Micron Euro Surgical Management of Middle Cerebral Artery Bifurcation Aneurysms

Surgical Neurolog

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-Pal, 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, FinlandcDepartment of Neurosurgery, Kuopio University Hospital, 70211 Kuopio, Finland

Received 3 November 2006; accepted 28 November 2006

www.surgicalneurology-online.com

Abstract Background: Of the MCA aneurysms, those located at the main bifurcation of the MCA (MbifA)

0090-3019/$ – see fro

doi:10.1016/j.surneu.2

Abbreviations: CS

to intracranial anastom

hematoma; IC-IC ana

Aneurysms; LLAs, lat

MdistA, middle cere

subarachnoid hemorrh

4 Corresponding

E-mail address: ju

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 10000 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

y 67 (2007) 441–456

nt matter D 2007 Elsevier Inc. All rights reserved.

006.11.056

F, cerebrospinal fluid; CTA, computed tomography angiography; DSA, digital subtraction angiography; EC-IC anastomosis, extracranial

osis; ELANA, eximer laser-assisted nonocclusive anastomosis; ICA, internal carotid artery; ICG, indocyanine green; ICH, intracerebral

stomosis, intracranial to intracranial anastomosis; ICP, intracranial pressure; ISUIA, International Study of Unruptured Intracranial

eral lenticulostriate arteries; LSO, lateral supraorbital; MbifA, middle cerebral artery bifurcation aneurysm; MCA, middle cerebral artery;

bral artery distal aneurysm; M1A, middle cerebral artery trunk (M1) aneurysm; MRA, magnetic resonance angiography; SAH,

age; SELANA, sutureless eximer laser–assisted nonocclusive anastomosis.

author. Tel.: +358 50 4270220; fax: +358 9 47187560.

[email protected] (J. Hernesniemi).

Table 2

Patients with MbifAs in a consecutive and population-based series of 3005

patients with 4253 intracranial aneurysms from 1977 to 2005 in the Kuopio

Cerebral Aneurysm Data Base

No. of patients No. of aneurysms

Whole series 3005 4253

Patients with primary SAH 2365 3325

Patients without primary SAH 640 928

MCA aneurysms 1456 1704

M1As 221 (15%) 241 (14%)

MbifAs 1166 (80%) 1385 (81%)

MdistAs 69 (5%) 78 (5%)

Ruptured MCA aneurysms 802 802

M1As 73 (9%) 73 (9%)

MbifAs 711 (89%) 711 (89%)

MdistAs 18 (2%) 18 (2%)

MbifA

Total 1166 1385

Unruptured MbifAs 455 (39%) 674 (49%)

Ruptured MbifAs 711 (61%) 711 (51%)

R. Dashti et al. / Surgical Neurology 67 (2007) 441–456442

1. Introduction

1.1. Middle cerebral artery bifurcation aneurysms

Of the MCA aneurysms, those located at the main

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-

lation-based services, MbifAs are frequent targets of elective

surgery (unruptured), acute surgery (ruptured), and emer-

gency surgery (large ICH), even advanced approaches

(giant). Middle cerebral artery bifurcation aneurysms are

often broad necked and may be dysmorphic in shape

involving 1 or both branches of the bifurcation (M2s). The

challenge is to clip the neck adequately, without neck

remnants, while preserving the bifurcational flow.

1.2. Purpose of review

This review, and the whole series on intracranial

aneurysms, is intended for neurosurgeons who are sub-

specializing in neurovascular surgery. The purpose is to

review the practical anatomy, preoperative planning, and

avoidance of complications in the microsurgical dissection

and clipping of MbifAs.

1.3. Authors

This review is mainly based on the personal micro-

neurosurgical experience of the senior author (JH) in 2

Finnish centers (Helsinki and Kuopio), which serve without

selection the catchment area in the southern and eastern

Finland. These two centers have treated more than 10000

patients with aneurysm since 1951.

2. Occurrence of MbifAs

Middle cerebral artery aneurysms are most frequently

located at the main bifurcation of the MCA (MbifAs)

[11,20,39,40,45,47-49,58,59,78]. Middle cerebral artery

bifurcation aneurysms comprised 82.6% of the MCA

aneurysms of YaYargil’s series [78]. Tables 2-5 presents

the clinical data of patients with MbifA in a consecutive and

population-based series of 3005 patients with 4253 intra-

cranial aneurysms from 1977 to 2005 in the Kuopio

Cerebral Aneurysm Data Base. In the earlier analysis of

1314 patients with 1751 aneurysms from 1977 to 1992

[47,48], 561 (43%) patients had 690 MCA aneurysms, with

MbifAs comprising 80% of the MCA aneurysms. In the

present series (Table 2), MbifAs comprise 81% of the MCA

aneurysms. The increase in unruptured MCA aneurysms

Table 1

Three categories of MCA aneurysms

Location

M1A Main trunk of MCA, between ICA bifurcation and main

MCA bifurcation

MbifA Main MCA bifurcation

MdistA Branches distal to main MCA bifurcation or cortical branches

from 43% to 49% (Table 2) suggests that MRI and CT

studies increasingly disclosed unruptured MCA aneurysms

in the Finnish population.

2.1. Ruptured and unruptured MbifAs

Of the 3005 patients with aneurysm, 2365 (79%) had a

primary aneurysmal subarachnoid hemorrhage. The total

number of unruptured aneurysms in the series was 1888.

