Key-words: Anteroinferior-projecting aneurysm - distal transsylvian approach - middle cerebral
artery aneurysm - middle cerebral artery bifurcation aneurysm
Introduction
The middle cerebral artery bifurcation (MCAB), located at the first major bifurcation
of the middle cerebral artery (MCA), is the common location of intracranial aneurysms
(18%–20%) and the most common location of MCA aneurysms (80%–85%).[[1 ]],[[2 ]],[[3 ]] Majority of previous studies suggested that microsurgical clipping provided better
efficacy than endovascular techniques for the management of patients with MCA aneurysm.[[4 ]],[[5 ]],[[6 ]],[[7 ]]
The traditional pterional approach for MCA aneurysms by Yasargil et al. was proposed
in 1975. They utilized the microsurgical dissection of the MCA in the proximal to
distal fashion (proximal transsylvian approach).[[8 ]] Pritz et al. proposed the distal transsylvian approach (DTSA) for MCAB aneurysms
with good outcomes in 1994.[[9 ]] Various projections of MCAB aneurysms required different surgical strategies for
clipping. Heros and Fritsch proposed three main approaches for MCA aneurysms: (1)
the proximal Sylvian fissure (proximal transsylvian), (2) the distal Sylvian fissure
(distal transsylvian), and (3) transcortical superior temporal gyrus approach, which
were indicated for different locations and projections of MCA aneurysms. The disadvantage
of the proximal approach is that the dissection performed is relatively extensive
and risks of injury to the Sylvian fissure are high. The important drawback of the
distal approach was a late exposure of the M1 segment for the proximal control.[[2 ]]
For clipping of the MCAB aneurysms with anteroinferior projection, identification
of the proximal and middle parts of M1, which usually course superoposteriorly into
the deep part of the Sylvian fissure, is difficult and needs extensive Sylvian fissure
dissection carrying a high risk of brain damage. The authors performed the DTSA for
clipping of this specific type of MCAB aneurysms. The proximal control, the most important
step, was early obtained by accessing the dorsal surface of the distal M1 segment
with distal Sylvian fissure dissection [[Figure 1 ]]. With this approach, the aneurysm neck was exposed before the aneurysm dome [[Figure 2 ]] and the proximal Sylvian fissure dissection was not necessary.
Figure 1: The distal transsylvian approach for the anteroinferior-projecting middle cerebral
artery bifurcation aneurysm. (a) Skin incision, skull flap, and direction of the approach
(arrow). (b) The direction of the approach to the middle cerebral artery bifurcation
and aneurysm neck (arrow). (c) Magnification of (b) demonstrated the direction (arrow)
and target of the approach
Figure 2: Case No. 2 (a) right anterolateral view of three-dimensional CTA demonstrates an
anterior-projecting MCAB aneurysm and direction of the DTSA (arrow). (b and c) 3D
CTA with skull base shows the direction of the DTSA approach (arrow) in different
views. (d) The right supraclinoid internal carotid artery (arrow) and proximal M1
(asterisk) were exposed through the subfrontal route. (e) The entire right Sylvian
fissure was exposed and prepared using two retractors for dissection. (f) The starting
point of dissection was 6 - 7 cm from the tip of the temporal lobe. (g) Wide opening
of the distal Sylvian fissure. (h) MCAB (asterisk), superior trunk (S), and inferior
trunk (I) of M2 were identified through the DTSA. (i) Final view after a definite
aneurysmal clipping. CTA - Computed tomography angiography, DTSA - Distal transsylvian
approach, M1 - The first segment of the middle cerebral artery, M2 - The second
segment of the middle cerebral artery, MCAB - Middle cerebral artery bifurcation
In this study, rates of early exposure of distal M1 and complete aneurysm obliteration
were evaluated to determine the efficacy of DTSA. Surgical complications, such as
premature aneurysm rupture, postoperative brain contusion, and lenticulostriate artery
injury, were also evaluated to identify the safest approach.
Materials and Methods
Patients with anteroinferior-projecting MCAB aneurysms who underwent the DTSA for
aneurysm clipping at the Faculty of Medicine Vajira Hospital, Navamindradhiraj University,
between June 2018 and January 2021 were retrospectively reviewed. Patient data, aneurysm
characteristics, MCAB location, the incidence of premature rupture of aneurysm, completeness
of aneurysm obliteration, postoperative complications, and Glasgow outcome score (GOS)
at 3 months postoperatively were reviewed and analyzed.
