Surgical Neurology 67 (2007) 441 – 456

www.surgicalneurology-online.com
Aneurysm–Rainbow Team/Helsinki
Microneurosurgical management of middle cerebral
artery bifurcation aneurysms
Reza Dashti, MDa, Juha Hernesniemi, MD, PhDa,4, Mika Niemel7, MD, PhDa,
Jaakko Rinne, MD, PhDc, Matti Porras, MD, PhDb, Martin Lehecka, MDa, Hu Shen, MDa,
Baki S. Albayrak, MDa, Hanna Lehto, MDa, P7ivi Koroknay-Pál, MD, PhDa,
Rafael Sillero de Oliveira, MDa, Giancarlo Perra, MDa, Antti Ronkainen, MD, PhDc,
Timo Koivisto, MD, PhDc, Juha E. J77skel7inen, MD, PhDc
Departments of aNeurosurgery and bRadiology, Helsinki University Central Hospital, 00260 Helsinki, Finland
c
Department of Neurosurgery, Kuopio University Hospital, 70211 Kuopio, Finland
Received 3 November 2006; accepted 28 November 2006

Abstract Background: Of the MCA aneurysms, those located at the main bifurcation of the MCA (MbifA)
are by far the most frequent. The purpose of this article is to review the practical anatomy,
preoperative planning, and avoidance of complications in the microsurgical dissection and clipping
of MbifAs.
Methods: This review, and the whole series on intracranial aneurysms, is mainly based on the
personal microneurosurgical experience of the senior author (JH) in 2 Finnish centers (Helsinki and
Kuopio), which serve without patient selection the catchment area in southern and eastern Finland.
Results: These 2 centers have treated more than 10 000 patients with intracranial aneurysms since
1951. In the Kuopio Cerebral Aneurysm Data Base of 3005 patients with 4253 aneurysms, MbifAs
formed 30% of all ruptured aneurysms, 36% of all unruptured aneurysms, 35% of all giant
aneurysms, and 89% of all MCA aneurysms. Importantly, in 45%, rupture of MbifA caused an ICH.
Conclusions: Middle cerebral artery bifurcation aneurysms are often broad necked and may involve
one or both branches of the bifurcation (M2s). The anatomical and hemodynamic features of MbifAs
make them usually more favorable for microneurosurgical treatment. In population-based services,
MbifAs are frequent targets of elective surgery (unruptured), acute surgery (ruptured), and
emergency surgery (large ICH), even advanced approaches (giant). The challenge is to clip the
neck adequately, without neck remnants, while preserving the bifurcational flow.
D 2007 Elsevier Inc. All rights reserved.
Keywords: Aneurysm; Middle cerebral artery; Bifurcation; Surgery; Microsurgical technique; Clipping; Subarachnoid
hemorrhage

Abbreviations: CSF, cerebrospinal fluid; CTA, computed tomography angiography; DSA, digital subtraction angiography; EC-IC anastomosis, extracranial
to intracranial anastomosis; ELANA, eximer laser-assisted nonocclusive anastomosis; ICA, internal carotid artery; ICG, indocyanine green; ICH, intracerebral
hematoma; IC-IC anastomosis, intracranial to intracranial anastomosis; ICP, intracranial pressure; ISUIA, International Study of Unruptured Intracranial
Aneurysms; LLAs, lateral lenticulostriate arteries; LSO, lateral supraorbital; MbifA, middle cerebral artery bifurcation aneurysm; MCA, middle cerebral artery;
MdistA, middle cerebral artery distal aneurysm; M1A, middle cerebral artery trunk (M1) aneurysm; MRA, magnetic resonance angiography; SAH,
subarachnoid hemorrhage; SELANA, sutureless eximer laser–assisted nonocclusive anastomosis.
4 Corresponding author. Tel.: +358 50 4270220; fax: +358 9 47187560.
E-mail address: juha.hernesniemi@hus.fi (J. Hernesniemi).

0090-3019/$ – see front matter D 2007 Elsevier Inc. All rights reserved.
doi:10.1016/j.surneu.2006.11.056
442 R. Dashti et al. / Surgical Neurology 67 (2007) 441 – 456

