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Surgical Neurology 71 (2009) 649 – 667

www.surgicalneurology-online.com
Technique
Microneurosurgical management of internal carotid artery
bifurcation aneurysms☆
Martin Lehecka, MD a , Reza Dashti, MD, PhD a , Rossana Romani, MD a , Özgür Çelik, MD a ,
Ondrej Navratil, MD a , Leena Kivipelto, MD, PhD a , Riku Kivisaari, MD, PhD a , Hu Shen, MD a ,
Keisuke Ishii, MD, PhD a , Ayse Karatas, MD a , Hanna Lehto, MD a , Jouji Kokuzawa, MD, PhD a ,
Mika Niemelä, MD, PhD a , Jaakko Rinne, MD, PhD b , Antti Ronkainen, MD, PhD b ,
Timo Koivisto, MD, PhD b , Juha E. Jääskelainen, MD, PhD b , Juha Hernesniemi, MD, PhD a,⁎
a
Department of Neurosurgery, Helsinki University Central Hospital, 00260 Helsinki, Finland
b
Department of Neurosurgery, Kuopio University Hospital, 70211 Kuopio, Finland
Received 25 December 2008; accepted 31 January 2009

This paper by The Rainbow Team from Finland on the practical aspects of clipping of carotid bifurcation aneurysms is a superb piece of work. If the reader
follows every detail, from the anatomical descriptions to the specifics of surgery, for these aneurysms, he/she will be successful. The authors describer the rarely
written technique of Drake of grasping the aneurysm and pulling it into the clip being applied. I learned this idea by watching Professor Drake's videos almost
30 years ago and have used this technique many times. The authors also describe the use of cotton balls to keep the lenticulostriate vessels away from the
aneurysm being clipped. They note the precise location for the temporary clip on the carotid just distal to the anterior choroidal artery and the also rarely
described technique of only using temporary clips for 5 minutes or less — a technique that prevents ischemia with temporary occlusion. The paper is filled with
excellent tips on surgery for the aneurysm surgeon. This, and the accompanying videos, comprise an outstanding publication and are the result of carefully
learned and noted experience.

James I. Ausman, MD, PhD, Editor

Abstract Background: Internal carotid artery bifurcation aneurysms form 2% to 9% of all IAs. They are more
frequent in younger patients than other IAs. In this article, we review the practical microsurgical
anatomy, the preoperative imaging, surgical planning, and the microneurosurgical steps in the
dissection and the clipping of ICAbifAs.
Methods: This review and the whole series on IAs are 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 11 000 patients with IAs since 1951. In the Kuopio
Cerebral Aneurysm Database of 3005 patients with 4253 IAs, 831 (28%) patients had altogether 980
ICA aneurysms, of whom 137 patients had 149 (4%) ICAbifAs. Ruptured ICAbifAs, found in 78
(52%) patients, with median size of 8 mm (range, 2-60 mm), were associated with ICH in 15 (19%)

Abbreviations: 3D, 3-dimensional; A1, proximal segment of anterior cerebral artery; ACA, anterior cerebral artery; AChA, anterior choroid artery; AChAA,
AChA aneurysm; ACoA, anterior communicating artery; CBF, cerebral blood flow; CSF, cerebrospinal fluid; CT, computed tomography; CTA, CT angiography;
DSA, digital subtraction angiography; IA, intracranial aneurysm; ICA, internal carotid artery; ICAbifA, internal carotid artery bifurcation aneurysm; ICAcavA,
aneurysm on the intracavernous portion of the ICA; ICAextra, extracranial ICA; ICAextraA, extracranial ICA aneurysm; ICAintra, intracranial extradural ICA;
ICAintraA, intracranial extradural ICA aneurysms subdivided into ICAcavAs and ICApetrAs; ICAmalignantA, blister-like (malignant) ICA aneurysm on the
ICA trunk; ICAophtA, paraophthalmic (clinioid-ophthalmic) ICA aneurysm; ICApetrA, aneurysm on the Petrosal portion of the ICA; ICAtrunkA, ICA trunk
aneurysm; ICAwallA, aneurysms at the nonbranching sites of the ICA trunk wall; ICG, indocyanine green; ICH, intracerebral hematoma; IVH, intraventricular
hemorrhage; LLA, lateral lenticulostriate artery; LSO, lateral supraorbital approach; M1, proximal segment of middle cerebral artery; MCA, middle cerebral
artery; MLA, medial lenticulostriate artery; MRI, magnetic resonance imaging; OphtA, Ophthalmic artery; PCA, posterior cerebral artery; PCoA, posterior
communicating artery; PCoAA, PCoA aneurysm; RAH, recurrent artery of Heubner; SAH, subarachnoid hemorrhage.
☆
Conflict of interest statement: The authors declare to have no conflict of interest.
⁎ Corresponding author. Tel.: +358 50 427 0220; fax: +358 9 471 87560.
E-mail address: juha.hernesniemi@hus.fi (J. Hernesniemi).

0090-3019/$ – see front matter © 2009 Elsevier Inc. All rights reserved.
doi:10.1016/j.surneu.2009.01.028
650 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667

patients. Ten (7%) ICAbifAs were giant (≥25 mm). Multiple aneurysms were seen in 59 (43%)
patients. The ICAbifAs represented 18% of all IAs ruptured before the age of 30 years.
Conclusions: The main difficulty in microneurosurgical management of ICAbifAs is to preserve
flow in all the perforators surrounding or adherent to the aneurysm dome. This necessitates perfect
surgical strategy based on preoperative knowledge of 3D angioarchitecture and proper orientation
during the microsurgical dissection.
© 2009 Elsevier Inc. All rights reserved.
Keywords: Aneurysm; Bifurcation; Clipping; Internal carotid artery; Microanatomy; Microsurgical technique; Perforators; Subarachnoid hemorrhage

1. Introduction compared to IAs at other locations [1,21,23]. The ICAbifAs

We classify ICA aneurysms into 7 groups based on their
site of origin, wall morphology, and clinical or surgical
behavior: (a) ICAextraAs, (b) ICApetrAs and ICAcavAs, (c)
ICAophtAs, (d) ICAwallAs and ICAmalignantAs, (e) ICA-
PCoAAs, (f) ICA-AChAAs, and (g) ICAbifAs (Table 1).
1.1. Internal carotid artery bifurcation aneurysms
Dott [11] was the first neurosurgeon to treat an ICA
aneurysm by direct surgery, wrapping it with a piece of
muscle in 1933. This was also the first surgical attempt to
treat an IA [67]. Since that time, despite the advances in the
field of microneurosurgery, aneurysms at this location have
remained difficult to treat.
The ICAbifAs are located at the bifurcation of the ICA
where it divides into the A1 segment of the ACA and the
M1 segment of the MCA (Fig. 1). The ICA bifurcation is
usually the highest point of the Circle of Willis. The apex of
the ICA bifurcation, similar to the MCA bifurcation or the
tip of the basilar artery, is under particular hemodynamic
stress and high wall shear stress [45]. This apparently adds
to the risk of saccular IA formation through pathological
remodeling of the arterial wall of the branching site by
impact, deflection, separation of CBF streamlines, and
vortex formation at the lateral angles [45,63]. The ICAbifAs
tend to arise rather at the junction of the ICA and the A1
segment of the ACA than at the junction of the ICA and the
M1 segment of the MCA [46,65].
The ICAbifAs are unusual lesions. Their most striking
feature is the younger age of patients at the time of rupture as
Table 1
Categories of ICA aneurysms
Category Location
ICAextra Extracranial ICA
ICAintra Intracranial extradural ICA
ICApetr Petrous segment ICA
ICAcav Intracavernous segment ICA
ICAopht Paraophthalmic ICA
ICAtrunk Medial, superior and inferior wall of ICA trunk
ICAwall Nonbranching sites of the ICA trunk wall
ICAmalignant Blister-like (malignant) of the ICA trunk
PCoA Origin of PCoA
AChA Origin of Anterior chroidal artery
ICAbif ICA bifurcation
may represent more than 40% of all IAs in patients younger
than 20 years [23,27,28,33,51]. There is no clear explana-
tion, but arterial wall deficits and wider angle of the ICA
bifurcation may be risk factors.
The microneurosurgical exposure and clipping of ICAbi-
fAs is demanding due to (a) high position with respect to the
skull base, (b) attachment of the dome to the surrounding
brain parenchyma, (c) large number of perforators surround-
ing the base and/or the dome, and (d) the relatively high risk
of intraoperative rupture. The orientation of the aneurysm
dome affects the clipping, with the posterior orientation
being the most difficult. Precise dissection in the 3D
anatomy of ICAbifAs and the surrounding perforators
requires not only experience and microsurgical skill but
also patience to work on the aneurysm base under repeated
protection of temporary and pilot clips.
1.2. Purpose of the review
This review, and the whole series on IAs, is intended for
neurosurgeons who are subspecializing in neurovascular
surgery. The purpose is to review the practical anatomy, the
preoperative planning, and the avoidance of complications in
the microsurgical dissection and clipping of ICAbifAs.
1.3. Authors
The microneurosurgical technique in this review is
mainly based on the personal experience of the senior author
(JH) in 2 Finnish centers (Helsinki and Kuopio), which serve
without selection the catchment area in Southern and Eastern
Finland. These 2 centers have treated more than 10 000
patients with IAs since 1951 and more than 9000 patients
during microsurgical era since mid 1970s. The data
presented in our series of articles represent 3005 consecutive
patients harboring 4253 IAs from the Kuopio Cerebral
Aneurysm Database (1977-2005). The aim is to present a
consecutive, nonselected population-based series of IAs.
This database is not reflective of the personal series of the
senior author (JH) alone.
2. Occurrence of ICAbifAs
The ICAbifAs are reported to represent from 2% to 9%
[5,21,35,37,46,67,79] of all IAs. Tables 2-5 present the
clinical data on the 137 patients with ICAbifA in a
 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667 651