Operative techniques for distal transsylvian approach
After careful evaluation of the preoperative computed tomography (CT) angiography,
the surgical approach was planned [[Figure 2 ]]a,[[Figure 2 ]]b,[[Figure 2 ]]c. The patient was placed in supine position with the head of the bed tilted approximately
30° above the heart level. The patient's face was turned approximately 40°–45° away
from the side of the operation with the vertex parallel to the floor and the neck
extended in the sniffing position. The important key that facilitates this approach
was the vertex not directed down but parallel to the floor to prevent falling down
of the temporal lobe to obscure the Sylvian fissure. Two self-retaining retractors
were prepared. After the scalp flap was created, frontotemporal craniotomy was performed
to cover the whole length of the Sylvian fissure [[Figure 1 ]]a. The sphenoid ridge was drilled until flat. The dura was opened in “U” shape with
the base at the sphenoid ridge to cover the proximal and distal Sylvian fissures.
When subarachnoid hemorrhage with brain edema was observed, the frontal lobe was gently
elevated and the cerebrospinal fluid was released from the carotid cistern and lamina
terminalis. The supraclinoid internal carotid artery (ICA) and proximal M1 segment
of MCA were secured through the subfrontal route [[Figure 2 ]]d. This step should be carefully performed in case the aneurysm dome adheres to
the sphenoid wing. Under high magnification of the operating microscope, the distal
Sylvian fissure was sharply dissected with micro-scissors using the integrated multi-maneuver
dissection technique after the arachnoid membrane was tensed using two retractors
[[Figure 2 ]]e. The starting point of the dissection was 6–7 cm from the tip of the temporal
lobe in the side of no bridging veins [[Figure 2 ]]f. Outside-in and inside-out (paperknife) technique was used to dissect the Sylvian
fissure with high magnification.[[10 ]],[[11 ]] The key step of this technique is the distal Sylvian fissure dissection deep down
to the dorsal surface of distal M1 before dissecting the aneurysm dome. The middle
part of the M1 segment, which usually courses in the deep part of the Sylvian fissure,
was not necessarily identified. With the meticulous cutting of arachnoid trabeculae
and wide opening of the distal Sylvian fissure, both retractor blades were placed
on both sides of the Sylvian fissure (intrasylvian retraction) and work as brain holders
[[Figure 2 ]]g. The spatulas were transitioned in a “fan-stair” shape in steps according to the
Sylvian fissure's profile.[[12 ]] The Sylvian veins and their branches should be preserved as much as possible. M4,
M3, and M2 segments of MCA were identified respectively, and then the superior or
inferior trunk of M2 was followed proximally to MCAB and distal M1 segment before
dissection of the aneurysm neck and dome [[Figure 2 ]]h. The dorsal surface of M1 was confirmed and prepared for temporally clip placement
without damaging the lenticulostriate arteries. Both sides of the aneurysm neck were
identified and prepared for neck clipping. In the case of short M1 segment with the
distal M1 obscured by limen insulae, exposure of the distal M1 is not easy and the
pilot (tentative) clipping on the aneurysm dome should be prepared for premature rupture.
The medial retraction of the limen insulae may be performed to identify the distal
M1. The hallmark to differentiate the distal M1 from proximal M2 branches was lenticulostriate
arteries located on the dorsal wall. After the proximal control at the distal M1 from
the dorsal side, the definite clipping of the aneurysm neck should be placed at the
ideal closure line [[Figure 2 ]]i and [[Figure 3 ]].[[13 ]],[[14 ]],[[15 ]] The patency of M1 and both M1 were confirmed using a micro-Doppler and indocyanine
green.
Figure 3: Ideal closure line clipping and direction of clip application in illustrative cases.
(a) Right MCAB aneurysm with the anterior projection of case No. 2. (b) Right MCAB
aneurysm with the anterior projection of case No. 8. (c) Left MCAB aneurysm with the
anterior projection of case No. 9. (d) Left MCAB aneurysm with the anterior projection
of case No. 12. MCAB - Middle cerebral artery bifurcation
Outcome assessment
Surgical outcomes were evaluated at 3 months postdischarge with GOS by direct examinations
or telephone interviews. A patient with good grade was defined as having an initial
World Federation of Neurosurgical Societies (WFNS) grade of 1–3 in ruptured cases
and an intact neurological status at preoperative period in unruptured cases. Patients
with an initial WFNS grade of 4–5 in the subarachnoid hemorrhage group and a major
neurological deficit in the unruptured group was classified as patients with poor
grade.
Postoperative brain contusion, new neurological deficit postoperatively, intraoperative
lenticulostriate artery injury, completeness of aneurysm obliteration, premature rupture
of aneurysms, and surgical outcome were analyzed. GOS of 4 and 5 was defined as favorable
outcomes, whereas GOS of 1–3 was defined as an unfavorable outcome.