Table 2 presents the incidence of MbifAs as compared to the

whole series. Middle cerebral artery bifurcation aneurysm

was the most frequent site for both ruptured (n = 711, 34%)

and unruptured (n = 674, 36%) aneurysm in the series.

Middle cerebral artery bifurcation aneurysm was also the

most frequently associated aneurysm in SAH cases (298

[12%] of the 2365 patients with SAH). Table 3 presents the

characteristics of MbifAs with comparison between rup-

tured and unruptured groups. Interestingly, 29% of the

ruptured MbifAs were less than 8 mm in size, which shows

that small aneurysms are also dangerous and puts into

question the ISUIA study results [24], at least in Finland.

Among the 1704 MCA aneurysms, the 69 giant ones (4%)

were most frequently located in the bifurcation (n = 55).

Distribution of infrequent 18 fusiform aneurysms is

presented in Table 3.

2.2. Associated aneurysms

Middle cerebral artery bifurcation aneurysms are often

associated with other aneurysms as seen in Table 4. The

most frequently associated aneurysm was MCA bifurcation

in 204 (17%) patients. Bilateral (mirror) MbifAs were seen

in 165 (14%) patients.

2.3. Intracerebral hematoma

Middle cerebral artery bifurcation aneurysms bled

frequently into the adjacent brain in as much as 45% of

the 711 ruptured cases. Most ICHs (84%) projected toward

the temporal lobe (Table 5). Intracerebral hematoma is

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 (b7 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 (z25 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.

R. Dashti et al. / Surgical Neurology 67 (2007) 441–456 443

thought to affect the outcome mainly by the initial brain

damage [37,38,47,48,79].

Table 4

Distribution of patients with single and multiple aneurysm in ruptured and

unruptured groups

Ruptured Unruptured Total

Patients with MbifA 711 455 1166

Single aneurysm 495 (70%) 158 (35%) 653 (56%)

Multiple aneurysms 216 (30%) 297 (65%) 513 (44%)

Associated MbifAs 109 95 204

Unilateral 17 10 27

Bilateral 85 80 165

Both 7 5 12

Associated aneurysms

at other sites

107 202 309

Data are based on number of patients.

3. Microsurgical anatomical considerations of MbifAs

Middle cerebral artery aneurysms can be classified into

proximal (M1A), bifurcational (MbifA), and distal types

(MdistA) (Table 1). Proximal MCA aneurysms or M1As are

located in the main trunk (M1), between the bifurcation of

the ICA and the main bifurcation of MCA [6]. Middle

cerebral artery bifurcation aneurysm is the focus of the

present article. Distal MCA aneurysm, originating from the

M2 or more distal branches of MCA, will be the focus of a

separate article.

Middle cerebral artery bifurcation aneurysms are located

in the sylvian fissure, between the frontal and temporal

lobes, where diverse vascular anatomy may affect the

outcome of surgery. The sylvian fissure varies in shape

and volume, and previous SAHs may toughen the arachnoid

in and on the fissure [5,77]. The venous anatomy of the

sylvian fissure is complex and varies highly [26,62,77].

Middle cerebral artery is the major terminal branch of the

ICA supplying a large part of the cerebral hemisphere along

with the insula, lentiform nucleus, and internal capsule [66].

Middle cerebral artery is the most complex major cerebral

artery owing to its anatomical and hemodynamic features.

The detailed microneurosurgical anatomy of MCA has

been described by YaYargil [77,78] and several others

[16,50,62,66,68,69].

3.1. Middle cerebral artery bifurcation

The main trunk (M1) of the MCA starts at the carotid

bifurcation in the sylvian cistern. M1 runs laterally until the

level of limen insula where it splits usually into 2

(bifurcation) branches (M2s), the superior (frontal) and

inferior (temporal) ones [66,77] (Fig. 1). The location of the

bifurcational complex in the sylvian fissure, depending on

the length of M1, as well as the angioarchitecture of the

complex varies considerably [16,66,77,78]. M2s run some-

what parallel to and supply the insula [16]. In the study of

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

the M1 trunk creates ba false bifurcation,Q so named by

YaYargil [77], and is seen in 7.5% of the hemispheres

studied by Tqre et al. [66]. Lateral lenticulostriate arteries

originate mainly from the M1 trunk (see below), and

identification of their origin should help to distinguish the

true MCA bifurcation. In 55% of the hemispheres studied

by Tqre et al, the dominant M2 trunk bifurcated soon after

the main bifurcation (intermediate branch). This gave an

impression of trifurcation in 12.5%, and quadrifurcation was

seen in 2.5% when both M2s bifurcated immediately [66].

Umansky et al [67] reported bifurcation in 66%, trifurcation

in 26%, and quadrifurcation in 4%, and Gibo et al [16]

reported bifurcation in 78%, trifurcation in 12%, and

multiple trunks in 10%.

3.2. Perforating arteries

Lateral lenticulostriate arteries vary much in number

(1-20) and sites of origin [16,31,66,68,69,77]. Lateral

lenticulostriate arteries mainly arise from the frontal aspect

or cortical branches of M1. However, LLAs may also

arise, in up to 23%, from the MCA bifurcation, M2, or an

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%)

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.


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.

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).


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 le

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].


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].

ft intertruncal MbifA (see also video MbifA-1).

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

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

existence of ICH or associated aneurysms. Proper approach

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].

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 towardthe 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.

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.


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

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 MbifAwall. 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

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 (bdoubleclippingQ). 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


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.

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.


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.


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


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.


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.


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.


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).


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 rupturedMbifA 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

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 (b20 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

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


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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