2.1. Ruptured and unruptured ICAbifAs

In our series, 498 (51%) of the 980 ICA aneurysms
presented with SAH, of which 78 (16%) were ICAbifAs
(Table 2). Of the 149 ICAbifAs, 78 (52%) were ruptured and
71 (48%) unruptured (Table 3). Their size distribution is
presented in Table 4. Of the 78 ruptured ICAbifAs, 39 (50%)
were smaller than 7 mm, suggesting that even small
unruptured ICAbifAs would require occlusive therapy.
Importantly, the ICAbifAs ruptured at a median age of
44 years (range, 11-81 years) as compared to 51 years for the
whole series. The ICAbifAs represented as much as 27%
(n = 6) of all IAs ruptured before 20 years of age (n = 22) and
18% (n = 25) before 30 years of age.
2.2. Intracerebral hematoma and IVH
Of the 78 patients with ruptured ICAbifAs, ICH was
present in 15 (19%) and IVH in 18 (23%) (Table 3).
Fig. 1. Illustration showing site of origin for ICAbifAs and its relation to Intracerebral hematoma was usually located in the frontal
segments and branches of the supraclinoid ICA.
lobe, and it often extended into the ventricular system
(Table 4).
consecutive and population-based series of 3005 patients 2.3. Associated aneurysms
with 4253 IAs from 1977 to 2005 in the Kuopio Cerebral
Aneurysm Database. Of the 3005 patients, 831 (28%) had In our series, 59 (43%) of the 137 patients with ICAbifA
980 ICA aneurysms (Table 2). There were 137 patients with had at least 1 associated IA (Table 5), most frequently on
149 ICAbifAs, 4% of all the 4253 IAs and 15% of all the the MCA. Bilateral ICAbifAs occurred in 8 (6%) patients
980 ICA aneurysms. The left side (n = 84, 56%) slightly (Table 5).
dominated over the right side (n = 65, 44%). There was
only one fusiform ICAbifA. Giant ICAbifAs occurred in
3. Microsurgical anatomical considerations of ICAbifAs
7% (n = 10) in our series (Table 3).
3.1. Internal carotid artery
Table 2
Patients with ICA aneurysms in a consecutive and population-based series of The microneurosurgical anatomy of the ICA and its
3005 patients with 4253 IAs from 1977 to 2005 in the Kuopio Cerebral
branches has been earlier described by Yaşargil et al [84-86]
Aneurysm Database
and others [17,20,44,57,67] in detail.
No. of patients No. of aneurysms
Whole series 3005 4253
Patients with primary SAH 2365 3325 Table 3
Patients without primary SAH 640 928 Characteristics of 149 ICAbifAs
ICA aneurysms 831 980
Ruptured Unruptured Total
ICAextraAs + ICAintraAs 95 (11%) 106 (11%)
ICAophtAs 85 (10%) 93 (9%) No. of aneurysms 78 71 149
ICAtrunkAs 65 (8%) 69 (7%) Median aneurysm 8 (range, 2–60) 5 (range, 1–40) 7 (range, 1–60)
PCoAAs 436 (52%) 464 (47%) size (mm)
AChAAs 95 (11%) 99 (10%) Aneurysm size, n (%)
ICAbifAs 137 (16%) 149 (15%) Small (b7 mm) 39 (50) 35 (49) 74 (50)
Ruptured ICA aneurysms 498 498 Medium (7-14 mm) 21 (27) 32 (45) 53 (36)
ICAextraAs + ICAintraAs 6 (1%) 6 (1%) Large (15-24 mm) 10 (13) 2 (3) 12 (8)
ICAophtAs 30 (6%) 30 (6%) Giant (≥25 mm) 8 (10) 2 (3) 10 (7)
ICAtrunkAs 39 (8%) 39 (8%) Aneurysm side, n (%)
PCoAAs 306 (61%) 306 (61%) Right 34 (44) 31 (44) 65 (44)
AChAAs 39 (8%) 39 (8%) Left 44 (56) 40 (56) 84 (56)
ICAbifAs 78 (16%) 78 (16%) ICH, n (%) 15 (19) – –
Fusiform ICA aneurysms 34 36 Frontal 11 – –
Fusiform ICAextraAs + ICAintraAs 13 14 Temporal 4 – –
Fusiform ICAophtAs 2 2 Parietal 0 – –
Fusiform ICAtrunkAs 7 8 IVH, n (%) 18 (23) – –
Fusiform PCoAAs 9 9 Preoperative 30 (38) – –
Fusiform AChAAs 2 2 hydrocephalus, n (%)
Fusiform ICAbifAs 1 1
Data are given in number of aneurysms.
652 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667

Table 4
Intracerebral hematoma, IVH, and acute hydrocephalus associated with aneurysm rupture on different ICA segments
ICAextraAs + ICAintraAs ICAophtAs ICAtrunkAs PCoAAs AChAAs ICAbifAs
Ruptured aneurysms 6 30 39 306 39 78
ICH only 0 3 (10) 1 (3) 14 (5) 1 (3) 5 (6)
ICH with IVH component 0 1 (3) 5 (13) 11 (4) 0 10 (13)
IVH only 0 4 (13) 8 (21) 65 (21) 10 (26) 8 (10)
Preoperative hydrocephalus 3 (50) 13 (43) 21 (54) 129 (42) 21 (54) 30 (38)

Fischer divided the ICA into 5 different segments: (a) 3.3. Branches and segments of the supraclinoid ICA
cervical, (b) petrous, (c) cavernous, (d) clinoid, and (e)
The supraclinoid ICA bifurcates into its 2 terminal
supraclinoid [12]. Rhoton et al [59,60] defined 4 segments:
branches: (a) the proximal M1 segment of the MCA and
(a) cervical (C1), (b) petrous (C2), (c) cavernous (C3), and
(b) the proximal A1 segment of the ACA just below the
(d) supraclinoid (C4) [17] (Fig. 2).
anterior perforating substance (Figs. 3 and 4; see video
The cervical ICA portion extends from the common
ICAbifA—1 Hernesniemi). Other main branches arising
carotid artery to the external orifice of the carotid canal. The
from the prebifurcational supraclinoid ICA are (a) the
petrous portion runs in the carotid canal to the apex of the
OphtA, (b) several small superior hypophyseal arteries, (c)
petrous pyramid, medial to the Gasserian ganglion, from
the PCoA, (d) the AChA, (e) the 2 to 3 small branches to the
which point the ICA runs (a) upward, (b) forward, and (c)
uncus, and (f) the artery to the dura of anterior clinoid
medially over the foramen lacerum to reach the poster-
process [85]. Besides these major branches, an average of 8
olateral portion of the cavernous sinus, becoming the
(3-12) small perforating arteries originate from the trunk of
intracavernous portion. After the cavernous sinus, the ICA
supraclinoid ICA [59].
becomes intradural with its clinoid and supraclinoid
The supraclinoid portion of the ICA is divided into 3
segments [85].
segments based on the origin of its major branches (Fig. 1):
3.2. Supraclinoid portion of the ICA (C4) (a) the ophthalmic segment, the longest segment of the C4
portion, extending from the origin of the OphtA to the origin
The supraclinoid ICA enters the intradural space and
of the PCoA; (b) the communicating segment, extending
carotid cistern inferomedially to the anterior clinoid process
from the origin of the PCoA to the origin of the AChA; and
[85]. The relation of anterior clinoid process with the
(c) the choroid segment, extending from the origin of the
proximal part of intradural ICA varies and depends on its size
AChA to ICA bifurcation [59].
and pneumatization of the bone and the length of intradural
ICA. Proximal part of the artery and occasionally its 3.3.1. Ophthalmic artery
proximal branches (ie, OphtA and PCoA) may be covered The OphtA is the single major branch of the ICA that runs
by the anterior clinoid process. The supraclinoid ICA then medially. It usually arises from the medial (78%) or the
travels in an upward and posterolateral direction. Because
the intradural approach toward the ICA is pointed parallel to
the sphenoid ridge and/or orbital roof toward the anterior
clinoid process, it is of utmost importance to disclose the
relation of skull base and the anterior clinoid process to the
vessel in preoperative imaging studies.