Results
Among 97 patients with MCA aneurysms, 13 underwent microsurgical clipping of anteroinferior-projecting
MCAB aneurysms using the DTSA [[Table 1 ]]. Ten patients (76.9%) suffered from ruptured MCAB aneurysms, including 8 (80%)
with initial WFNS grades 1–2 (good grade). Three patients (23.1%) had unruptured MCAB
aneurysms, which are incidentally discovered. Increased size of the aneurysm was detected
in the serial imaging in one patient (case No. 1). One patient (case No. 3) with unruptured
aneurysm had previous subarachnoid hemorrhage from a contralateral MCAB aneurysm.
Another unruptured case (case No. 13), with MCAB aneurysm and anterior temporal artery
aneurysm, suffered from A1 injury during removal of large planum sphenoidale meningioma
via contralateral pterional craniotomy and need flow augmentation bypass from superficial
temporal artery to the anterior cerebral artery.
Table 1: Patient data, middle cerebral artery bifurcation aneurysm characteristic, surgical
complications, and outcomes
Ten patients (76.9%) were classified as good grade including eight ruptured and two
unruptured cases. Three patients had poor grade (23.1%), including two with ruptured
(case No. 6, 9) and one with unruptured aneurysm (case No. 13) who has preoperative
paraparesis from the previous surgery. Grade 3 of the modified Fisher grade was detected
in 9 patients (90%) with ruptured aneurysm. The average size of the aneurysm was 4.2
mm. Aneurysm projections were anterior in six patients (46.1%), anteroinferior in
four (30.8%), inferior in two (15.4%), and anterolateral in one (7.7%). Curvatures
of the M1 segment of MCA were posterior in six (46.1%) and posterosuperior in six
patients (46.1%). The straight course of the M1 segment was detected in one patient
(7.7%).
On the preoperative CT angiography (CTA), the MCAB located at or below the Sylvian
fissure line [[[Figure 4 ]], a straight line from the limen insulae to lateral Sylvian fissure in coronal plane]
was detected in all patients [[Figure 4 ]]a, [[Figure 4 ]]b and [[Figure 4 ]]d, except in one patient (case No. 9) with MCAB located above the line [[Figure 4 ]]c. The early distal M1 exposure was intraoperatively achieved in all patients, except
in one patient (case No. 9) with MCAB located above the line. Premature rupture of
the aneurysm occurred in one patient (7.7%, case No. 9) who achieved favorable outcomes
at 3 months postoperatively. The lenticulostriate artery injury did not occur intraoperatively
in all patients. No brain contusion was demonstrated on postoperative CT scan.
Figure 4: The Sylvian fissure line (dashed line) and MCAB (asterisk) were marked in coronal
computed tomography angiography. (a) In case No. 2, the MCAB was located below the
Sylvian fissure line. (b) In case No. 4, the MCAB was located at the Sylvian fissure
line. (c) In case No. 9, the MCAB was located above the Sylvian fissure line. (d)
In case No. 13, the MCAB was located below the Sylvian fissure line. MCAB - Middle
cerebral artery bifurcation
Favorable outcome at 3 months was achieved in 100% and 84.6% of patients with good
grade and all patients, respectively. Unfavorable outcome in observed in two patients
due to severe vasospasm with hemorrhagic infarction (case No. 6) and preoperative
paraparesis from previous surgery (case No. 13). Clinical vasospasm causing postoperative
hemiparesis was detected in three patients (23.1%, case No. 6, 8, 9), which all have
modified Fisher grade 3. Transient hemiparesis was detected in 2 patients who completely
recovered within 3 months. The rate of complete aneurysm obliteration and preservation
of both M2 branches was 100%. New postoperative neurological deficit at 3 months postoperatively
was detected in one patient (case No. 6) who suffered severe vasospasm with hemorrhagic
infarction.
Illustrative cases
Case 1
A 67-year-old female patient [case No. 2 in [[Table 1 ]]] suddenly presented with headache and full level of consciousness (WFNS Grade 1).
CT and CTA revealed a thick subarachnoid hemorrhage (modified Fisher Grade 3), a 4-mm
right MCAB aneurysm with anterior projection, and a posterosuperior curved right M1
segment [[Figure 2 ]]a,[[Figure 2 ]]b,[[Figure 2 ]]c. The DTSA was performed for neck clipping without premature aneurysm rupture [[Figure 2 ]]d to [[Figure 2 ]]i. The direction of the approach was depicted by the arrow in [[Figure 2 ]]a,[[Figure 2 ]]b,[[Figure 2 ]]c. Aneurysm clipping was performed in the ideal closure line [[Figure 3 ]]a. Postoperative CTA showed complete obliteration of the aneurysm with preservation
of both M2 branches [[Figure 5 ]]a and [[Figure 5 ]]b. The postoperative period was uneventful. The patient had a GOS of 5 at 3 months
postoperatively.
