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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


may represent more than 40% of all IAs in patients younger
We classify ICA aneurysms into 7 groups based on their
than 20 years [23,27,28,33,51]. There is no clear explana-
site of origin, wall morphology, and clinical or surgical
tion, but arterial wall deficits and wider angle of the ICA
behavior: (a) ICAextraAs, (b) ICApetrAs and ICAcavAs, (c)
bifurcation may be risk factors.
ICAophtAs, (d) ICAwallAs and ICAmalignantAs, (e) ICA-
The microneurosurgical exposure and clipping of ICAbi-
PCoAAs, (f) ICA-AChAAs, and (g) ICAbifAs (Table 1).
fAs is demanding due to (a) high position with respect to the
1.1. Internal carotid artery bifurcation aneurysms skull base, (b) attachment of the dome to the surrounding
brain parenchyma, (c) large number of perforators surround-
Dott [11] was the first neurosurgeon to treat an ICA ing the base and/or the dome, and (d) the relatively high risk
aneurysm by direct surgery, wrapping it with a piece of of intraoperative rupture. The orientation of the aneurysm
muscle in 1933. This was also the first surgical attempt to dome affects the clipping, with the posterior orientation
treat an IA [67]. Since that time, despite the advances in the being the most difficult. Precise dissection in the 3D
field of microneurosurgery, aneurysms at this location have anatomy of ICAbifAs and the surrounding perforators
remained difficult to treat. requires not only experience and microsurgical skill but
The ICAbifAs are located at the bifurcation of the ICA also patience to work on the aneurysm base under repeated
where it divides into the A1 segment of the ACA and the protection of temporary and pilot clips.
M1 segment of the MCA (Fig. 1). The ICA bifurcation is
usually the highest point of the Circle of Willis. The apex of 1.2. Purpose of the review
the ICA bifurcation, similar to the MCA bifurcation or the
This review, and the whole series on IAs, is intended for
tip of the basilar artery, is under particular hemodynamic
neurosurgeons who are subspecializing in neurovascular
stress and high wall shear stress [45]. This apparently adds
surgery. The purpose is to review the practical anatomy, the
to the risk of saccular IA formation through pathological
preoperative planning, and the avoidance of complications in
remodeling of the arterial wall of the branching site by
the microsurgical dissection and clipping of ICAbifAs.
impact, deflection, separation of CBF streamlines, and
vortex formation at the lateral angles [45,63]. The ICAbifAs 1.3. Authors
tend to arise rather at the junction of the ICA and the A1
The microneurosurgical technique in this review is
segment of the ACA than at the junction of the ICA and the
mainly based on the personal experience of the senior author
M1 segment of the MCA [46,65].
(JH) in 2 Finnish centers (Helsinki and Kuopio), which serve
The ICAbifAs are unusual lesions. Their most striking
without selection the catchment area in Southern and Eastern
feature is the younger age of patients at the time of rupture as
Finland. These 2 centers have treated more than 10 000
patients with IAs since 1951 and more than 9000 patients
Table 1 during microsurgical era since mid 1970s. The data
Categories of ICA aneurysms presented in our series of articles represent 3005 consecutive
Category Location patients harboring 4253 IAs from the Kuopio Cerebral
Aneurysm Database (1977-2005). The aim is to present a
ICAextra Extracranial ICA
ICAintra Intracranial extradural ICA consecutive, nonselected population-based series of IAs.
ICApetr Petrous segment ICA This database is not reflective of the personal series of the
ICAcav Intracavernous segment ICA senior author (JH) alone.
ICAopht Paraophthalmic ICA
ICAtrunk Medial, superior and inferior wall of ICA trunk
ICAwall Nonbranching sites of the ICA trunk wall 2. Occurrence of ICAbifAs
ICAmalignant Blister-like (malignant) of the ICA trunk
PCoA Origin of PCoA The ICAbifAs are reported to represent from 2% to 9%
AChA Origin of Anterior chroidal artery [5,21,35,37,46,67,79] of all IAs. Tables 2-5 present the
ICAbif ICA bifurcation 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) 649–667 653