Table 5
Patients with an ICAbifA and possible associated aneurysms
Ruptured Unruptured Total
ICAbifA ICAbifA
Patients with ICAbifA 78 59 137
Patients with single aneurysm 58 (74) 20 (34) 78 (57)
Patients with 20 (26) 39 (66) 59 (43)
multiple aneurysms
Associated ICAbifAs 5 3 8
Same ICA 0 0 0
Opposite ICA 5 2 7
Both ICAs 0 1 1
Associated aneurysms at other sites 15 36 51
Fig. 2. Microsurgical division of ICA into C1 to C4 segments and their
Data are given in number of patients. relation to petrous bone, cavernous sinus, and sphenoid sinus (SS).
 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667
Fig. 3. Illustration demonstrating the different perforator groups near the
ICA bifurcation.
middle (22%) one third of the superior surface of the
supraclinoid ICA below the optic nerve and above the dura
of the cavernous sinus. Sometimes, it can arise already from
the cavernous segment (up to 8% ) of the ICA, but it is only
very rarely absent altogether. The OphtA runs anterolaterally
below and attached to the undersurface of the optic nerve to
enter the optic canal. The intradural segment of the OphtA is
usually short, but it is often possible to visualize the origin
and the proximal segment of the OphtA without or with
minor retraction of the optic nerve [17,52,56,59,85].
3.3.2. Superior hypophyseal arteries
The superior hypophyseal arteries are a complex group of
small vessels (average, 2; range, 1-5) with a diameter of 0.1
to 0.5 mm. They arise from the posteromedial, medial, or
posterior aspect of the ophthalmic segment of the ICA in the
midway between the origin of the OphtA and PCoA
Fig. 4. Intraoperative microanatomy view of the ICA bifurcation showing A) the perforators behind the right ICA bifurcation, the LLAs, and the AChA (A); the
origin of LLAs and MLAs on the left side (B); right-sided ICAbifA, RAH passing behind the aneurysm, duplication of AChA, and origin of PCoA (C).
653
Table 6
Supplementary videos on microneurosurgery of IAs published in Surgical
Neurology
Videos on ICAbifAs (present paper)
1. Microanatomy of ICA bifurcation
2. Clipping of unruptured anterior projecting ICAbifA
3. Clipping of unruptured superior projecting ICAbifA
4. Clipping of unruptured large, calcified ICAbifA
5. Clipping of ruptured previously coiled and posterosuperior projecting
ICAbifA
6. Clipping of unruptured previously clipped (recurrent) ICAbifA
7. Clipping of unruptured superior projecting ICAbifA, the contralateral
approach
Previously published videos in this series:
ACoA aneurysms [24]
Proximal ACA aneurysms (A1 segment) [6]
Distal ACA aneurysms (A2 segment and frontobasal branches) [41]
Distal ACA aneurysms (A3 segment) [39]
Distal ACA aneurysms (A4-A5 segments and distal branches) [40]
Proximal MCA aneurysms (M1 segment) [9]
MCA bifurcation aneurysms [8]
Distal MCA aneurysms (M2-M4 segments) [7]
[16,34,38,59,85]. The superior hypophyseal arteries run
medially under the optic chiasm to terminate in the tuber
cinereum, anterior lobe of the pituitary, and inferior surface
of the optic nerve and the chiasm. Because the superior
hypophyseal arteries may provide major blood supply to the
optic nerve and the chiasm, their preservation during
dissection is of vital importance [34].
3.3.3. Posterior communicating artery
The PCoA arises from the posteromedial, posterior, or
rarely from the medial wall of the supraclinoid ICA, 2 to
8 mm after its origin [59]. Rare origin from the OphtA has
also been reported [2]. The PCoA runs backward and
medially, above the sella turcica, slightly above and medial
to the occulomotor nerve, and below the tuber cinereum to
join the PCA in the interpeduncular cistern. Inside the carotid
cistern, an arachnoid sleeve similar and adherent to that of
654 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667
the occulomotor nerve covers the PCoA. The distal part of
the PCoA may be in close relation to the dura of the posterior
clinoid process or even lie inside the groove within the
process [59,81,85]. The PCoA can be absent altogether in up
to 14% of cases [81,85]. Fetal type of PCoA is marked by a
PCoA of large diameter, which courses more laterally, above
or even lateral to the oculomotor nerve to join the posterior
circulation, where the proximal segment of the PCA (P1
segment) is hypoplastic or aplastic [59]. Infundibular
dilatation of the PCoA is another frequent variation (in 6%
of cases) [59] and easily mistaken for aneurysm on
preoperative images.
3.3.4. Anterior choroid artery
The AChA is the first posterolateral branch distal to the
PCoA. In most cases, it arises closer to the origin of
the PCoA (2-5 mm) than to the ICA bifurcation [60,85]. The
AChA is nearly always present [60], but it can sometimes
originate also from other arteries such as the PCoA or the
MCA in up to 23% of cases [4,47,50,60,69]. The diameter of
the AChA ranges from 0.5 to 2.0 mm, and the pattern of
origin of the artery may also be highly variable [60,85]. The
AChA may arise as a single trunk or multiple vessels from
posterolateral wall of ICA. To identify and preserve the
AChA during different steps of dissection toward ICAbifAs
or temporary clipping one should be aware of these possible
anatomic variations and the course of the AChA [88]. After
its origin in carotid cistern, the AChA enters the crural
cistern with a posteromedial direction and is often found
behind the ICA bifurcation. The artery courses lateral and
inferior to the optic tract, passes through the wing of ambient
cistern, to enter the choroidal fissure [60,85].
3.3.5. Uncal arteries
The uncal arteries usually originate distal to the AChA or
from the very proximal part of the MCA [85].
3.3.6. Artery to the dura of the anterior clinoid process
The dural branch of the ICA is a small branch usually
originating from the anterior wall of the ICA 3 to 5 mm
proximal to its bifurcation or rarely from the proximal A1
segment. It passes toward the dura of the anterior clinoid
process. Avulsion of this artery due to retraction may cause
bleeding from the wall of the parent artery [85].
3.3.7. Perforating branches of the supraclinoid ICA
Each segment of the supraclinoid ICA gives off a series of
perforating branches with a relatively constant site of
termination. During various steps of dissection and tempor-
ary clipping for ICAbifAs, a comprehensive knowledge of
the possible sites of origin and trajectories of these small
vessels is of paramount importance. The perforating
branches arising from the ophthalmic segment (average, 4;
range, 1-7) arise from the posterior or medial wall of the ICA
and pass medially to (a) the optic nerve and the chiasm, (b)
the infundibulum, and (c) the floor of the third ventricle [59].
The perforating branches arising from the communicating
segment are rare. Infrequently, up to 3 small perforators arise
from the posterior side of the ICA wall and pass to (a) the
optic tract, (b) the premamillary part of the floor of the third
ventricle, (c) the optic chiasm, and (d) the infundibulum.
They rarely enter the anterior or posterior perforating
substances [59]. The perforating branches of the choroidal
segment (average, 4; range, 1-9) arise from the posterior half
of the ICA wall, pass upward and terminate in (a) the anterior
perforating substance, (b) the optic tract, and (c) the uncus.
Some of these perforators may also arise from the ICA
bifurcation [44,60,62].
3.3.8. Perforating branches around the ICA bifurcation
There are a large number of perforating branches with
their course behind the ICA bifurcation. These perforators
arise from (a) the choroidal segment of the ICA, (b) the
AChA, (c) the RAH, (d) the MLAs, and (e) the LLAs (Fig. 3)
[6,9,17,43,44,62,75,85]. These vessels may be stretched to
varying degrees by the ICAbifAs or have their origins
involved in the base of the aneurysm. Extreme care should be
taken not to severe them during various stages of dissection
and clipping. They should be identified and if possible
protected during dissection or clipping by, for example, a
small cottonoid.
3.3.9. Anatomical variants of ICA, M1, and A1
Several variants of the supraclinoid ICA are known which
may affect intraoperative orientation during dissection of
ICAbifAs: (a) hypoplastic ICA, (b) absent ICA, (c) ICA
trifurcation, (d) or persistence of fetal remnants [10,29,71]. A
hypoplastic ICA diminishes in caliber at or shortly distal to its
origin. In these cases, the petrous and sellar segments are
frequently also absent [71]. The exact incidence of
hypoplasia or aplasia of the ICA is not known but seems to
be less than 0.01% [3,71] and is rare. Its cause is unknown,
and only about 100 cases have been described in the literature
[10,18]. Three major patterns of collateral circulation have
been described for hypoplasia/absence of the ICA (for details
see de Medonca et al [10]). The ICA trifurcation is rare and
results from the anomalies of the terminal part of the ICA
itself, from accessory origins of the AChA, and from the
absent M1 [29]. Fetal remnants of anastomosis between the
carotid arteries and the vertebral system can persist [10].
Several vascular anomalies of both the M1 and A1
segments can occur. They have been previously described in
our papers on microneurosurgical management of proximal
MCA aneurysms and proximal ACA aneurysms [6,9].
3.4. Cisternal anatomy of supraclinoid ICA
An extensive review on the cisternal anatomy was
previously published by Yaşargil et al [85,87]. Based on
the height of the ICA bifurcation and the size and projection