Figure 5: Postoperative CTA of case No. 2. Revealed complete aneurysm obliteration and preservation
of both M2 branches. (a) Three-dimensional CTA excluding the base of the skull in
anteroposterior view. (b) Three-dimensional CTA including the base of the skull in
superior view. CTA - Computed tomography angiography
Case 2
A 47-year-old male patient [case No. 9 in [[Table 1 ]]] presented with sudden alteration of consciousness (WFNS Grade 4). Diffuse thick
SAH (modified Fisher Grade 3), a left anterior-projecting MCAB aneurysm, and posterior
curved M1 segment were detected on CTA [[Figure 6 ]]a,[[Figure 6 ]]b,[[Figure 6 ]]c. The MCAB was located above the Sylvian fissure line [[Figure 4 ]]c. The DTSA was performed for aneurysm clipping. The premature aneurysm rupture
was occurred before the exposure of the M1 segment. The tentative clipping on the
aneurysm dome was immediately performed to stop the bleeding [[Figure 6 ]]d. After controlling the M1 segment, the aneurysm neck, superior trunk, and inferior
trunk of M2 branches were identified [[Figure 6 ]]e, and then definite aneurysm clipping was performed [[Figure 6 ]]f. Postoperative CTA revealed complete obliteration of the aneurysm with preservation
of both M2 branches [[Figure 7 ]]a and [[Figure 7 ]]b. Transient right hemiparesis due to clinical vasospasm occurred in the postoperative
period. The patient was discharged with right hemiparesis, and she had a GOS of 5
at 3 months postoperatively.
Figure 6: (a-c) Preoperative CTA of case No. 9. showed the anterior-projecting MCAB aneurysm
in anteroposterior, superior, and left posterolateral views. (d) Intraoperative images
showed the tentative clipping on the aneurysm dome after a premature rupture. (e)
The distal M1 segment (asterisk), superior trunk (S), and inferior trunk (I) of M2
were identified. (f) The final view after the definite clipping. MCAB - Middle cerebral
artery bifurcation, CTA - Computed tomography angiography
Figure 7: Postoperative CTA of case No. 9 revealed complete aneurysm obliteration and preservation
of both M2 branches. (a) Three-dimensional CTA without the base of the skull in anteroposterior
view. (b) Three-dimensional CTA with the base of the skull in superior view. CTA -
Computed tomography angiography
Discussion
Middle cerebral artery bifurcation aneurysm management: Clip or coil
For MCA aneurysms, several studies showed that the efficacy of the surgical clipping
is better than the coiling with regard to the occlusion rate.[[4 ]],[[5 ]],[[6 ]],[[7 ]],[[16 ]] However, with regard to the functional outcome and procedural complications, the
endovascular approach was comparable to the surgical clipping.[[5 ]],[[7 ]] MCAB aneurysms typically have a wide neck that usually incorporates the origin
of one or both M2 branches. As a result of this configuration, surgical clipping played
a major role for the treatment of MCAB aneurysms with lower complication and morbidity
rates.[[17 ]]
Surgical approaches for clipping Middle cerebral artery bifurcation aneurysms
The traditional pterional approach by Yasargil et al. for MCA aneurysm utilized proximal
to distal dissection of the MCA (proximal transsylvian approach).[[8 ]] Pritz et al. proposed the DTSA for MCAB aneurysms particularly when a long M1 is
present without incidence of premature aneurysm rupture. The advantages of this approach
include a relatively short length of Sylvian fissure dissection and minimal brain
retraction and injury, whereas its important drawback is the lack of early M1 exposure
for proximal control.[[2 ]],[[9 ]],[[18 ]]
The aneurysm projections and the course of the M1 segment affected the selection of
surgical approaches. Projections of MCAB aneurysms with hemodynamic relation to the
course of M1 segment were divided in three types: (1) inferior projection with superiorly
curved M1, (2) superior projection with inferiorly curved M1, and (3) superolateral
projection with the oblique course of M1.[[2 ]] Dashti et al. classified MCAB aneurysms into five types: Superior projection, inferior
projection, lateral projection, medial projection, and complex aneurysms. Different
surgical strategies were suggested for each type of aneurysms. For the inferior projection
aneurysm, they suggested the proximal to distal Sylvian fissure dissection (proximal
transsylvian approach). With frontal lobe retraction, the ICA, M1, and frontal M2
branches were sequentially identified. The temporal lobe retraction was suggested
to be avoided due to the risk of premature rupture.[[1 ]] Elsharkawy et al.[[19 ]] and Di Bonaventura et al.[[20 ]] proposed the technique of focused opening of the Sylvian fissure for the microsurgical
management of MCA aneurysms. With this technique, a 10–15-mm Sylvian opening was sufficient
for proximal control and aneurysm clipping without an extensive Sylvian fissure dissection.