1. Introduction Table 2
Patients with MbifAs in a consecutive and population-based series of 3005
1.1. Middle cerebral artery bifurcation aneurysms patients with 4253 intracranial aneurysms from 1977 to 2005 in the Kuopio
Cerebral Aneurysm Data Base
Of the MCA aneurysms, those located at the main
No. of patients No. of aneurysms
bifurcation of the MCA (MbifA) (Table 1) are by far the
most frequent [11,20,21,39,40,45,47-49,58,59,78]. In popu- Whole series 3005 4253
Patients with primary SAH 2365 3325
lation-based services, MbifAs are frequent targets of elective
Patients without primary SAH 640 928
surgery (unruptured), acute surgery (ruptured), and emer- MCA aneurysms 1456 1704
gency surgery (large ICH), even advanced approaches M1As 221 (15%) 241 (14%)
(giant). Middle cerebral artery bifurcation aneurysms are MbifAs 1166 (80%) 1385 (81%)
often broad necked and may be dysmorphic in shape MdistAs 69 (5%) 78 (5%)
Ruptured MCA aneurysms 802 802
involving 1 or both branches of the bifurcation (M2s). The
M1As 73 (9%) 73 (9%)
challenge is to clip the neck adequately, without neck MbifAs 711 (89%) 711 (89%)
remnants, while preserving the bifurcational flow. MdistAs 18 (2%) 18 (2%)
MbifA
1.2. Purpose of review Total 1166 1385
Unruptured MbifAs 455 (39%) 674 (49%)
This review, and the whole series on intracranial Ruptured MbifAs 711 (61%) 711 (51%)
aneurysms, is intended for neurosurgeons who are sub-
specializing in neurovascular surgery. The purpose is to
from 43% to 49% (Table 2) suggests that MRI and CT
review the practical anatomy, preoperative planning, and
studies increasingly disclosed unruptured MCA aneurysms
avoidance of complications in the microsurgical dissection
in the Finnish population.
and clipping of MbifAs.
2.1. Ruptured and unruptured MbifAs
1.3. Authors
Of the 3005 patients with aneurysm, 2365 (79%) had a
This review is mainly based on the personal micro-
primary aneurysmal subarachnoid hemorrhage. The total
neurosurgical experience of the senior author (JH) in 2
number of unruptured aneurysms in the series was 1888.
Finnish centers (Helsinki and Kuopio), which serve without
Table 2 presents the incidence of MbifAs as compared to the
selection the catchment area in the southern and eastern
whole series. Middle cerebral artery bifurcation aneurysm
Finland. These two centers have treated more than 10 000
was the most frequent site for both ruptured (n = 711, 34%)
patients with aneurysm since 1951.
and unruptured (n = 674, 36%) aneurysm in the series.
Middle cerebral artery bifurcation aneurysm was also the
2. Occurrence of MbifAs most frequently associated aneurysm in SAH cases (298
[12%] of the 2365 patients with SAH). Table 3 presents the
Middle cerebral artery aneurysms are most frequently characteristics of MbifAs with comparison between rup-
located at the main bifurcation of the MCA (MbifAs) tured and unruptured groups. Interestingly, 29% of the
[11,20,39,40,45,47-49,58,59,78]. Middle cerebral artery ruptured MbifAs were less than 8 mm in size, which shows
bifurcation aneurysms comprised 82.6% of the MCA that small aneurysms are also dangerous and puts into
aneurysms of YaYargil’s series [78]. Tables 2-5 presents question the ISUIA study results [24], at least in Finland.
the clinical data of patients with MbifA in a consecutive and Among the 1704 MCA aneurysms, the 69 giant ones (4%)
population-based series of 3005 patients with 4253 intra- were most frequently located in the bifurcation (n = 55).
cranial aneurysms from 1977 to 2005 in the Kuopio Distribution of infrequent 18 fusiform aneurysms is
Cerebral Aneurysm Data Base. In the earlier analysis of presented in Table 3.
1314 patients with 1751 aneurysms from 1977 to 1992
[47,48], 561 (43%) patients had 690 MCA aneurysms, with 2.2. Associated aneurysms
MbifAs comprising 80% of the MCA aneurysms. In the
Middle cerebral artery bifurcation aneurysms are often
present series (Table 2), MbifAs comprise 81% of the MCA
associated with other aneurysms as seen in Table 4. The
aneurysms. The increase in unruptured MCA aneurysms
most frequently associated aneurysm was MCA bifurcation
in 204 (17%) patients. Bilateral (mirror) MbifAs were seen
Table 1 in 165 (14%) patients.
Three categories of MCA aneurysms
Location 2.3. Intracerebral hematoma

M1A Main trunk of MCA, between ICA bifurcation and main Middle cerebral artery bifurcation aneurysms bled
MCA bifurcation frequently into the adjacent brain in as much as 45% of
MbifA Main MCA bifurcation the 711 ruptured cases. Most ICHs (84%) projected toward
MdistA Branches distal to main MCA bifurcation or cortical branches the temporal lobe (Table 5). Intracerebral hematoma is
 R. Dashti et al. / Surgical Neurology 67 (2007) 441 – 456 443

Table 3
Characteristics of MbifAs and comparison between ruptured and unruptured groups
Ruptured Unruptured Total

No. of aneurysms 711 (51%) 674 (49 %) 1385 (100%)

Median aneurysm size mm 10 (range, 1-80) 5 (range, 1-65) 8 (range, 1-80)
Aneurysm size
Small ( b 7 mm) 206 (29%) 390 (57%) 596 (43%)
Medium (7-14 mm) 341 (48%) 241 (36%) 582 (42%)
Large (15-24 mm) 121 (17%) 31 (5%) 152 (11%)
Giant ( z 25 mm) 43 (6%) 12 (2%) 55 (4%)
Aneurysm side
Right 407 (57%) 367 (54%) 774 (56%)
Left 304 (43%) 307 (46%) 611 (44%)
Fusiform MCA aneurysms 4 14 18
Fusiform M1A 0 6 (42%) 6 (33%)
Fusiform MbifA 3 (75%) 5 (36%) 8 (45%)
Fusiform MdisA 1 (25%) 3 (21%) 4 (22%)
Data are based on number of aneurysms.