of the ICAbifA, a different combination of several cisterns,
(a) the carotid cistern, (b) the olfactory cistern, (c) the lamina
terminalis cistern, and (d) the sylvian cistern, may surround
the aneurysm. Strict attention to these cisternal boundaries is
mandatory for orientation to proper dissection planes [84].
 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667
During the dissection toward the ICAbifAs, to release
CSF, opening of the carotid cistern is usually one of the first
intradural steps. The carotid cistern is limited superiorly by
the dura of the anterior clinoid process and the orbitofrontal
lobe; it shares the medial wall with the chiasmatic cistern;
the tentorial edge and mesial temporal lobe limit it laterally;
the inferior limit is the cavernous sinus; and posteriorly, it is
limited by the crural cistern. The carotid cistern also shares
“the Liliequist membrane,” a single membrane of arachnoid
with varying thickness, in common with the interpedun-
cular cistern located at its inferior border. The supraclinoid
ICA, origins of its branches, and the fronto-orbital veins
draining into the sphenoparietal sinus are all within the
carotid cistern. The supraclinoid ICA travels entirely inside
the carotid cistern in a superior-anterior direction with a
variable degree of lateral bend toward the ICA bifurcation.
The relation of the ICA and the optic nerve can vary from a
parallel course of the artery and the nerve to a concave or
convex curve of the artery compared to the nerve [85].
Thick trabeculated arachnoid bands within the carotid
cistern are attached to the origin of the PCoA, the AChA,
and the oculomotor nerve. A careful dissection of these
arachnoid attachments is mandatory for mobilization of
the supraclinoid ICA [85]. Occasionally, the origin of the
PCoA may be heavily involved with the dura overlying
the posterior clinoid process making the dissection even
more demanding.
The chiasmatic cistern or optic cistern contains the optic
nerves, pituitary stalk, branches from the supraclinoid ICA to
these structures, and the OphtA. The lamina terminalis
cistern located in front of the lamina terminalis is limited by
the rostrum of the corpus callosum superiorly and the optic
chiasm inferiorly. The A1 arises from the ICA in the carotid
cistern and with a medial and somewhat anterior course
enters the lamina terminalis cistern. A group of thick
arachnoid bands extending from the olfactory triangle to the
lateral side of optic nerve encase the A1 segment at this point
[62,85]. This is important to note when dissecting and
mobilizing the ICA bifurcation complex. The lamina
Fig. 5. Illustration of the 3 subcategories of ICAbifAs: the anterior or forward projecting ICAbifA, the superior or upward projecting ICAbifA, and the posterior
or backward projecting ICAbifA.
655
terminalis cistern contains the A1 segment, the MLAs, the
RAH, ACoA complex, the origins of A2 segments of the
ACA, the orbitofrontal and rarely the frontopolar arteries,
and the anterior cerebral veins [85].
The M1 segment of the MCA begins at the carotid
bifurcation, lateral to the optic chiasm, and enters the sylvian
cistern. In a similar way to the A1 segment, there are thick
arachnoid bands covering the very proximal part of the M1 at
this point. The M1 then runs laterally and posteriorly until
the level of the limen insula [6,8,9,75-77].
3.5. Venous structures
The superficial and deep venous structures of the ICA
bifurcation region are complex and vary a lot [58,85].
Superficial middle and anterior cerebral veins run over or
under the ICA bifurcation to reach the sphenoparietal or
cavernous sinus [58,85]. The deep venous system, including
the anterior and deep middle cerebral veins and the basal
vein of Rosenthal, may be found near the inferior aspect of
the ICA bifurcation [58,85]. Particular care is necessary
during dissection and mobilization of the (a) ICA trunk, (b)
M1 trunk and (c) A1 trunk, and (d) their perforators so as not
to sever the veins.
3.6. Classification of ICAbifAs according to the
dome projection
We find it essential to classify the ICAbifAs according to
the dome projection because it is important for the
microsurgical approach and strategy. Like others
[21,35,86], we classify the ICAbifAs into (a) anteriorly, (b)
superiorly, and (c) posteriorly projecting (Fig. 5). The
anteriorly projecting ICAbifAs originate from the anterior
aspect of the ICA bifurcation with their dome projecting into
the lateral fronto-orbital gyrus or the base of the olfactory
tract. The superiorly projecting ICAbifAs originate from the
superior aspect of the ICA bifurcation with their dome
projecting into the anterior perforated substance, the lateral
portion of the lamina terminalis cistern, or the sylvian
656 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667
cistern. The posteriorly projecting ICAbifAs originate from
the posterior aspect of the ICA bifurcation with their dome
projecting into the carotid and interpeduncular or even the
ambient and crural cisterns.
4. Imaging of ICAbifAs
Digital subtraction angiography is still the present “gold
standard” in many centers. Multislice helical CTA is the
primary modality for imaging of IAs in our centers for
several reasons: (a) the virtual independence from the
hemodynamic situation; (b) the noninvasive and quick
imaging technique; (c) the comparable sensitivity and
specificity to DSA in aneurysms larger than 2 mm
[19,30,31,68,73,80,82,83]; (d) the disclosure of calcifica-
tions in the walls of arteries and the aneurysm [13,66]; and
(e) the quick reconstruction of 3D images that, for example,
show the surgeon's view of the ICA bifurcation. Some
ICAbifAs may be difficult to visualize by routine 3D CTA
[30,66], usually due to very small size, so that subsequent
rotational 3D DSA is required. Occasionally, ICAbifAs may
be difficult to visualize by routine DSA or CTA, mostly
small ones or those projecting backward, so that subsequent
oblique projections or rotational images are need.
For intraoperative navigation, 3D CTA and/or DSA
reconstructions should be rotated to illustrate (a) the
angioarchitecture of the ICA bifurcation and its relation to
the skull base, (b) projection of the ICAbifA dome and its
relationship to the A1 and M1 segments, and (c) the site of
possible rupture. Other lesions of the ICA should be
differentiated and vascular aberrations should be looked
for, and their possible impact on flow conditions at the ICA
bifurcation should be assessed. In giant and fusiform
ICAbifAs, MRI with different sequences, along with 3D
CTA, helps to distinguish the true wall of the aneurysm and
the intraluminal thrombosis.
In the workstation, 3D CTA images can be rotated
accordingly to evaluate the surgeon's view to the ICA
bifurcation, which is not standard but is tailored according to
the dome's projection and relation to the M1 and A1
segments. The prime concern is to find a view that best helps
to preserve the perforators around the base and the dome of
the aneurysm.
4.1. The CTA anatomy of the ICA bifurcations in
200 patients
The regions of both ICA bifurcations were studied in 200
patients who underwent CTA for IAs from September 2007
to June 2008 at Helsinki University Hospital.
Below the ICA bifurcation, the mean diameter of the right
ICA was 3.6 mm (range, 2.0-6.1 mm) and that of the left ICA
3.7 mm (range, 2.0-5.8 mm). Perforators were seen in 94%
in the right ICA bifurcation region (median, 3; range, 1-7)
and in 97% in the left ICA bifurcation region (median, 3;
range, 1-5).
In the coronal section, the right supraclinoid ICA (C4) had
straight course in 107 (54%) patients and the left one in 118
(59%) patients. Lateral or medial curvature was seen in 91
(46%) patients on the right and in 81 (41%) patients on the
left. The mean lateral deviation of the supraclinoid ICA from
the vertical axis in the coronal plane was 46° (range, 0°-87°)
on the right and 38° (range, 4°-87°) on the left. Both the
course and lateral deviation of the ICA is important to asses
from the preoperative images to allow for optimal head
positioning and visualization of the ICAbifA.
5. Microneurosurgical strategy with ICAbifAs
The ICAbifAs are challenging to approach because they
are located at the highest point of the ICA, overlaid by the
frontal lobe and surrounded by perforators. The surgical
trajectory should provide optimal visualization of the whole
ICA bifurcation and the ICAbifA with the least possible brain
retraction. The aim of the microneurosurgical clipping is the
total occlusion of the aneurysms sac with preservation of flow
in the main branches and the perforating arteries surrounding
the aneurysm dome. The perforators in the ICA bifurcation
region (RAH, MLAs, LLAs, AChA, PCoA) may be adherent
to the dome and may be severed during (a) retraction, (b)
dissection, (c) coagulation, (d) kinking, (e) compression for
hemostasis, (f) temporary occlusion, or (g) final clipping. It is
important to familiarize oneself with the 3D angioarchitecture
of the ICA bifurcation complex in each case and to orientate
accordingly during the microneurosurgical dissection to
spare the vessels. The projection of the aneurysm dome has
to be considered during the head positioning to provide a
clear view to the dome and to optimize the view to dissect the
perforators, many of which are hidden behind the dome. The
CTA is helpful in evaluating the bony relations, trajectory of
the ICA, and the height of the ICA bifurcation. High position
of the ICA tip will require a careful and clean dissection in the