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]
Fig. 3. Illustration demonstrating the different perforator groups near the MCA bifurcation aneurysms [8]
ICA bifurcation. Distal MCA aneurysms (M2-M4 segments) [7]

middle (22%) one third of the superior surface of the [16,34,38,59,85]. The superior hypophyseal arteries run
supraclinoid ICA below the optic nerve and above the dura medially under the optic chiasm to terminate in the tuber
of the cavernous sinus. Sometimes, it can arise already from cinereum, anterior lobe of the pituitary, and inferior surface
the cavernous segment (up to 8% ) of the ICA, but it is only of the optic nerve and the chiasm. Because the superior
very rarely absent altogether. The OphtA runs anterolaterally hypophyseal arteries may provide major blood supply to the
below and attached to the undersurface of the optic nerve to optic nerve and the chiasm, their preservation during
enter the optic canal. The intradural segment of the OphtA is dissection is of vital importance [34].
usually short, but it is often possible to visualize the origin
3.3.3. Posterior communicating artery
and the proximal segment of the OphtA without or with
The PCoA arises from the posteromedial, posterior, or
minor retraction of the optic nerve [17,52,56,59,85].
rarely from the medial wall of the supraclinoid ICA, 2 to
3.3.2. Superior hypophyseal arteries 8 mm after its origin [59]. Rare origin from the OphtA has
The superior hypophyseal arteries are a complex group of also been reported [2]. The PCoA runs backward and
small vessels (average, 2; range, 1-5) with a diameter of 0.1 medially, above the sella turcica, slightly above and medial
to 0.5 mm. They arise from the posteromedial, medial, or to the occulomotor nerve, and below the tuber cinereum to
posterior aspect of the ophthalmic segment of the ICA in the join the PCA in the interpeduncular cistern. Inside the carotid
midway between the origin of the OphtA and PCoA cistern, an arachnoid sleeve similar and adherent to that of

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).
654 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667