thought to affect the outcome mainly by the initial brain what parallel to and supply the insula [16]. In the study of
damage [37,38,47,48,79]. Tqre et al [66], M2s are seldom of equal diameter (15%) and
usually the inferior (temporal) trunk is dominant (50%).
Occasionally, a thick frontal or temporal cortical branch of
3. Microsurgical anatomical considerations of MbifAs
the M1 trunk creates ba false bifurcation,Q so named by
Middle cerebral artery aneurysms can be classified into YaYargil [77], and is seen in 7.5% of the hemispheres
proximal (M1A), bifurcational (MbifA), and distal types studied by Tqre et al. [66]. Lateral lenticulostriate arteries
(MdistA) (Table 1). Proximal MCA aneurysms or M1As are originate mainly from the M1 trunk (see below), and
located in the main trunk (M1), between the bifurcation of identification of their origin should help to distinguish the
the ICA and the main bifurcation of MCA [6]. Middle true MCA bifurcation. In 55% of the hemispheres studied
cerebral artery bifurcation aneurysm is the focus of the by Tqre et al, the dominant M2 trunk bifurcated soon after
present article. Distal MCA aneurysm, originating from the the main bifurcation (intermediate branch). This gave an
M2 or more distal branches of MCA, will be the focus of a impression of trifurcation in 12.5%, and quadrifurcation was
separate article. seen in 2.5% when both M2s bifurcated immediately [66].
Middle cerebral artery bifurcation aneurysms are located Umansky et al [67] reported bifurcation in 66%, trifurcation
in the sylvian fissure, between the frontal and temporal in 26%, and quadrifurcation in 4%, and Gibo et al [16]
lobes, where diverse vascular anatomy may affect the reported bifurcation in 78%, trifurcation in 12%, and
outcome of surgery. The sylvian fissure varies in shape multiple trunks in 10%.
and volume, and previous SAHs may toughen the arachnoid
3.2. Perforating arteries
in and on the fissure [5,77]. The venous anatomy of the
sylvian fissure is complex and varies highly [26,62,77]. Lateral lenticulostriate arteries vary much in number
Middle cerebral artery is the major terminal branch of the (1-20) and sites of origin [16,31,66,68,69,77]. Lateral
ICA supplying a large part of the cerebral hemisphere along lenticulostriate arteries mainly arise from the frontal aspect
with the insula, lentiform nucleus, and internal capsule [66]. or cortical branches of M1. However, LLAs may also
Middle cerebral artery is the most complex major cerebral arise, in up to 23%, from the MCA bifurcation, M2, or an
artery owing to its anatomical and hemodynamic features.
The detailed microneurosurgical anatomy of MCA has Table 4
been described by YaYargil [77,78] and several others Distribution of patients with single and multiple aneurysm in ruptured and
[16,50,62,66,68,69]. unruptured groups
Ruptured Unruptured Total
3.1. Middle cerebral artery bifurcation
Patients with MbifA 711 455 1166
The main trunk (M1) of the MCA starts at the carotid Single aneurysm 495 (70%) 158 (35%) 653 (56%)
bifurcation in the sylvian cistern. M1 runs laterally until the Multiple aneurysms 216 (30%) 297 (65%) 513 (44%)
level of limen insula where it splits usually into 2 Associated MbifAs 109 95 204
Unilateral 17 10 27
(bifurcation) branches (M2s), the superior (frontal) and Bilateral 85 80 165
inferior (temporal) ones [66,77] (Fig. 1). The location of the Both 7 5 12
bifurcational complex in the sylvian fissure, depending on Associated aneurysms 107 202 309
the length of M1, as well as the angioarchitecture of the at other sites
complex varies considerably [16,66,77,78]. M2s run some- Data are based on number of patients.
444 R. Dashti et al. / Surgical Neurology 67 (2007) 441 – 456
Table 5
Incidence and locations of intracerebral hematoma and occurrence of
hydrocephalus in patients with ruptured MbifAs
No. of patients
Ruptured MbifAs 711
ICH 322 (45%)
Temporal 271
Frontal 50
Parietal 1
Hydrocephalus 206 (29%)
accessory M2 [31,66] (Fig. 2). Lateral lenticulostriate
arteries enter the brain via the central and lateral parts of
the anterior perforating substance and supply the sub-
stantia innominata, the putamen, the globus pallidus, and
the head and body of the caudate nucleus, the internal
capsule, and, the adjacent corona radiata, and the central
portion of the anterior commissure and MbifAs in general
may involve LLAs at their branching sites [69,78],
displacing, compressing, distorting, or stretching them
[31]. During dissection and exposure of the distal M1
trunk and the bifurcation, and during clipping of MbifAs
that project toward the insula (see below), the site and
pattern of exit of LLAs are of special concern [66,77]
(Fig. 2). Furthermore, while mobilizing the bifurcation
and the M2 trunks, it is of great importance to avoid
severing the pial vessels supplying the insula. The safety
margin in mobilizing M2 trunks is narrow in this region,
3 to 5 mm [69].
3.3. Orientation of MbifAs
The orientation of MbifAs in the sylvian fissure depends
on the depth of the fissure, the length and course of M1, and
the projection of the MbifA dome [36]. The orientation may
be distorted by a space-occupying ICH.
Fig. 1. Intraoperative view of left MCA inside the sylvian fissure. F
indicates middle cerebral artery superior (frontal) trunk; FTA, frontotem-
poral artery; T, middle cerebral artery inferior (temporal) trunk.
Fig. 2. Intraoperative view of right insular-type MbifA (see also video
MbifA-4). A indicates aneurysm; F, middle cerebral artery superior (frontal)
trunk; T, middle cerebral artery inferior (temporal) trunk.
According to the projection of the dome in the sylvian
fissure, YaYargil [78] classified MbifAs into 3 main types:
(1) Anterosuperior projection, toward the sylvian fis-
sure, subdivided into medial and lateral. The dome
may be adherent to the arachnoid coverings of the
sylvian fissure, even to the dura of the sphenoid
wing, risking early rupture during exposure.
(2) Posterior projection, between the M2s.
(3) Inferior projection, toward the insula. Lateral
lenticulostriate arteries may be inferomedially in
close relation to the aneurysm base, and their
visualization is of great importance before bipolar
reshaping of the dome and clipping of the neck.
We classify MbifAs into 5 main types:
(1) Intertruncal MbifA. The dome projects superiorly in
the coronal (AP) plane and posteriorly in the axial
plane. Intertruncal MbifAs lay between the M2s,
the base often more on the thicker M2, and M2s are
more or less involved in the base (Fig. 3).
(2) Inferior MbifA. The dome projects inferiorly in the
coronal (AP) plane and anteriorly (toward the
sphenoid ridge) in the axial plane (Fig. 4).
(3) Lateral MbifA. The dome projects laterally in the
coronal (AP) plane and laterally in the axial plane,
in the same direction as M1 (Fig. 5).
(4) Insular MbifA. The dome projects medially (toward
the insula) in the coronal (AP) plane and medially
in the axial plane (Fig. 6).
Types 2 to 4 are not intertruncal and do not principally
involve the M2s.
(5) Complex MbifA. In some dysmorphic and large or
giant aneurysms, the growth of the dome may be
multidirectional and the relation with M1 and M2s
may be a combination of the aforementioned types
(Fig. 7).
 R. Dashti et al. / Surgical Neurology 67 (2007) 441 – 456
4. Imaging of MbifAs
Digital subtraction angiography is still the present gold
standard in many centers. Multislice helical CTA is the
primary modality in our centers for several reasons:
noninvasive and quick imaging; comparable sensitivity
and specificity to DSA in aneurysms larger than 2 mm
[9,17,25,33,35,61,64,65,70,72-74,76,80]; disclosure of cal-
cifications in the walls of arteries and the aneurysm; quick
reconstruction of 3D images that, for example, show the
surgeon’s view of MbifA and the adjacent sphenoid ridge
[52,74]. Middle cerebral artery bifurcation aneurysm is the
most frequent cause of aneurysmal ICH [47]. ICHs are
temporal or insular, or frontal or deep basal, and should be
differentiated from spontaneous deep hemorrhages [23].
For intraoperative navigation, 3D CTA or DSA recon-
structions should be evaluated for the length, depth, and
course of M1 in the sylvian fissure; the projection of the
MbifA dome from the bifurcation; and, for safe clipping, the
relationship of the M2s and adjacent branches to the fundus
and the dome. The surgeon’s view of the MCA bifurcation is
in the plane of the sylvian fissure, and the sector ranges from
a straight frontal view (08) to an almost lateral view (some
908). In the workstation, 3D CTA images can be rotated
accordingly to evaluate the surgeon’s view, and a suitable
bony exposure can be performed with virtual tools. In large,
giant, and fusiform MbifAs, MRI with different sequences
along with 3D CTA helps to distinguish the true wall of the
aneurysm and the eventual intraluminal thrombosis.
5. Microsurgical strategy with MbifAs
In population-based neurovascular services, MbifAs are
frequent targets of elective surgery (unruptured), acute
surgery (ruptured), and emergency surgery (large ICH),
Fig. 3. Axial (A) and coronal (B) CTA images of a left intertruncal MbifA (see also video MbifA-1).
445
even advanced approaches (giant). Middle cerebral artery
bifurcation aneurysms are also frequent as associated
aneurysms. Middle cerebral artery bifurcation aneurysms
are often broad necked and may involve one or both M2s.
Other branches may be attached to their wall, and, less
frequently, perforators may be at risk when originating in
the bifurcational region. Consequently, the most important
problem is how to place the clip(s) so that the MbifA neck is
adequately occluded, without leaving any neck remnants
(bdog earsQ), while the bifurcational flow is preserved. One
should have a clear understanding of the length, depth, and
course of M1 in the sylvian fissure, of the projection of the
MbifA dome, and of the 3D bifurcational anatomy before
head positioning [36].
5.1. Neuroanesthesiologic principles
A general review of our neuroanesthesiologic principles
has been published previously [44].
5.2. Intracerebral hematoma
Middle cerebral artery bifurcation aneurysm is the most
frequent cause of aneurysmal ICH that requires emergen-
cy evacuation [47]. In the Kuopio series, as much as 45%
of the 711 ruptured MbifAs had bled into the adjacent
brain tissue (Table 5). In our practice, patients with
massive ICHs are transferred directly to the operating
room from acute CTA for immediate evacuation and
clipping, and processed 3D images become available until
early craniotomy. Early surgical evacuation of massive
ICH is believed to improve the outcome with ruptured
MCA aneurysms [1,2,4,18,39,47,51,53,63,75,79]. The
propensity for ICH may explain the higher than average
management morbidity and mortality of patients with
MbifA [47].
446 R. Dashti et al. / Surgical Neurology 67 (2007) 441 – 456