narrow angle of the very proximal part of the sylvian fissure.
In addition, the basal vein of Rosenthal with its tributaries and
the medial sylvian vein must be secured to avoid unpredict-
able postoperative complications.
5.1. Neuroanesthesiological principles
A general review of our neuroanesthosiological principles
has been published previously [55].
5.2. Intracerebral hematoma
In the Kuopio series, ruptured ICAbifAs were associated
with ICH in 19%. Occasionally, there was only the ICH with
no additional blood in the subarachnoid space. The ICH is
usually located in the frontal lobe, in 73% in the Kuopio
series. In our practice, patients with massive ICH are
transferred directly to operating room after acute CTA for
immediate removal of the ICH and aneurysm clipping. The
relative close proximity of ICAbifAs to the ventricular
system predisposes to IVH (Table 4), which is an
 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667
independent risk factor for poor outcome in aneurysmal
SAH [61].
5.3. Acute hydrocephalus
In case of acute hydrocephalus, 38% in the Kuopio series
(Table 3), we have 3 primary treatment options: (a) opening
the lamina terminalis for CSF removal before clipping; (b)
placing ventricular drainage, often through the lamina
terminalis, in most cases after securing the ruptured
aneurysm; and (c) in severe cases, we may insert external
ventricular drainage before or in the beginning of the
craniotomy. These procedures also allow removal of blood
from the ventricular system.
5.4. Approach and craniotomy
Exposure of the ICAbifA surgery depends on several
factors: (a) deviation of the ICAbifA base with respect to the
A1 and M1 segments, (b) presence of ICH and/or IVH, (c) the
length of the supraclinoid ICA and the height of ICA tip from
the skull base, (d) lateral or medial deviation of the ICA
bifurcation with respect to the optic nerve and the
occulomotor nerve, (e) size and orientation of the ICAbifA
dome, (f) presence and extent of atherosclerotic plaques in the
parent artery and the aneurysm base, (g) presence of
associated aneurysms, (h) preexisting neurological deficits,
and (i) possible earlier operations. The proper surgical
approach requires a mental spatial view of the angioarchi-
tecture of the ICA bifurcation and its relation to the
surrounding structures. This affects the head position, the
extent of craniotomy, selecting the proper place for arachnoid
opening, and the intrasylvian orientation. In addition, the
approach also depends on the personal experience.
Generally, ICAbifAs are approached from the ipsilateral
side, especially if ruptured and associated with ICH. The
presence of other aneurysms may influence the surgical
approach if clipping of all available aneurysms is attempted
through the same exposure. Unruptured ICAbifAs with the
dome projecting anteriorly or superiorly dome can be also
approached from the contralateral side over the midline,
provided that the ICA tip is not too high and there are no large
venous structures obstructing the view (see video ICAbifA—
7 Hernesniemi). In all the posteriorly projecting ICAbifAs
and large superiorly projecting ICAbifAs, proper visualiza-
tion of the perforators attached to the posterior wall of the
aneurysm would be very difficult from the contralateral side
and would lead to injury. The contralateral approach requires
more retraction/lifting of the frontal lobe, and we do not
recommend it in acute SAH and brain swelling. Reoperation
of a recently clipped ICAbifA can be performed from the
same side as arachnoid scarring has not yet developed, but
later, the contralateral approach should be considered.
The standard pterional approach, introduced by Yaşargil
et al [84,86], has been widely used for ICAbifAs by many
authors [5,14,22,37]. In our practice, the LSO as a more
direct and simple approach for the ICAbifAs is preferred to
657
the classical pterional approach by the senior author (JH).
The LSO craniotomy is a more subfrontal and less invasive
modification of the pterional approach for the anterior
circulation aneurysms [25]. The LSO craniotomy, described
in detail elsewhere [25], is demonstrated on video in our
article on the aneurysms on the M1 segment of the MCA in
Surgical Neurology [9] (Table 6). This approach illustrates
the philosophy of applying minimally invasive techniques to
enhance a surgical exposure while minimizing the need for
brain retraction. Because the angle of approach toward the
ICAbifA is little less lateral than that provided by the
pterional approach, patency of all the perforators hidden by
the aneurysm dome needs to be checked even more
meticulously once the final clip is in place. Proper choice
of the length of the final clip plays an important role here.
Briefly, the head fixed to the head frame is (a) elevated
clearly above the cardiac level, (b) rotated toward the
opposite side according to the projection of the ICAbifA
dome, (c) tilted somewhat laterally to visualize the ICA
bifurcation complex, and (d) extended. The goal is to have the
very proximal part of the Sylvian fissure almost vertical.
Because ICAbifAs are located higher than other ICA
aneurysms, the head has to be extended more than for other
locations. It is our practice to adjust the position of the fixed
head and body during the operation as needed [26]. 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 the head during microsurgery. If this feature
is not available, the table can be rotated as needed [26].
After minimal shaving, an oblique frontotemporal skin
incision is made behind the hairline (see also the video M1A-
1 in Dashti et al [9]). The incision stops 2 to 3 cm above the
zygoma, and the temporal muscle is split vertically by a short
incision. 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, the projection of the
ICAbifA, and the presence of ICH. Usually, a small LSO
craniotomy is all that is necessary. 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 backward
projecting ICAbifA, the lateral sphenoid ridge is drilled to
create a more lateral view to the ICA bifurcation complex.
The dura is incised curvilinearly with the base sphenoid-
ally. 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, even after removal
of CSF from the basal cisterns, a small cortical incision is
made accordingly, avoiding the Broca area, and some
hematoma is evacuated to gain space. This may risk the
658 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667
rerupture of the ICAbifA, which would be difficult to control
through the ICH cavity. In removing ICH clot, before or after
clipping, minor force should be applied not to sever the
perforating arteries. Intracerebral hematoma in the immedi-
ate vicinity of the aneurysm should be left in place until the
proximal and distal control has been obtained. Finally, more
ICH can be removed at the end of operation.
5.6. Cerebrospinal fluid drainage
In most unruptured ICAbifAs, the carotid cistern and the
chiasmatic cistern are opened to gradually release CSF. In
ruptured ICAbifAs, we begin the subfrontal dissection from
the suprasellar cistern toward the chiasm and open the
lamina terminalis for additional CSF removal. The only
exception is very few cases in which the aneurysm does not
allow approach toward lamina terminalis. For the anteriorly
projecting ICAbifAs (see below), retraction of the frontal
lobe may risk rupture of the aneurysm. In these cases, we
advise not to retract the frontal lobe and not to open the
lamina terminalis until proximal control of the ICA has
been established. Intraoperative ventricular puncture is
rarely adopted.
5.7. Dissection toward ICAbifA
The first and most important precaution when approach-
ing the ICAbifAs is to prepare a site for proximal control of
the ICA, usually just above the origin of the AChA. All the
initial steps of the dissection are oriented toward this goal.
Dissection of carotid and optic cisterns at the very early steps
of surgery is continued with the identification of proper place
for the temporary clips on the proximal ICA. The shape and
size of anterior clinoid process and its relation with the ICA
should once more be evaluated under magnification of the
operating microscope. A small branch of intracranial ICA is
usually arising from the superomedial aspect of the artery
and penetrating the dura covering the anterior clinoid
process. This artery should be identified and either preserved
or coagulated because it may be torn at its origin producing a
hole in the parent artery, a situation usually difficult to
manage. In addition to the proximal control, it is advisable to
have distal control of both the M1 and A1 segments as well.
Especially with large ICAbifAs, it may initially prove
difficult to expose the A1 without risking rupture of the
aneurysm, and it may be necessary to wait for later stages of
the surgery before the A1 can be adequately uncovered.
The next step is dissection of the proximal one third of the
sylvian fissure. For most ICAbifAs, only the very proximal
part of the sylvian fissure, some 1 to 2 cm, needs to be
opened. In large or giant ICAbifAs, a more extensive
opening of the sylvian fissure may be required. The exact
point of entry into the sylvian fissure is not critical, and the
most advantageous spot is usually where transparent
arachnoid is present. The venous anatomy on the surface
of the sylvian fissure is highly variable. Multiple large veins
often follow the course of the sylvian fissure, draining into
the sphenoparietal or cavernous sinuses. These veins are
