation technique used was based on that described in the University
of Southern California Skull Base Dissection Manual.[12 ] The cerebral arterial and venous systems were flushed with normal saline, followed
by one bottle of an arterial conditioner (Metaflow, Dodge Chemicals, Cambridge, Massachusetts).
Cadaveric head specimens were then soaked in a diluted Metaflow solution overnight
followed by soaking in methanol for 24 hours. Carotid arteries were next flushed with
5% buffered formalin and heads left to soak in this solution for 1 to 2 weeks until
brain consistency mimicked that of living tissue.
Dissection Technique
Specimens were rigidly fixed in place and a bicoronal scalp flap elevated. An orbitozygomatic
craniotomy was then performed and included mobilization of the temporal process of
the zygomatic bone. Extradural dissection was conducted to maximize removal of the
orbital roof. At completion of this portion of the dissection and under the operative
microscope, the dura was opened and an extensive dissection of the sylvian fissure
and basal cisterns was performed. Frontal and temporal lobe retractors were then placed.
At this point in the dissection, a base set of measurements was obtained ([Table 1 ]). These measurements were repeated after intradural anterior and posterior clinoidectomies
and finally after mobilization of the third cranial nerve from its tentorial insertion.
Table 1
Changes in exposure and surgical freedom following resection of the anterior and posterior
clinoids during a modified orbitozygomatic approach to the basilar tip
Resection
“Triangle” exposure (mm2 )
Proximal control (mm)
Surgical freedom at basilar tip (degrees)
Nerve III
Optic nerve
Nerve III access (inferior–superior)
Nerve III access (medial–lateral)
Optic nerve access (inferior–superior)
Baseline
93.7 ± 38.5a
57.1 ± 19.3a
8.3 ± 3.1a
22.6 ± 6.8a
−
18.7 ± 9.3a
Anterior clinoid
91.4 ± 35.2a
89.7 ± 31.9b
9.0 ± 3.1a
24.4 ± 9.2a
29.7 ± 6.3a
23.6 ± 10.6b
Posterior clinoid
120.4 ± 25.1b
74.0 ± 19.0a,b
11.4 ± 5.1b
30.3 ± 5.5b
31.7 ± 4.6a
26.5 ± 11.1c
Mobilization of the third nerve
140.1 ± 25.4b
82.1 ± 31.1b
12.2 ± 5.1b
30.8 ± 5.5b
36.1 ± 6.1b
−
Note: Mean ± standard deviation. Values with unlike superscripts are different at:
p < 0.017 (“triangle” exposures); p < 0.012 (proximal control); p < 0.047 (surgical freedom). Hyphen indicates data not collected.
Stereotactic Measurements
Cadaveric head specimens were rigidly fixed to the bench top and remained in the same
position during all dissection steps and data gathering. Stereotactic data was gathered
by use of a frameless navigational device (StealthStation, Medtronic Inc., Broomfield,
Colorado). The StealthStation reference arc was positioned in a vice close to the
cadaveric head and measurements obtained with the frameless stereotactic pointer probe.
Measurements consisted of simple three-dimensional coordinates for each data point
and were extracted from the working files of the StealthStation recording system software.
Cadaveric head specimens were not imaged.
The exposure through the opticocarotid and carotidoculomotor triangles was estimated
by calculation of the area defined by a small number of discrete points at the periphery
of each respective “triangle.” These discrete points were designated as follows: (1)
lateral edge of the ON as it enters the optic canal, (2) lateral edge of the ON at
the optic chiasm, at the inflection point, (3) medial edge of the ICA, at its bifurcation,
(4) medial edge of cranial nerve III at the proximal-most point visible, (5) medial
edge of cranial nerve III, midway between points 4 and 6, (6) medial edge of cranial
nerve III as it enters the cavernous sinus, (7) lateral, proximal-most point visible
on the ICA, (8) medial proximal-most point visible on the ICA, and (9) lateral edge
of the ICA, midway between points 3 and 8. The area for the opticocarotid triangle
was estimated as the sum of the areas of geometric triangles formed by points 2-3-9,
2-9-8, and 2-8-1. The carotidoculomotor triangle was likewise estimated as the sum
of the areas of geometric triangles 3-4-5, 3-5-9, 5-9-6, and 9-6-7 ([Fig. 1A, B ]).
Fig. 1 Surgical positioning, skin incision, and bony exposure of the orbitozygomatic approach
(left and right). Left landmarks: 1 lateral edge of the optic nerve as it enters the optic canal; 2 lateral edge of the optic nerve at the optic chiasm, at the inflection point; 3 medial edge of the internal carotid artery, at its bifurcation; 4 medial edge of cranial nerve III at the proximal-most point visible; 5 medial edge of cranial nerve III, midway between points 4 and 6; 6 medial edge of cranial nerve III as it enters the cavernous sinus; 7 lateral, proximal-most point visible on the internal carotid artery; 8 medial proximal-most point visible on the internal carotid artery; 9 lateral edge of the internal carotid artery, midway between points 3 and 8.