Fig. 4. Axial (A), coronal (B), and 3D reconstruction CTA images (C) of a right inferior MbifA (see also video MbifA-2).

5.3. Acute hydrocephalus existence of ICH or associated aneurysms. Proper approach

In case of acute hydrocephalus, 29% in the Kuopio
series (Table 5), we may start immediate ventricular
drainage to reduce the ICP and to lower the risk of brain
damage, in most cases after securing an acutely ruptured
aneurysm. In acute SAH, it is our practice to open the
lamina terminalis for CSF removal before clipping. A
catheter can be inserted in the third ventricle through the
same opening in the lamina terminalis for postoperative
ICP monitoring and CSF drainage.
5.4. Approach and craniotomy
Exposure in MbifA surgery depends on the length of M1,
the size and projection of the aneurysm dome, and the
requires a mental spatial view of the architecture of MCA
arterial tree in the sylvian fissure and its relation to the bony
landmarks. We measure the distance between ICA and
MCA bifurcations (length of M1 segment) in CTA images,
in both coronal and axial planes. This is particularly
important in planning the head position, extent of craniot-
omy, and selection of the proper place for arachnoid
opening and intrasylvian orientation. The LSO approach
[19], a less invasive modification of the pterional approach
[77] is preferred by the senior author (JH) for surgery of
MbifAs. The standard pterional approach is reserved for
selected cases with space-occupying ICH. A detailed
description of the LSO craniotomy is published elsewhere
[19], and LSO is also visualized in our M1 aneurysm (M1A)
article in this journal [6].
 R. Dashti et al. / Surgical Neurology 67 (2007) 441 – 456 447

Fig. 5. Axial (A), coronal (B), and 3D reconstruction CTA images (C) of a left lateral MbifA (see also video MbifA-3).