generally running on the temporal side of the sylvian fissure.
Principally, we prefer to dissect the arachnoid covering of the
sylvian fissure on the frontal side. In the presence of multiple
large veins or anatomic variations, however, dissection plan
should be tailored. Dissection of the sylvian fissure is more
difficult in acute SAH with swollen brain or due to adhesions
from previous SAH or microsurgery. Preservation of the
dissection plane is mandatory.
We usually open a small window in the arachnoid with a
pair of jeweler forceps or a sharp needle acting as arachnoid
knife and then expand the sylvian fissure by injecting water
using a handheld syringe, that is, the water dissection
technique of Toth [48]. The idea is to get relatively deep into
the sylvian fissure to enter the cistern of sylvian fissure from
this small arachnoid opening. Once inside the sylvian cistern,
the dissection proceeds proximally by gently spreading the
fissure in an inside-out manner. In our experience, this
technique has proven to allow easier identification of the
proper dissection plane. Cottonoids are often soft means of
dissection and retraction during this stage. Pressure on both
walls of the fissure will stretch the overlying bridging tissues,
facilitating their sharp dissection. All arachnoid attachments
and strands are cut sharply by microscissors, which can be
also used as a dissector when the tips are closed. To preserve
larger veins, some small bridging veins may be coagulated
and dissected if needed. It is very important not to retract the
frontal lobe because the dome of the aneurysm is usually
buried in subfrontal cortex. Bipolar forceps and suction act
both as dissection instruments and also as delicate micro-
retractors [26].
Once the proximal part of the MCA (M1 segment) is
identified, the dissection should continue along its lateral
surface to identify the anterolateral wall of the ICA. At this
point, the arachnoid of the sylvian cistern is converging the
carotid, olfactory, lamina terminalis, and optic cisterns,
which may all be in contact with the aneurysm to various
degrees. We do not start to dissect the aneurysm base at this
point yet. Instead, we proceed with further dissection of the
carotid cistern and the optic cistern and identify the lateral
branches of the ICA, that is, AChA and PCoA, and we
enhance mobilization of the frontal lobe and remove tension
on the sylvian veins.
When approaching the superiorly or posteriorly oriented
ICAbifAs, our technique is to first identify the proximal M1
segment inside the sylvian fissure and then move along the
M1 toward the ICA bifurcation. From there, the dissection is
oriented along the ICA to prepare site for proximal control.
Finally, we dissect deeper and visualize the A1 segment
more medially. For the anteriorly oriented ICAbifAs, the
dissection starts with opening of the very proximal part of the
sylvian fissure to identify the ICA bifurcation directly. The
dissection then continues proximally along the ICA to
prepare a site for the proximal control, and then the M1
segment is exposed to gain distal control. The A1 remains
often hidden behind the aneurysm dome at this stage. During
 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667
the exposure of the ICA, the M1, and A1, the goal is also to
locate and identify all the branches and perforators in the area
so that their location and course is clear before applying
temporary clips or final clips.
At this stage of dissection, a proper place for temporary
clip application should be prepared. We prefer to apply the
temporary clip distal to the origin of the AChA in a
perforator free zone. Presence of associated aneurysm on the
ipsilateral ICA, severe atherosclerosis, and calcifications or
large size of the ICAbifA necessitate more proximal location.
With the sites for proximal control of the ICA and distal
control of M1 secured, dissection and preparation of the
ipsilateral A1 segment for temporary clipping are the next
advisable step. This may facilitate control of contralateral
flow to the aneurysm. Our practice is to direct the dissection
medially toward the olfactory and lamina terminalis cistern
to identify the A1 segment, its perforators, and RAH. This is
usually applicable for posteriorly or superiorly projecting
ICAbifAs. However, in case of anterior projecting ICAbifAs
or large and giant aneurysms, the risk of premature rupture of
the aneurysm is a real challenge.
During the exposure of the ICA, the M1, and the A1, the
goal is to locate the point of origin and trajectory of all the
perforators, which may be adherent to the posterior wall of
the aneurysm and to preserve them during various stages of
dissection, temporary, or final clipping. Furthermore, the
course of the PCoA and the AChA must be determined and
the relationship of their branches to the aneurysm dome
noted. The temporopolar and the anterior temporal arteries
should be mobilized over few millimeters so that they will
not be torn by retraction. The dissection then always
continues to visualize the ICA perforators. In case of small
ICAbifA, these perforators will usually be free, but they may
be involved with large or giant ones; usually, perforators are
better seen after temporary and/or pilot clipping. In addition
to the MLAs originating from the A1, also the RAH has to be
visualized. The dome of the ICAbifA is often adherent to or
buried in the orbitobasal frontal lobe, so retraction of the
frontal lobe should be minimal during the dissection. In case
of acute SAH or when the ICAbifA is embedded in the
frontal lobe, a small resection at the frontobasal cortex may
be necessary.
Use of mechanical retractors should be avoided until
dissection is completed and aneurysm base is exposed. At
this stage, retractors may help clipping by retaining space.
6. Dissection and clipping of the ICAbifA
6.1. General principles
The close proximity of several perforator groups makes
the dissection of the ICAbifA tedious in the narrow working
channel in the proximal part of the sylvian fissure [9] (Figs. 4
and 6). The aneurysm base with the adjacent arterial
branches should be visualized before clipping. If the
ICAbifA is obstructing the view toward the perforators
659
hidden behind the dome, it may be necessary to first place a
pilot clip at the aneurysm base and with that in place to
continue dissection of the perforators. A small cottonoid can
be used to protect and mobilize perforators during the final
dissection. Good proximal and distal control together with
checking of the patency of the surrounding perforating
branches is key to the successful clipping of the ICAbifA.
6.2. Dissection under temporary clipping of arteries
Nowadays we use temporary clipping nearly always both
during the dissection and clipping of the ICAbifA. Their use
reduces intraluminal pressure and facilitates sharp dissection
of both the aneurysm and the adjacent arteries. Dissection and
preparation of the sites for the temporary clip(s) in the
perforator free zones of the ICA, M1, and A1 should be
performed with sharp dissection with fine-tipped bipolar
forceps or with microdissector. Blunt tip forceps can simulate
placement of temporary or pilot clip. One temporary clip,
usually a small one, curved or straight, is applied proximal to
the aneurysm on the ICA. We prefer the location just
proximal to the ICA bifurcation, distal to the AChA. Care is
needed not to include perforators or the AChA inside the
temporary clip. Using as short temporary clips as possible,
only enough to occlude the whole ICA, can often prevent this.
The second small straight temporary clip is applied on the M1
trunk avoiding the LLAs. The third clip is placed on the A1
where extreme care is needed not to involve the RAH or the
perforators. If the A1 trunk cannot be reached safely due to,
for example, large aneurysm sac, dissection has to proceed
with temporary clips placed on the ICA and the M1 only. A
small cottonoid can be placed over the temporary clip to
gently press it aside and to protect it from dissecting
instruments. To prevent ischemic brain injury, temporary
occlusion should be as short as possible, each period less than
5 minutes.
Under temporary clipping, the dissection of the ICAbifA
can proceed safely. Arachnoid adhesions can be further
separated by microscissors. The dissection continues around
the aneurysm base to prepare site for the pilot clip. All the
perforators should be freed from the base, most of them will
be on the posterior aspect of the aneurysm. Occasionally, the
aneurysm dome is partially or fully buried in the fronto-
orbital lobe. The pia mater will then be opened around the
aneurysm dome, and a few millimeters of subpial tissue is
resected. Freeing the aneurysm from the fronto-orbital area
will release tension on the aneurysm dome caused either by
retraction of the frontal lobe of dissection or clipping of the
aneurysm neck. If significant venous bleeding occurs during
the dissection of the inferior-posterior aspect of the
aneurysm, injury to the basal vein of Rosenthal should be
suspected. When the main part of the aneurysm base is freed,
a short, straight pilot clip is applied along the direction of the
M1 trunk to prevent perforators accidentally slipping into the
clip. Temporary clips should be removed in distal to
proximal order. When removing temporary clips, they are
first opened in place to test for unwanted bleeding. Hasty
660 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667