Surgical freedom available for the surgeon's instruments was estimated as an angle
measured from the basilar apex as the vertex. The stereotactic probe was placed first
at the basilar apex, through either the third nerve or the ON “triangle,” and the
coordinates of this point were recorded. Then a micro-dissector was placed at the
basilar apex, and the dissector rotated sequentially to the medial- and lateral-most
extent possible, and then the inferior- and superior-most extent possible and the
coordinates of the dissector handle recorded with the stereotactic probe at each point.
In this way, three points in space were recorded in turn, defining either a mediolateral
or inferosuperior angle centered at the basilar apex. The measurements were repeated
sequentially, as appropriate, after each stage of the dissection.
Proximal control was measured by recording the coordinates of the stereotactic probe
first at the basilar apex and then at the proximal-most point visible along the artery
after each stage of the dissection.
Statistical Analysis
Statistical analysis was performed using repeated analysis of variance measurements
using the Bonferroni inequality to detect posthoc pairwise differences. For surgical
freedom measurements through the ON “triangle,” only six specimens allowed sufficient
access to place the stereotactic probe, thus reducing the sample size from 14.
Results
The initial area of the carotidoculomotor triangle, the opticocarotid triangle, and
the exposed length of the BA was 93.7 ± 38.5 mm2 , 57.1 ± 19.3 mm2 , and 8.3 ± 3.1 mm, respectively. Anterior clinoidectomy increased the exposed area
of opticocarotid triangle significantly from 57.1 ± 19.3 mm2 to 89.7 ± 31.9 mm2 (p < 0.017). Surgical freedom for the surgeon's hands and instruments was also increased
significantly from 18.7 ± 9.3 degrees to 23.6 ± 10.6 degrees in inferosuperior projection
of the opticocarotid triangle (p < 0.047). Resection of the anterior clinoid process (ACP) did not improve the exposed
area of the carotidoculomotor triangle and proximal control of the BA.
Posterior clinoidectomy significantly increased the carotidoculomotor triangle from
93.7 ± 38.5 mm2 to 120.4 ± 25.1 mm2 (p < 0.017) together with the exposed length of the upper BA from 8.3 ± 3.1 mm to 11.4 ± 5.1 mm
(p < 0.012). Surgical freedom is also increased in the inferosuperior projection of
the carotidoculomotor triangle after posterior clinoidectomy (p < 0.047). Mobilization of the third nerve did not increase the exposure of the carotidoculomotor
triangle and the proximal control of the BA significantly. The mobilization of the
third nerve resulted in an increased in surgical freedom in the mediolateral projection
of the carotidoculomotor triangle only (p < 0.047). Results are summarized in [Table 1 ].
Discussion
The pterional transsylvian approach is a standard procedure for upper BA aneurysms.[2 ] Combining it with resection of the orbital roof or rim or with resection of the
zygomatic arch may result in more gentle brain retraction with a shorter trajectory
to the lesion. Despite this extensive removal of extradural bony structures, the size
of the operative field continues to be limited since dissection for upper BA aneurysms
is performed mainly through deeper spaces, either the opticocarotid or carotidoculomotor
triangle. The opticocarotid triangle is limited by the ON, ICA, A1, and anterior clinoid,
whereas the carotidoculomotor triangle is limited by the oculomotor nerve, ICA, and
anterior clinoid and posterior clinoid process (PCP) ([Fig. 2 ]). As reported by Yasargil, dissection through the opticocarotid triangle is sometimes
limited when the ICA and ON are closely opposed.[1 ] If this triangle is wide enough for aneurysm dissection, temporary clipping makes
the space narrower and neck clipping becomes more difficult. Under these circumstances,
both the opticocarotid and carotidoculomotor triangles should be used for major dissection
of aneurysms and/or temporary clipping. Several techniques have been suggested to
expand these triangles, including anterior clinoidectomy, mobilization of the ICA
and oculomotor nerve, and posterior clinoidectomy.[7 ]
[8 ]
[13 ]
[14 ] The removal of the ACP has been an important step in the management of aneurysms
involving the paraclinoid region and upper BA.[6 ]
[15 ]
[16 ]
[17 ] It allows early decompression and mobilization of the ON and improved surgical exposure
as reported by Evans et al[18 ] in a cadaveric study. This group of investigators documented a twofold increase
in the exposed length of the ON and the opticocarotid triangle and an almost fourfold
increase in the maximal width of the opticocarotid triangle by removing the ACP. Exposure
and incision of the distal dural ring after anterior clinoidectomy allows more effective
ICA mobilization laterally or medially by increasing the movable portion of the ICA
from a mean of 6 to 13 mm.[14 ] Our results showed that anterior clinoidectomy increased the exposed area of opticocarotid
triangle significantly from 57.1 ± 19.3 mm2 to 89.7 ± 31.9 mm2 . Surgical freedom for the surgeon's hands and instruments was also increased significantly
from 18.7 ± 9.3 degrees to 23.6 ± 10.6 degrees in inferosuperior projection of the
opticocarotid triangle. Resection of the ACP did not improve the exposed area of the
carotidoculomotor triangle and proximal control of the BA.