Briefly, the head fixed to the head frame is (a) elevated
clearly above the cardiac level, (b) rotated 258 to 308 toward
the opposite side, (c) tilted somewhat laterally for optimal
visualization of the MCA bifurcation and the aneurysm
base, and (d) minimally extended. It is an error to overturn
the head so that the temporal lobe turns over the sylvian
fissure and the aneurysm in the surgeon’s view. It is our
practice to adjust the position of the fixed head and body
during the operation as needed [19]. We prefer to use a
Sugita head frame with 4-point fixation. Besides providing
good retraction force by its fishhooks, it allows the surgeon
to rotate it during surgery. If this feature is not available the
table can be rotated as needed.
After minimal shaving, an oblique frontotemporal skin
incision is made behind the hair line (see also the video
M1A-1 in Ref. [6]). The incision is short and stops 2 to 3 cm
above the zygomatic arch. The incision is partially opened
by frontal spring hooks. The temporal muscle is split
vertically by a short incision, and one spring hook is placed
in the incision to retract the muscle toward the zygomatic
arch. The 1-layer skin-muscle flap is retracted frontally by
spring hooks until the superior orbital rim and the anterior
zygomatic arch are exposed. The extent of craniotomy
depends on the surgeon’s experience and preferences.
Usually, a small LSO craniotomy is all that is necessary
(the keyhole principle). A single burr hole is placed just
under the temporal line in the bone, the superior insertion of
the temporal muscle. The bone flap of 3  3 cm is detached
mostly by the side-cutting drill, and the basal part can be
drilled before lifting. In case of ICH or giant MbifA, a larger
craniotomy is performed toward the zygomatic arch such as
the classic pterional craniotomy. The vertical bone ridge and
lateral sphenoid ridge are drilled to create an optimal view
of the sylvian cistern.
448 R. Dashti et al. / Surgical Neurology 67 (2007) 441 – 456

Fig. 6. Axial (A), coronal (B), and 3D reconstruction CTA images (C) of a right (arrow) insular MbifA (see also video MbifA-4).

The dura is incised curvilinearly with the base
sphenoidally. Dural edges are elevated by multiple stitches,
extended over craniotomy dressings. From this point on, all
surgery is performed under the operating microscope,
including the skin closure.
5.5. Intracerebral hematoma
In case of large ICH and lack of space, after dissection
of proximal M1 to gain control, a small cortical incision is
made accordingly in the temporal side of the sylvian
fissure, or in the frontal side, avoiding the Broca’s area. If
the mass is too great, a small part of the hematoma is
evacuated through the cortical incision to gain space but
not to expose the aneurysm as this may risk rerupturing the
MbifA, which would be difficult to control through the
ICH cavity. In removing the ICH clot, before or after
clipping, minor force should be applied so as not to sever
the perforating arteries.
5.6. Cerebrospinal fluid drainage
In most unruptured MbifAs, we directly open the sylvian
fissure. In all ruptured MbifAs and in some unruptured ones,
carotid and chiasmatic cisterns are first opened to gradually
let CSF [59]. In acute SAH, we usually continue the
dissection subfrontally to open the lamina terminalis for
additional CSF removal. Intraoperative ventricular puncture
is rarely adopted.
5.7. Intrasylvian dissection toward MbifA
For intrasylvian orientation, it is important to evaluate the
preoperative images for the depth of the sylvian fissure, the
 R. Dashti et al. / Surgical Neurology 67 (2007) 441 – 456 449

Fig. 7. Axial (A), coronal (B), and 3D reconstruction images (C) of a complex large left MbifA.