Fig. 6. Superior projecting unruptured ICAbifA (arrow) as seen on preoperative DSA in A-P view (A); preoperative DSA in sagittal view (B); postoperative DSA
in anterior-posterior (A-P) view (C); postoperative DSA in sagittal view (D); and intraoperative drawing of the clipping (E). Notice the exact length of the clip on
postoperative DSA.

removal can be followed by heavy bleeding and great
difficulties in placing the clip back. While removing the
temporary clips, even the slightest resistance should be noted
as possible involvement of a small attached branch in the clip
or its applier.
6.3. Clipping of the ICAbifA base
A proper selection of clips with different shapes and
lengths of blades, and applicators, suiting the imaged
ICAbifA anatomy, should be ready for use. A limited
selection of final clips is needed when temporary clipping of
the arteries and bipolar shaping of the aneurysm dome is
used. To prevent kinking or occlusion of adjacent branches,
the smallest but adequate final clip should be selected. If
bipolar reshaping is not considered, then the blade of a single
occluding clip should be one and a half times the width of the
base as suggested by Drake. Frequent short-term application
of temporary clips during the placement and replacement of
aneurysm clips is routine in our practice. We prefer inserting
first a pilot clip to the ICAbifA dome, preferring Sugita clips
for their wide opening and blunt tips. In large or complex
ICAbifAs, stepwise clipping of the aneurysm dome toward
 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667
the base with further dissection facilitates complete occlu-
sion. The pilot clip is later exchanged for a smaller and
lighter final clip after reshaping of the dome by bipolar
coagulation to make the neck smaller.
The clip is generally best introduced across the neck of
the aneurysm along M1 trunk, slowly wiggling the blades
between the neck of the aneurysm and the ACA and the
MCA as well as their branches to avoid crimping of the
parent artery or “dog earing” of the aneurysm. As the clip is
slowly closed, the surrounding arteries and perforators are
inspected for kinking, twisting, and compromised flow. With
the final clip in place, the whole aneurysm dome should be
freed and checked that no perforators or other arteries (RAH,
MLAs, LLAs, AChA) are attached to its wall and involved
inside the final clip. After the clipping, the aneurysm dome is
punctured and the collapsed sac can be mobilized,
coagulated, transected, and removed. The clip blades should
completely close the neck of the aneurysm. To ensure
complete occlusion, under temporary clipping, the final clip
is opened and the escaping remnants of the aneurysm sac are
pulled inside the final clip with suction or ring forceps to
ensure complete occlusion. Adequate dissection, proper
sizes of clips, and careful checking that the clip blades are
well placed up to their tips are required to preserve the
adjacent branches. If the first clip slides, exposing some of
the neck, another clip may be applied proximal to the first
one for final closure (“double clipping”). Multiple clipping
using 2 or more clips is occasionally required for wide-based
aneurysms. Previously coiled ICAbifAs (see video ICAbifA
—6 Hernesniemi) pose additional difficulties for adequate
clip placement because there may not be enough free base for
safe application of the clip. In such a situation, one should
consider removing some or all of the coils under temporary
clipping to provide extra room for the clip at the base [72].
Removal of the retractors and cottonoids may cause kinking
of the parent artery or compression of the perforators by the
clip. The flow in the branches should be checked once more
and papaverin applied.
6.4. ICAbifA rupture before clipping
The ICAbifA may rupture during any step of the
approach or the dissection. The 2 most common causes of
intraoperative rupture are lifting of the frontal lobe and
dislocation of the ICA while the aneurysm dome is still
adherent to the frontal lobe. The risk is highest for the
anteriorly projecting ICAbifAs. In case of rupture, control
should be first attempted via suction and compression of the
bleeding site with cottonoids. Short and sudden hypotension
by cardiac arrest, induced by intravenous adenosine [55],
can be used to facilitate quick dissection and application of a
pilot clip in case of uncontrolled bleeding. If the rupture
takes place before completing the dissection, there is no
point in trying to clip the aneurysm because this might
produce severe lesion in the bifurcation or the aneurysm.
Temporary clips must be applied to the parent vessels
proximally and distally, and the aneurysm is prepared for
661
pilot clipping under local flow arrest. A small and thin-
walled ICAbifA may rupture at its neck during dissection. In
such a case, under temporary clipping, reconstruction of the
base by including a small part of the parent artery inside the
clip should be attempted.
6.5. Very small ICAbifAs
Very small (2-3 mm) ICAbifAs may be difficult to
identify preoperatively and intraoperatively due to super-
imposition of the ICA and its branches. In very small
ICAbifAs, clipping is difficult because their wall is thin and
fragile. Without temporary clipping, the final clip would
easily tear the whole aneurysm off and leave a hole in the
ICA, which would be very difficult to control. Temporary
clipping reduces intraluminal pressure and softens the dome
so that a straight or gently curved microclip can be placed
over the aneurysm without compromising the perforators.
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 exposing some of
the neck, double clipping may be applied (see above).
6.6. Intraoperative verification of clipping
We routinely use microvascular Doppler to check the flow
in the proximal and distal arteries and branches after
clipping, but unexpected occlusions are still sometimes
seen in the postoperative angiography [32]. Nowadays, we
routinely use noninvasive ICG infrared angiography [53,54].
The ICG angiography reduces the need of intraoperative
catheter angiography for clipping control. It allows intrao-
perative confirmation of the patency of the main arterial
branches and of the perforators deep inside the surgical field
[70]. In giant and complex ICAbifAs, catheter angiography
under the digital C-frame guidance with memory is needed
for intraoperative assessment of the flow.
6.7. Resection of the ICAbifA dome
The dome can be resected for the final check of closure
and for research purposes [15,36,74]. In some large and giant
aneurysms, clipping is not possible without opening the
aneurysm and emptying the aneurysm sac, which makes it
possible to adapt the resected walls together with final clips.
This policy teaches one to dissect the aneurysm domes more
completely, thereby avoiding unexpected closure of the
perforators (see above). It also allows inspection of the
posterior surface of the aneurysm to ensure that the final clip
has not caught any of the perforators.
7. Considerations for individual ICAbifA
dome projections
7.1. Anteriorly projecting ICAbifA
7.1.1. Planning
The anteriorly or “forward” projecting ICAbifAs
originate from the anterior aspect of the ICA bifurcation
662 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667