Fig. 2 Cadaveric surgical exposure of the opticocarotid and carotidoculomotor triangles
before (left) and after (right) drilling of the anterior and posterior clinoids. BA,
Basilar artery; CN III, oculomotor nerve, the third cranial nerve; ICA, internal carotid
artery; PCP, posterior clinoid process; SCA, superior cerebellar artery.
Although ACP can be removed extradurally[1 ]
[19 ] or intradurally,[8 ]
[20 ] extradural clinoidectomy has several advantages over an intradural technique, such
as easier anatomical orientation that may result in more extensive and faster removal
and better protection of the intradural structures by the overlying dura. We recently
reported a modified technique of performing an extradural anterior clinoidectomy that
results in technical simplicity, decreased incidence of neurovascular damage, postoperative
cerebrospinal fluid leaks, and tension pneumocephalus.[1 ]
[16 ]
[21 ]
[22 ] When surgery is performed following subarachnoid hemorrhage of an aneurysm in close
anatomical association with the ACP, removal of the extradurally hollowed ACP should
be performed intradurally to avoid inadvertent rupture from extradural manipulation.
Major complications of anterior clinoidectomy include rhinorrhea, visual defect, optic
and oculomotor nerve injury, injury to the ICA, and rupture of the aneurysm.[1 ]
[16 ]
[22 ]
According to their location relative to the posterior clinoid, upper BA aneurysms
can be divided into three types[23 ]: those located more than 5 mm above the PCP are called supraclinoid, those located
within 5 mm of PCP are called clinoid, and infraclinoid aneurysms are located more
than 5 mm inferior to the PCP. It has been reported that 14 to 19% of upper BA aneurysms
are below the level of PCP.[24 ]
[25 ] Yasargil described removal of PCP to successfully expose aneurysms hidden by the
PCP.[1 ] Dolenc described a transcavernous approach by mobilizing the ICA and oculomotor
nerve after anterior and posterior clinoidectomies to increase in the carotidoculomotor
triangle and the length of BA exposed.[7 ] The mean increase in the exposure of the upper BA in transcavernous approach was
13.4 and 12.8 mm in the cadaver studies performed by Chanda and Nanda[26 ] and Seoane et al,[27 ] respectively. Exposing the cavernous sinus and unroofing the oculomotor nerve in
the transcavernous approach carries the risk of significant bleeding from the cavernous
sinus and injury to the oculomotor nerve and cavernous ICA. Since additional procedures
in this anatomically complex region of the skull base are associated with increased
morbidity and risk, each step of bony removal and surgical procedure should be evaluated
quantitatively and the resultant advantage and risks should be carefully analyzed.
In this study, we document that posterior clinoidectomy significantly increase the
carotidoculomotor triangle from 93.7 ± 38.5 mm2 to 120.4 ± 25.1 mm2 together with the exposed length of the upper BA from 8.3 ± 3.1 mm to 11.4 ± 5.1
mm. The angle available to use surgical equipment was also increased in the inferosuperior
projection of the carotidoculomotor triangle. Altogether, this will result in an easier
and safer application of temporary clipping for proximal control and a better angle
without obstruction of the surgeon's view. Youssef et al[11 ] showed that anterior clinoidectomy and ICA mobilization increased the carotidoculomotor
triangle 44% anteriorly and 28% posteriorly, and exposed length of the BA increased
by 69% after posterior clinoidectomy. We, however, believe that the removal of the
posterior clinoid is the major step in increasing the exposed area of the carotidoculomotor
triangle mainly for two reasons. First, in our study, the removal of ACP did not affect
the exposed area of the carotidoculomotor triangle, and, second, Youssef et al did
not examine the successive exposure afforded by each step of this multistep approach.
The benefits from mobilizing the third nerve for exposure of the carotidoculomotor
triangle and the proximal control of the BA were not significant enough compared with
those after posterior clinoidectomy. Although it resulted in a significant increase
in surgical freedom in the mediolateral projection of the carotidoculomotor triangle,
we think that the mobilization of the third nerve should not be performed routinely
in patients with the low lying basilar apex aneurysms since this approach is associated
with oculomotor dysfunction in more than two-thirds of patients.[7 ]
[16 ]
Conclusion
Together, the anterior and posterior clinoidectomies significantly improved the area
of exposure for the opticocarotid and carotidoculomotor triangle and exposed length
of the BA available for proximal control. This improvement on both triangles is extremely
important for large or giant aneurysms of the upper BA or aneurysms hidden by the
posterior clinoid, since the main dissection and clipping of the aneurysms can be
performed through one of these spaces without difficulty, while the other space is
being used for proximal control by temporary clipping. The only benefit gained by
mobilization of the third nerve was increased surgical freedom in the mediolateral
projection of the carotidoculomotor triangle.