length and course of M1 and M2s, and the projection and
size of the aneurysm dome [36]. In addition, CTA should be
carefully reviewed for calcifications in the M1 trunk, the
bifurcation, and the MbifA wall. Calcified plaques in the M1
wall will interfere with temporary clipping, and those at the
bifurcation area may risk rupture during clipping or result in
incomplete closure of the neck [5,21].
The extent and placement of the arachnoidal opening
depend on whether the MbifA is unruptured or ruptured,
length of M1, size of MbifA, and position of the dome
according to M2s. Ruptured status, presence of secondary
pouch, intertruncal or lateral projection of the dome, and
involvement of branches and eventually bifurcation in the
dome suggest a more distal opening of the sylvian fissure,
preparing at the same time for temporary clipping of M1 or
ICA if needed. Unruptured status, small size, and the dome
projecting toward the insula or inferiorly in the sylvian
fissure suggest a direct approach to the aneurysm. In giant
MbifAs, the sylvian fissure is opened widely, both from the
carotid cistern and distal to the aneurysm.
Dissection of the sylvian fissure is more difficult with
swollen brain in acute SAH or with adhesions from previous
SAH or microsurgery. Preservation of the dissection plane is
mandatory. The arachnoid covering is first opened with a
pair of jeweler’s forceps at the frontal side of the superficial
sylvian vein. We use a handheld saline syringe to expose the
undersurface of the arachnoid covering for both-sided
dissection and to expand spaces for further dissection, that
is, the water dissection technique of Toth [32]. Suction by its
distal shaft and bipolar forceps by its opening force are used
for gentle retraction [19]. Arachnoid membranes and strands
are cut sharply by microscissors, which can also be used as a
450 R. Dashti et al. / Surgical Neurology 67 (2007) 441 – 456
Fig. 8. Complete occlusion of MbifA while preserving blood flow in the
main trunks and perforating branches.
dissector when closed. Cottonoids can be used as soft
expanders and controllers of venous oozing in the sylvian
fissure. Retractors are applied after dissection to retain some
space for clipping, but otherwise their use is avoided [36].
All venous structures need to be preserved, but sometimes a
small bridging vein has to be severed [36,59].
6. Dissection and clipping of MbifAs
6.1. General principles
Usually, it is not advisable to dissect the dome completely
before applying the pilot clip, but sharp dissection of the
arteries around and adjacent to the base is crucial. M1, M2s,
and adjacent and perforating branches near the bifurcation
should be unhurriedly, clearly, and painstakingly visualized
before final clipping of the MbifA neck (Fig. 8).
6.2. Dissection under temporary clipping of arteries
Frequent use of temporary clips allows for safe and sharp
dissection of MbifAs and the adjacent arteries. The duration
of each temporary occlusion should be kept as short as
possible (maximally 5 minutes). Curved temporary clips
may be more suitable for distal M1 and straight ones for
M2s. Dissection and preparation of sites for temporary clips
should be performed with bipolar forceps with plump tips or
with a microdissector. The proximal clip can be close to the
bifurcation, but the distal ones should be in a distance so as
not to interfere with the visualization and permanent
clipping of the MbifA neck. It is practical to gently press
the temporary clip down by a small cottonoid to protect it
from the dissecting instruments. The distal temporary clips
are removed first and the proximal clips last. When
removed, the temporary clip should be first opened carefully
in place to determine whether any unwarranted bleeding
occurs. Quick removal may be followed by heavy bleeding
and great difficulties in placing the clip back. Furthermore,
while removing the temporary clip, even the slightest
resistance should be noted as possible involvement of a
small branch of the clip or its applier.
6.3. Clipping of MbifA neck
A proper selection of clips with different shapes and
lengths of blades, and applicators, suiting the imaging
anatomy of MbifAs, should be made ready for use. A
limited selection of final clips is needed when temporary
clipping of the arteries and bipolar shaping of the aneurysm
dome are used. If reshaping is not considered, the blade of a
single occluding clip should be 1.5 times longer than the
width of the base. We prefer inserting first a pilot clip to the
MbifA dome, preferring Sugita clips for their wide opening
distance and plump tips. Adequate dissection, proper size of
clips, and painstaking and careful checking that both blades
are placed properly up to their tips are required to preserve
the M2s and adjacent branches. If the first clip slides
exposing some of the neck, another clip may be introduced
proximal to the previous one for final closure (bdouble
clippingQ). Because the bifurcation may become kinked or
occluded after removal of the retractors, the flow should be
checked once more and papaverin applied.
6.4. Middle cerebral artery bifurcation aneurysm rupture
before clipping
Middle cerebral artery bifurcation aneurysm may rupture
while opening the sylvian fissure or dissecting the aneurysm
base. The risk of rupture is highest for the lateral type,
followed by the intertruncal type and the inferior type,
respectively (see above). The rupture site is at the dome
rather than at the base. Control should be first attempted via
suction and compression of the bleeding site with cotto-
noids. Sudden and short hypotension by cardiac arrest,
induced by intravenous adenosine [44], can be used to
facilitate quick dissection and application of a pilot clip in
case of uncontrolled bleeding. A pilot clip may be inserted
to a ruptured secondary pouch if visible. Otherwise, a
temporary clip is inserted proximally on M1, and on one or
both M2s as needed, to allow further dissection of the base
and final clipping. A small and thin-walled MbifA may
rupture at its neck during dissection. In that case, under
temporary clipping of the arteries, reconstruction of the base
by involving a part of M2(s) in the clip should be attempted.
6.5. Very small MbifAs
In very small (2-3 mm) MbifAs, clipping is difficult
because the wall is fragile. Temporary clipping of M1 and
M2s reduces intraluminal pressure and softens the dome
[36]. With minimal reduction of the arterial lumen, a thin
 R. Dashti et al. / Surgical Neurology 67 (2007) 441 – 456
portion of the healthy arterial wall is taken inside the clip
for safe closure of the neck. If the first clip slides ex-
posing some of the neck, double clipping may be applied
(see above).
6.6. Intraoperative verification of clipping
We routinely use micro-Doppler to check the patency of
M2s after clipping, but surprise occlusions would still be
seen in postoperative angiography. Noninvasive ICG
infrared angiography [42,43] is very promising in our
hands. It helps the orientation during dissection and visual-
izes wall thickness and plaques, perforating arteries, and
incomplete neck occlusion. ICG angiography will reduce
the need for invasive angiography for intraoperative
clipping control, but digital C-frame guidance with tract
memory is still needed for intraoperative assessment of flow
in giant and complex aneurysms.
6.7. Resection of MbifAs dome
When appropriate, not risking the M2s, we resect the
aneurysm dome for the final check of closure and for
research purposes [12,13]. This policy teaches one to dissect
aneurysm domes more completely and thereby avoid
closure of branching arteries (see above). Opening of the