the occulomotor nerve covers the PCoA. The distal part of from the posterior side of the ICA wall and pass to (a) the
the PCoA may be in close relation to the dura of the posterior optic tract, (b) the premamillary part of the floor of the third
clinoid process or even lie inside the groove within the ventricle, (c) the optic chiasm, and (d) the infundibulum.
process [59,81,85]. The PCoA can be absent altogether in up They rarely enter the anterior or posterior perforating
to 14% of cases [81,85]. Fetal type of PCoA is marked by a substances [59]. The perforating branches of the choroidal
PCoA of large diameter, which courses more laterally, above segment (average, 4; range, 1-9) arise from the posterior half
or even lateral to the oculomotor nerve to join the posterior of the ICA wall, pass upward and terminate in (a) the anterior
circulation, where the proximal segment of the PCA (P1 perforating substance, (b) the optic tract, and (c) the uncus.
segment) is hypoplastic or aplastic [59]. Infundibular Some of these perforators may also arise from the ICA
dilatation of the PCoA is another frequent variation (in 6% bifurcation [44,60,62].
of cases) [59] and easily mistaken for aneurysm on
preoperative images. 3.3.8. Perforating branches around the ICA bifurcation
There are a large number of perforating branches with
3.3.4. Anterior choroid artery their course behind the ICA bifurcation. These perforators
The AChA is the first posterolateral branch distal to the arise from (a) the choroidal segment of the ICA, (b) the
PCoA. In most cases, it arises closer to the origin of AChA, (c) the RAH, (d) the MLAs, and (e) the LLAs (Fig. 3)
the PCoA (2-5 mm) than to the ICA bifurcation [60,85]. The [6,9,17,43,44,62,75,85]. These vessels may be stretched to
AChA is nearly always present [60], but it can sometimes varying degrees by the ICAbifAs or have their origins
originate also from other arteries such as the PCoA or the involved in the base of the aneurysm. Extreme care should be
MCA in up to 23% of cases [4,47,50,60,69]. The diameter of taken not to severe them during various stages of dissection
the AChA ranges from 0.5 to 2.0 mm, and the pattern of and clipping. They should be identified and if possible
origin of the artery may also be highly variable [60,85]. The protected during dissection or clipping by, for example, a
AChA may arise as a single trunk or multiple vessels from small cottonoid.
posterolateral wall of ICA. To identify and preserve the
AChA during different steps of dissection toward ICAbifAs 3.3.9. Anatomical variants of ICA, M1, and A1
or temporary clipping one should be aware of these possible Several variants of the supraclinoid ICA are known which
anatomic variations and the course of the AChA [88]. After may affect intraoperative orientation during dissection of
its origin in carotid cistern, the AChA enters the crural ICAbifAs: (a) hypoplastic ICA, (b) absent ICA, (c) ICA
cistern with a posteromedial direction and is often found trifurcation, (d) or persistence of fetal remnants [10,29,71]. A
behind the ICA bifurcation. The artery courses lateral and hypoplastic ICA diminishes in caliber at or shortly distal to its
inferior to the optic tract, passes through the wing of ambient origin. In these cases, the petrous and sellar segments are
cistern, to enter the choroidal fissure [60,85]. frequently also absent [71]. The exact incidence of
hypoplasia or aplasia of the ICA is not known but seems to
3.3.5. Uncal arteries be less than 0.01% [3,71] and is rare. Its cause is unknown,
The uncal arteries usually originate distal to the AChA or and only about 100 cases have been described in the literature
from the very proximal part of the MCA [85]. [10,18]. Three major patterns of collateral circulation have
3.3.6. Artery to the dura of the anterior clinoid process been described for hypoplasia/absence of the ICA (for details
The dural branch of the ICA is a small branch usually see de Medonca et al [10]). The ICA trifurcation is rare and
originating from the anterior wall of the ICA 3 to 5 mm results from the anomalies of the terminal part of the ICA
proximal to its bifurcation or rarely from the proximal A1 itself, from accessory origins of the AChA, and from the
segment. It passes toward the dura of the anterior clinoid absent M1 [29]. Fetal remnants of anastomosis between the
process. Avulsion of this artery due to retraction may cause carotid arteries and the vertebral system can persist [10].
bleeding from the wall of the parent artery [85]. Several vascular anomalies of both the M1 and A1
segments can occur. They have been previously described in
3.3.7. Perforating branches of the supraclinoid ICA
our papers on microneurosurgical management of proximal
Each segment of the supraclinoid ICA gives off a series of
MCA aneurysms and proximal ACA aneurysms [6,9].
perforating branches with a relatively constant site of
termination. During various steps of dissection and tempor-
3.4. Cisternal anatomy of supraclinoid ICA
ary clipping for ICAbifAs, a comprehensive knowledge of
the possible sites of origin and trajectories of these small An extensive review on the cisternal anatomy was
vessels is of paramount importance. The perforating previously published by Yaşargil et al [85,87]. Based on
branches arising from the ophthalmic segment (average, 4; the height of the ICA bifurcation and the size and projection
range, 1-7) arise from the posterior or medial wall of the ICA of the ICAbifA, a different combination of several cisterns,
and pass medially to (a) the optic nerve and the chiasm, (b) (a) the carotid cistern, (b) the olfactory cistern, (c) the lamina
the infundibulum, and (c) the floor of the third ventricle [59]. terminalis cistern, and (d) the sylvian cistern, may surround
The perforating branches arising from the communicating the aneurysm. Strict attention to these cisternal boundaries is
segment are rare. Infrequently, up to 3 small perforators arise mandatory for orientation to proper dissection planes [84].
M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667 655