Fig. 7. Anterior projecting unruptured ICAbifA as seen on preoperative axial CTA (A); preoperative 3D CTA reconstruction (B); postoperative coronal CTA (C);
and postoperative sagittal CTA (D).

(Fig. 7A-D, see video ICAbifA—2 Hernesniemi). They are
generally easier to visualize during dissection, and they are
less involved with perforators than other ICAbifAs. The
anteriorly projecting ICAbifAs are often embedded in the
fronto-orbital gyrus, so even slight retraction and elevation
of the frontal lobe can cause intraoperative rupture, for
example, during subfrontal dissection toward the lamina
terminalis. Therefore, in the ruptured anteriorly projecting
ICAbifAs, we prefer not to approach the chiasm and the
lamina terminalis until the aneurysm dome has been
dissected free. Unruptured anterior projecting ICAbifAs
can be also approached from the contralateral side, but our
preference is ipsilateral.
7.1.2. Head positioning and craniotomy
The head is extended, rotated about 20° to 30° toward the
contralateral side with a moderate lateral tilt to get the
proximal part of the sylvian fissure into almost vertical
position. The head is extended to expose the ICA bifurcation,
which would otherwise remain behind the frontal lobe. The
LSO craniotomy is performed in the standard fashion, and
the sphenoid ridge may be partially drilled off.
7.1.3. Dissection toward the aneurysm
The proximal part of the sylvian fissure is entered, and
CSF is released from the carotid cistern. The goal is to
identify the anterolateral wall of the ICA proximal to the
 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667
aneurysm. In acute SAH with tight brain, further CSF can be
released from the optic cistern. The frontal lobe should be
retracted and elevated as little as possible during the initial
steps of the dissection to prevent intraoperative rupture.
Once site for the proximal control on the ICA has been
prepared, dissection proceeds toward the aneurysm. The M1
is identified, and the aneurysm dome is dissected free from it.
The A1 is usually hidden by the aneurysm. With good
proximal and preferably also distal control, the dissection
can be now continued toward the chiasm, with the goal to
open the lamina terminalis with sharp forceps to further
release CSF. Ventriculostomy may also be considered if the
brain is swollen due to SAH, leaving no room to reach
lamina terminalis safely, but it might be difficult to perform
because of the complex head position.
7.1.4. Clipping
It is safer to dissect the aneurysm dome free under
temporary clipping. Attention should be paid to identify the
branches and perforators of the ICA, M1, and A1 trunks,
including the RAH. Large anteriorly projecting ICAbifA
may initially obstruct the view toward the A1 trunk,
preventing temporary clipping of the A1. The pilot clip is
inserted with the temporary clips on. The temporary clips
should be short and light so that they do not obstruct the view
toward the aneurysm base and do not damage the perforators.
The aneurysm sac is then opened and eventually reshaped
with bipolar coagulation, and the final clip is inserted. After
the temporary clips have been removed, the perforators are
rechecked once again.
7.2. Superiorly projecting ICAbifAs
7.2.1. Planning
The superiorly or upward projecting ICAbifAs originate
from the superior aspect of the ICA bifurcation (Figs. 6A-E
Fig. 8. Superior projecting ruptured ICAbifA with calcified wall. A: Preoperative coronal CTA showing calcification in the wall. B: Preoperative 3D CTA
reconstruction. C: Postoperative DSA showing patent ICA, M1, and A1 but no filling in the aneurysm.
663
and 8A-F; see video ICAbifA—3 Hernesniemi). Because of
their vertical dome orientation, they are located higher than
other ICAbifAs so that complete dissection of the dome
requires slightly more elevation of the frontal lobe. The
posterior and lateral walls are often involved with perfora-
tors, which have to be identified and separated before
clipping. Because of the dome orientation, the base can be
approached relatively safely and controlled before dissecting
the entire dome free. Unruptured superiorly projecting
ICAbifAs can also be approached from the contralateral
side, but then, the visualization of the perforators may be
more tedious. We do not see any particular advantage in the
contralateral approach, although we have a large experience
with this approach. The superiorly projecting ICAbifAs
occasionally present with a frontal ICH but no blood in the
subarachnoid space.
7.2.2. Head positioning and craniotomy
The head has to be extended little more than for the other
ICAbifAs to get higher from the skull base. Rotation and
lateral tilt are similar as for the other ICAbifAs. The LSO
craniotomy and drilling of the sphenoid ridge is performed in
a standard fashion.
7.2.3. Dissection toward the aneurysm
The dissection starts along the orbital roof toward the
suprasellar and optic cistern to release CSF. In acute SAH
with tight brain, the dissection is continued subfrontally
toward the lamina terminalis, which is opened and further
CSF is released. Once the brain has been relaxed and there is
more room, the proximal part of the sylvian fissure is entered.
Dissection of the sylvian fissure continues along the M1 trunk
toward the ICA, and the ICA trunk is followed to the proximal
direction, and the site for a proximal clip is prepared. The A1
trunk is then visualized and also prepared for temporary
clipping. Finally, the base of the aneurysm is dissected free.
664 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667
7.2.4. Clipping
A pilot clip is inserted over the aneurysm base under
temporary clipping. The ideal direction for final clipping
would be along the M1 trunk to prevent perforator occlusion.
However, the pilot clip has to be often inserted perpendicular
on the bifurcation because the dome is not yet mobile. When
inserting the pilot clip, utmost care is needed not to include
any perforators in the clip. The longer and wider the clip
blades are, the higher the risk of perforator occlusion. With the
pilot clip on, the aneurysm dome can be dissected from its
surroundings, and in particular, the back wall has to be
checked to ensure that no perforators are attached to it. The
final clip, as short as possible to minimize perforator damage,
is placed over the neck avoiding the perforators, and other
branches, including the AChA and the RAH. Whether a
straight or slightly curved clip is used depends on the 3D
anatomy. We do not recommend aggressive coagulation and
reshaping of the aneurysm due to high risk of perforator injury.
7.3. Posteriorly projecting ICAbifAs
7.3.1. Planning
The posteriorly or backward projecting ICAbifAs
originate from the superior and posterior aspect of the
ICA bifurcation (Fig. 5). They are usually the most
challenging ICAbifAs but fortunately also the least frequent
ones. They are heavily involved with the perforators, posing
the greatest risk for perforator injury. The dome is partially
obstructed by the ICA so that proper visualization of the
perforators, even if the aneurysm dome is small, is
particularly difficult. While clipping, an aneurysm remnant
is easily left unnoticed at the dead angle behind the ICA
trunk. The contralateral approach to the posteriorly project-
ing ICAbifAs is not advisable because it is extremely
difficult to get a proper visualization of the perforators that
envelope major part of the aneurysm dome.
7.3.2. Head positioning and craniotomy
The head position is similar to that for the superiorly
projecting ICAbifAs, with somewhat less head extension.
The LSO craniotomy is performed in the standard fashion.
It might be necessary to drill the sphenoid ridge more
profoundly to provide a somewhat more lateral view
toward the ICA bifurcation and, in particular, to its
posterolateral portion.
7.3.3. Dissection toward the aneurysm
The dissection starts in the same way as for the
superiorly projecting ICAbifAs. After the release of CSF,
the proximal part of the sylvian fissure is entered, and the
M1 trunk is followed toward the ICA bifurcation.
Dissection continues along the ICA trunk with the
identification of all the branches originating form it. As
with the superiorly projecting ICAbifAs, a small resection
in the fronto-orbital gyrus may be necessary. Here, the exact
course of the AChA in relation to the aneurysm dome has to
be identified. The site for proximal control on the ICA is
prepared proximal to the ICA bifurcation, and the
perforator free zones of the A1 and M1 trunks are prepared
for distal temporary clipping.
7.3.4. Clipping
Under temporary clipping, the slack dome is dissected
free from all the perforators in its vicinity. The RAH will
probably run in front of the aneurysm, but it may also be
hidden behind the dome. A pilot clip is inserted avoiding the
perforators, and the dome is further dissected. Finally, the
clip is exchanged for as small and light final clip(s) as
possible. The perforators have to be once again checked by
manipulating and shifting the clipped aneurysm. Coagula-
tion and reshaping of the aneurysm are not recommended
due to high risk of perforator injury.
8. Associated aneurysms
The ICAbifAs are often associated with other IAs. In the
Kuopio series, 43% of all ICAbifA patients and 26% of
those with a ruptured ICAbifA had at least 1 additional IA
(Table 5). Bilateral ICAbifAs were seen in only 6%. Our
strategy is usually to clip all the IAs that can be exposed
through the same craniotomy. It is advisable to clip the
ruptured IA first, and if this succeeds without particular
difficulties, additional IAs can be treated in the same
session. We do not prefer to clip the associated IAs if the
brain is swollen due to acute SAH. In particular, the
contralateral approach is not advisable if there is lack of
space in the suprachiasmatic area. We do not recommend
multiple craniotomies in acute SAH. The technique of
clipping multiple IAs at different locations is not recom-
mended at early learning curve. The ICAbifA may also be
accompanied by mini blebs, not seen in the preoperative
images, with poorly known natural history. Depending on
the patient's age and sclerosis of the parent arteries, these
blebs may be reduced with bipolar coagulation under the
temporary clipping and covered by small piece of cotton to
induce scarring.
9. Giant ICAbifAs
Giant ICAbifAs comprised 7% of all ICAbifAs in the
Kuopio series. The dome of a giant ICAbifA is usually at
least partially covered by the frontal lobe and extends also
into the sylvian fissure. Giant ICAbifAs often involve the
origins of the A1 and the M1. Perforating arteries frequently
follow and/or arise from the base region of these IAs, and it
may be very difficult, even impossible, to dissect them free.
The large size, distorted anatomy, origins of the perforating
arteries and other arterial branches directly from the
aneurysm, calcifications at the base, and intraluminal
thrombus make microneurosurgical management of giant
ICAbifAs very difficult. Importance of the whole ICA
bifurcation complex generally also prevents proximal
occlusion or trapping of the aneurysm even if bypass is done.
 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667
Comprehensive preoperative imaging by CTA, DSA, and
MRI is mandatory. The 3D reconstructions of the CTA and
DSA data help to show the aneurysm orientation with respect
to the bony landmarks and to identify calcifications in the
aneurysm wall. In addition, DSA provides important
information about the flow dynamics of the ICA bifurcation
complex. In giant and complex ICAbifAs, we prefer
intraoperative DSA to disclose surprise occlusions.
We generally prefer modified, larger LSO approach for
the giant ICAbifAs. Head positioning and craniotomy should
allow optimal for visualization of the proximal ICA as well
as the adjacent arteries. The size of the craniotomy should be
adapted accordingly. In general, the bone flap needs to be
larger and extend more toward the temporal lobe than in the
standard LSO approach. For adequate visualization of the
aneurysm base, a more extensive exposure of the sylvian
fissure is needed. If the lamina terminalis can be reached
over the bulging mass of the aneurysm, it is opened and CSF
released. The surrounding arteries and perforators need to be
identified before clipping attempts. Calcifications in the
aneurysm wall or intraluminal thrombus may prevent
adequate clipping of the giant ICAbifA neck (see video
ICAbifA—4 Hernesniemi). Intraluminal thrombus can be
removed under temporary clipping, using repeated irrigation
with saline, suction, forceps, or an ultrasonic aspirator. The
goal is to dissect the base free so that the whole aneurysm can
be collapsed and its base closed by the final clip(s). Pilot
clipping and molding of the aneurysm base by vascular
clamp(s) for final clipping may be considered [49], but
utmost care is needed not to severe the surrounding
perforators. Once the dome is decompressed and if the
aneurysm wall is not heavily calcified, it is usually reduced
by bipolar coagulation to allow for final dissection of the
neck, before deciding how to perform the final clipping.
Again, care is taken not to sever the perforators. In case of
thin-walled ICAbifA with no thrombus inside, the aneurysm
sac can be directly opened under temporary clipping,
collapsed and shrunken by bipolar coagulation.
The base of the giant ICAbifA requires often complex clip
reconstruction. Multiple clips are applied to ensure complete
occlusion of the neck while leaving all the perforators and
branches originating from the neck open. The vessel origins
in the base can be reconstructed using fenestrated clips [42].
Aneurysms with thick and strong wall require several clips.
If the first clip slides on a broad base, a ring clip can be first
inserted to compress the distal part of the neck, thereafter a
straight second clip is placed proximally to close the
remaining neck inside the ring of the first clip (Drake's
tandem-clipping technique with fenestrated clips) [49]. If
required, especially in the ICAbifAs with a strong and
calcified base, part of the base is left open not to occlude the
origins of the A1 and/or the M1. With the neck clipped, one
must ensure that there is no kinking in the A1 and the M1 and
that the terminal ICA is open. The patency of the
surrounding arteries is checked with microvascular Doppler,
ICG angiography, and/or intraoperative DSA. Removal of
665
intraluminal thrombus may induce quick rethrombosis, and
therefore, we also advocate early postoperative angiography
to find surprise occlusions.
For the ICAbifAs, which significantly involve perfora-
tors, direct surgical clipping or trapping may not be
feasible. Parent vessel sacrifice with distal revascularization
by high-flow bypass may be the only treatment option in
these cases [78].
10. Fusiform ICAbifAs
Fusiform ICAbifAs are extremely rare, only 1 of 3005
patients in the Kuopio series (Table 2). They lack a definable
neck, which could be clipped while preserving the afferent or
efferent arteries (see video ICAbifA—6 Hernesniemi ). The
parent artery is either circumferentially involved in the
aneurysmal dilatation or it ends in a large thrombosed sac,
and its distal branches arise from the base of the sac [79].
Wrapping, trapping, excision, and bypass surgery can be
considered [64].
Acknowledgment
We thank Mr Ville Kärpijoki 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.2009.01.028.
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