aneurysm facilitates effective clipping by reducing intra-
luminal pressure and should be used in strong-walled, large,
and giant aneurysms (see Section 13).
7. Intertruncal MbifA
Intertruncal MbisAs project superiorly in the coronal
(AP) and posteriorly in the axial plane (Fig. 3). The dome
projects to the same direction as the M2 trunks and lies
between them. The base is often broad and involves the
origin of one M2 (the thicker one) or both. The attachment
of M2s to the base and the proximal part of the fundus
makes intertruncal MbifAs demanding to clip adequately.
7.1. Head position
The head is rotated 258 to 308 with minimal extension
and some lateral tilt, according to the length of M1, size of
the aneurysm, and site of the rupture, that is, the secondary
pouch if visible in the images.
7.2. Dissection toward the aneurysm
As the dome of the aneurysm lies between M2s, we
prefer distal opening of the sylvian fissure and careful
exposure of the frontal M2 at the beginning (video
MbifA-1). Dissection is continued to the frontal side of
the bifurcation, so as not to expose the aneurysm dome, and
then turned below to search the M1. In intertruncal MbifAs,
painstaking dissection of the base is required, with
visualization of M1 in the early phase of dissection for
temporary clip placement.
451
7.3. Temporary clipping
One temporary curved clip on M1 and a short straight clip
more on each M2 will usually soften the aneurysm so that
sharp dissection of the M2s from the aneurysm wall becomes
doable. The aneurysm may rupture while being dissected
under temporary clipping, but bleeding is not a problem and
the dissection even becomes easier. At least one M2 should
be free from the base before a pilot clip is adjusted over the
dome to control the aneurysm for final clipping.
7.4. Final clipping
After the main part of the aneurysm is dissected free under
the control of pilot clipping, the aneurysm sac is opened and
coagulated. Utmost care is taken to preserve the flow in the
M2s because MCA has less collateral flow than other major
cerebral arteries. Importantly, to obtain an optimal occlusion
of the base, that is, exclusion of the neck while preserving
flow in the M2s, the steps of temporary occlusion and final
clip adjustment should be repeated as many times as needed.
Nevertheless, the presence of calcified plaques or involve-
ment of M2s in the base may require that a proximal part of
the base is kept out of the clip(s). A ring clip accompanied by
a straight clip might be the best solution for the pilot clipping
and even for the final clipping (see above).
8. Inferior MbifA
Inferior MbifAs project inferiorly in the coronal (AP) and
anteriorly toward the sphenoid ridge, in the axial plane.
Consequently, the dome is projecting to the temporal aspect
of the surgeon’s view inside the sylvian fissure (Fig. 4).
8.1. Head position
Minor flexion of the head plus normal rotation and
increased lateral tilt provides a good view of the sphenoid
ridge and proximal part of M1. To obtain a better view of
the sphenoid ridge, the head can be lifted together with the
operating table during the operation if needed.
8.2. Dissection toward the aneurysm
After proximal opening of the sylvian fissure dissection is
continued on the frontal side of the bifurcation, and, with
slight retraction of the frontal lobe, M1 and frontal M2 are
visualized and dissected (video MbifA-2). Any retraction on
the temporal side would risk a rupture of the aneurysm.
After sharp dissection of M1 and frontal M2, the base of
the aneurysm will be exposed. Visualization of the temporal
M2 requires further careful dissection on the distal side of
the base.
8.3. Temporary clipping
One temporary curved clip on M1 and a short straight
clip on each M2 are usually applied, but both M2s can be
occluded simultaneously by a longer straight temporary
452 R. Dashti et al. / Surgical Neurology 67 (2007) 441 – 456
clip. The base of this aneurysm type is usually free of
perforating arteries or branches, and the pilot clip can be
placed easily. The dome, possibly attached to the dura,
may rupture during the application of the pilot clip but
without serious consequences.
8.4. Final clipping
The aneurysm dome is opened and the base is reshaped by
bipolar coagulation, and the final clip, usually a straight one,
is applied. Special attention must be paid to the origin of the
inferior or temporal M2 trunk which easily becomes pinched
or occluded by the distal tips of the clip blades.
9. Lateral MbifA
Lateral MbifAs project laterally in the coronal (AP) plane
and in the axial plane. In the surgeon’s view, lateral MbifAs
follow the same direction as the M1 trunk (Fig. 5).
9.1. Head position
Minor flexion of the head together with normal rotation
(258-308) and more pronounced lateral tilt provides the best
possible view of the base of the aneurysm and directs the tip
of the aneurysm away from surgical trajectory.
9.2. Dissection toward the aneurysm
Lateral MbifAs are frequently attached to the arachnoid
coverings of the sylvian fissure, risking premature rupture if
the dissection of the coverings is started improperly (video
MbifA-3). Sylvian dissection is started distally to find the
frontal M2 which is then followed toward the bifurcation
and the base of the aneurysm. To prepare for a premature
rupture, first the base of the aneurysm is carefully prepared
for a pilot clip placement over the dome, and then the
dissection is continued toward M1 to find a proper place for
a temporary clip on M1.
9.3. Temporary clipping
Temporary clips are placed on M1 and frontal M2, and
the softened aneurysm is dissected free at its base. Special
care must be taken to visualize the origin of the temporal
M2. After placement of the pilot clip, the temporary clips
can be removed.
9.4. Final clipping
The collapsed aneurysm dome is dissected and opened.
Coagulation and reshaping must be done with respect to the
origins of the M2s. A final clip is placed along the largest
diameter of the base.
10. Insular MbifA
Insular MbifA projects medially in the AP (coronal)
plane and medially in the axial plane. In the surgeon’s view,
insular MbifAs project behind the bifurcation, toward the
insular surface (Fig. 6).
10.1. Head position
The head is rotated more than normal ( N258-308) so that
the bifurcation is opened to the surgeon, making proximal
control and clipping most feasible. However, overturning
may cause hiding of the sylvian fissure by the temporal lobe.
10.2. Dissection toward the aneurysm
Because the aneurysm dome projects behind the bifur-
cation, distal to proximal dissection of the M2s, the
bifurcation and M1 are safe (video MbifA-4).
10.3. Temporary clipping
When M1 and M2s are free, 2 to 3 temporary clips are
applied (see Section 9), usually a curved clip for the M1 and
straight short clips for the M2s. With complete isolation of
the blood flow, the base of the aneurysm is carefully
dissected in its anterior and lateral parts.
10.4. Final clipping
The shortest possible pilot clip is placed on the base and
the temporary clips are removed. The position of the pilot
clip is carefully checked with particular care for small
perforating branches, which might easily be occluded, in the
same way as during clipping of ICA and basilar tip
aneurysms. We usually open and coagulate the aneurysm
dome and then replace the pilot clip with the smallest
possible clip that occludes the neck completely.
11. Complex MbifA
In this special group of dysmorphic and large or giant
aneurysms, the growth of the dome is usually multidirec-
tional and the relation of the base with M1 and M2s may be
a combination of other types (Fig. 7).