The part of the Sylvian fissure planned to be opened should be preoperatively localized
from CTA using the relation of the aneurysm neck and sphenoid ridge.
Different surgical approaches and various types of aneurysm projection have been proposed
in previous studies; however, the appropriate approach for each type of aneurysm projection
has not been clearly suggested and discussed.[[1 ]],[[2 ]],[[8 ]],[[9 ]],[[18 ]] With regard to aneurysm projection and course of M1 segment, the risk of premature
rupture due to a lack of early M1 exposure, a disadvantage of DTSA, was high in lateral-or
superior-projecting MCAB aneurysms, but low for anteroinferior-projecting aneurysms.
Authors used the DTSA for clipping of anteroinferior-projecting MCAB aneurysms because
the exposure of the M1 trunk, embedded in the deep part of the Sylvian fissure, is
difficult, and early exposure of distal M1 from the dorsal surface is easily obtained.
In addition, high risk of brain injury from extensive proximal Sylvian fissure dissection
and premature aneurysm rupture during frontal lobe retraction, especially in patients
with aneurysm that projects anteriorly and adheres to the sphenoid wing, from the
proximal transsylvian approach were our rationale for the selection of the DTSA.
Advantages and special considerations of the distal transsylvian approach
With the use of DTSA in the current study, authors used two retractor blades for the
frontal and temporal lobe retraction in the intrasylvian retraction manner, and retractor
blades were applied as the brain holder after a wide dissection of the Sylvian fissure;
therefore, the risk of premature rupture was minimized and the wide operative field
provided the sufficient area for the ideal closure line clipping that needs various
directions of the aneurysm clip application.[[13 ]],[[14 ]],[[15 ]]
For the MCAB aneurysm that projects anteroinferiorly, the course of the M1 segment
usually curves superoposteriorly into the deep part of the Sylvian fissure and the
frontal and temporal operculum that form the superficial part of the Sylvian fissure
usually adhere tightly.[[2 ]] With the DTSA, the middle part of the M1 segment, which usually locates in the
deep area of the Sylvian fissure, was not required; therefore, brain injury due to
extensive Sylvian fissure dissection can be avoided. The distal M1 segment, which
is located more superficial in the Sylvian fissure, was able to early identify the
proximal control using the distal approach.
The lenticulostriate arteries usually arise from the dorsal surface of the proximal
M1 segment and were rarely found to be associated with M1 bifurcation.[[3 ]] The DTSA, requiring exposure and proximal control at the distal M1 segment, may
provide a low risk of lenticulostriate artery injury as the 0% incidence of the artery
injury in the current study; however, the temporary clip on the distal M1 should be
carefully placed to avoid damage to these arteries.
Ulm et al. reported that the MCAB occurs at/or distal to the genu of MCA in 94% of
patients and a majority of MCAB aneurysms were associated with long M1 segment.[[3 ]] As the result of the current study, premature aneurysm rupture occurred in one
patient with the MCAB located above the Sylvian fissure line (high-positioned MCAB)
and underneath the limen insulae. Early exposure of the distal M1 was not achieved
in this patient. Therefore, special precaution should be taken when clipping the anteroinferior-projecting
MCAB aneurysm with high-positioned MCAB. The proximal M1 should be prepared via the
subfrontal route before the distal Sylvian fissure dissection, and a tentative clipping
on the aneurysm dome may be performed before dissecting the aneurysm neck and distal
M1.
Study limitations
Limitations of this study were its retrospective descriptive nature and small number
of participants due to the specific type of aneurysms and specific approach. With
our best knowledge, this is the first clinical study regarding the use of early exposure
of the dorsal surface of M1 segment via DTSA for anteroinferior-projecting MCAB aneurysms
with clinical outcomes.
Conclusions
DTSA, which simplifies the early exposure of the dorsal surface of distal M1, is safe
and effective for clipping anteroinferior-projecting MCAB aneurysms without extensive
Sylvian fissure dissection. High-positioned MCAB requires careful dissection of the
aneurysm neck with consideration of tentative clipping preparation.