Head positioning and craniotomy should be tailored
according to the 3D relation of aneurysm with the
bifurcation. After careful dissection, temporary clips are
applied to M1 and both M2s. Softened dome may be opened
and reshaped by bipolar coagulation (see above). Usually,
adequate clipping of the aneurysm needs a combination of
clips (Fig. 9).
12. Associated aneurysms
Middle cerebral artery bifurcation aneurysms are often
associated with other aneurysms, 44% of all patients with
MbifA and 30% of those with ruptured MbifA had at least one
additional aneurysm (Table 4). Bilateral (mirror) MbifAs
were seen in 12% of the patients with MbifA. Our strategy is
to clip all aneurysms that can be exposed through the same
craniotomy [7,8,30,71,78]. This may not be advisable if the
clipping of the ruptured aneurysm is difficult or the brain is
 R. Dashti et al. / Surgical Neurology 67 (2007) 441 – 456
Fig. 9. Optimal occlusion of a complex MbifA by 2 clips.
swollen owing to acute SAH [8,46]. Contralateral M1As
close to the ICA bifurcation can be clipped via the
contralateral approach irrespective of the orientations of the
aneurysms. A contralateral MbifA can also be reached, but
only if it projects downward in the sylvian fissure and the
length of M1 is reasonable (b 20 mm) (video MbifA-5). The
contralateral approach for bilateral MCA aneurysms is not
recommended at an early learning curve.
12.1. Mini-aneurysms
Middle cerebral artery bifurcation aneurysms may also
be accompanied by mini blebs not seen in preoperative
imaging and of poorly known natural history. Depending on
the patient’s age and sclerosis of parent arteries, we may
reduce them by bipolar coagulation under temporary
clipping of the parent artery [36] or, to induce fibrosis,
overlay a small piece of cotton and fibrin glue.
13. Giant MbifAs
Middle cerebral artery is the most frequent site for giant
aneurysms. In the Kuopio series, 4% of all MbifAs and 6%
of ruptured MbifAs were giant, with greater than 25 mm in
diameter (Table 3). Combined 3D DSA, CTA, and MRI data
are necessary for a complete view on the vascular anatomy,
intraluminal thrombus, and thickness and calcifications of
the wall [21,55,60]. In published series, direct clipping
was possible in the majority of cases (38%-71%) [14,15,
27-29,36,41]. Cases considered for bypass and reconstruc-
tive surgery are obviously increasing [3].
13.1. Occlusion of parent artery
In giant MbifAs filled with organizing thrombus that
involves the base, removal of basal thrombus exposes the
453
arterial wall elements, which may induce quick rethrombosis
proximal to the clip, resulting in total thrombosis of the
bifurcation. In such cases, it may be wise to consider a bypass
operation and occlusion of M1 to exclude the aneurysm.
13.2. Clipping of giant MbifAs
Giant MbifAs often protrude to the middle fossa,
distorting the intrasylvian anatomy, and shifting the
bifurcation superiorly and medially. In these cases, clipping
is considered, supported by a preoperative IC-IC or EC-IC
bypass if necessary. Giant MbifAs of the inferior or lateral
types can usually be resected and clipped, provided that
M2s are not heavily involved in the base. Notably, some
residual base may be accepted when the basal aneurysm
wall appears strong. In ruptured cases, we prefer acute
clipping; if huge in size, calcified wall or complex neck
anatomy is not an obstacle. The operative room setup and
patient’s positioning should allow intraoperative angiogra-
phy and endovascular supporting approaches.
The head position is adjusted for a better view of the
proximal M1 [36]. Classical pterional approach with a large
enough bone flap, also to the medial frontobasal direction, is
undertaken to allow specific neurovascular techniques. For
adequate visualization of the aneurysm base, an extensive
exposure of the sylvian fissure is needed. Internal carotid
artery bifurcation and proximal M1 and M2s (distal to the
aneurysm) should be exposed and prepared for temporary
clipping. In patients with ICH, we prefer a combination of
transsylvian and superior temporal approaches. Here,
besides the evacuation of a part of the hematoma, a narrow
cortical incision and subpial resection may provide a better
view of the aneurysm base and branches [22,36]. Lamina
terminalis is opened to let CSF drain.
Clips of proper lengths and configurations are selected.
Temporary clips are inserted into proximal M1 and M2s,
and the aneurysm dome is incised with a knife for internal
decompression, performed usually by suction or, in case of
major thrombus, by ultrasonic aspirator [21]. Intraluminal
thrombus is carefully removed, and the decompressed dome
is clamped between the neck and the incision by a
mosquito-like vascular clamp, used in vascular surgery.
The vascular clamp softens the base for aneurysm clips and
also prevents slipping of intraluminal thrombus inside M2s.
The lumen is irrigated copiously by saline. Then the dome is
usually reduced to allow for final dissection of the neck
anatomy before deciding how to perform the final clipping.
In case of extensive atheroma, it is dangerous to remove it
down to the base and some part of it is left out of the clip so
as not to occlude the trunks.
Strong aneurysms require several clips [55-57,60]. If the
first clip slides on a broad base, a ring clip can be first
inserted to compress a part of the neck, and a straight
second clip is placed proximally to close the remaining neck
inside the ring of the first clip (Drake’s tandem-clipping
technique) [5,10,21,55]. If required, some base is left so as
454 R. Dashti et al. / Surgical Neurology 67 (2007) 441 – 456
not to occlude the M2s. Patency of arteries is checked by
Doppler and angiography. Removal of intraluminal throm-
bus may induce quick rethrombosis, and therefore we
also advocate early postoperative angiography to find
surprise occlusions.
14. Fusiform MbifAs
Often, reconstruction of a fusiform aneurysm may be
achieved by clip(s) excluding the bbeer bellyQ from the
circulation. For the rest, other techniques like a sling around
the aneurysm with a clip and/or wrapping with cottonoids
and glue to enhance the scarring have been tried. However,
bypass operation followed by occlusion of the parent artery
is the treatment of choice.
15. Bypass operations and arteriotomies
Preoperative high-flow EC-IC or IC-IC bypass using the
ELANA or SELANA techniques [54], or low-flow super-
ficial temporal artery–MCA bypass, may be considered in
large or giant MbifAs, when the exclusion of the neck from
the parent and branching arteries cannot be performed [21].
A comprehensive neurovascular team should be prepared to
perform intraoperative arteriotomies, for example, to re-
move coils or thrombi, and intraoperative EC-IC or IC-IC
bypasses, also in case of emergency.
16. Clipping after inappropriate clipping or failed
coiling
The best moment to treat aneurysm is the first moment.
Intraoperative verification of clipping by angiography
reduces the rate of inappropriate clipping. Scarring after
improper clipping or occlusive material inside the aneurysm
after failed coiling makes later microsurgical occlusion
complicated and sometimes impossible. To reduce redo
surgeries, aneurysms should be treated in specialized centers
with a high flow of cases and an experienced team
mastering exosurgery and endosurgery [34].
Acknowledgments
We thank Mr Ville K7rpijoki for excellent technical
assistance.
Appendix A. Supplementary data
Supplementary data associated with this article can be
found, in the online version, at doi:10.1016/j.surneu.
2006.11.056.
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