During the dissection toward the ICAbifAs, to release terminalis cistern contains the A1 segment, the MLAs, the
CSF, opening of the carotid cistern is usually one of the first RAH, ACoA complex, the origins of A2 segments of the
intradural steps. The carotid cistern is limited superiorly by ACA, the orbitofrontal and rarely the frontopolar arteries,
the dura of the anterior clinoid process and the orbitofrontal and the anterior cerebral veins [85].
lobe; it shares the medial wall with the chiasmatic cistern; The M1 segment of the MCA begins at the carotid
the tentorial edge and mesial temporal lobe limit it laterally; bifurcation, lateral to the optic chiasm, and enters the sylvian
the inferior limit is the cavernous sinus; and posteriorly, it is cistern. In a similar way to the A1 segment, there are thick
limited by the crural cistern. The carotid cistern also shares arachnoid bands covering the very proximal part of the M1 at
“the Liliequist membrane,” a single membrane of arachnoid this point. The M1 then runs laterally and posteriorly until
with varying thickness, in common with the interpedun- the level of the limen insula [6,8,9,75-77].
cular cistern located at its inferior border. The supraclinoid
ICA, origins of its branches, and the fronto-orbital veins 3.5. Venous structures
draining into the sphenoparietal sinus are all within the
The superficial and deep venous structures of the ICA
carotid cistern. The supraclinoid ICA travels entirely inside
bifurcation region are complex and vary a lot [58,85].
the carotid cistern in a superior-anterior direction with a
Superficial middle and anterior cerebral veins run over or
variable degree of lateral bend toward the ICA bifurcation.
under the ICA bifurcation to reach the sphenoparietal or
The relation of the ICA and the optic nerve can vary from a
cavernous sinus [58,85]. The deep venous system, including
parallel course of the artery and the nerve to a concave or
the anterior and deep middle cerebral veins and the basal
convex curve of the artery compared to the nerve [85].
vein of Rosenthal, may be found near the inferior aspect of
Thick trabeculated arachnoid bands within the carotid
the ICA bifurcation [58,85]. Particular care is necessary
cistern are attached to the origin of the PCoA, the AChA,
during dissection and mobilization of the (a) ICA trunk, (b)
and the oculomotor nerve. A careful dissection of these
M1 trunk and (c) A1 trunk, and (d) their perforators so as not
arachnoid attachments is mandatory for mobilization of
to sever the veins.
the supraclinoid ICA [85]. Occasionally, the origin of the
PCoA may be heavily involved with the dura overlying 3.6. Classification of ICAbifAs according to the
the posterior clinoid process making the dissection even dome projection
more demanding.
The chiasmatic cistern or optic cistern contains the optic We find it essential to classify the ICAbifAs according to
nerves, pituitary stalk, branches from the supraclinoid ICA to the dome projection because it is important for the
these structures, and the OphtA. The lamina terminalis microsurgical approach and strategy. Like others
cistern located in front of the lamina terminalis is limited by [21,35,86], we classify the ICAbifAs into (a) anteriorly, (b)
the rostrum of the corpus callosum superiorly and the optic superiorly, and (c) posteriorly projecting (Fig. 5). The
chiasm inferiorly. The A1 arises from the ICA in the carotid anteriorly projecting ICAbifAs originate from the anterior
cistern and with a medial and somewhat anterior course aspect of the ICA bifurcation with their dome projecting into
enters the lamina terminalis cistern. A group of thick the lateral fronto-orbital gyrus or the base of the olfactory
arachnoid bands extending from the olfactory triangle to the tract. The superiorly projecting ICAbifAs originate from the
lateral side of optic nerve encase the A1 segment at this point superior aspect of the ICA bifurcation with their dome
[62,85]. This is important to note when dissecting and projecting into the anterior perforated substance, the lateral
mobilizing the ICA bifurcation complex. The lamina portion of the lamina terminalis cistern, or the sylvian

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.
656 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667

cistern. The posteriorly projecting ICAbifAs originate from In the coronal section, the right supraclinoid ICA (C4) had
the posterior aspect of the ICA bifurcation with their dome straight course in 107 (54%) patients and the left one in 118
projecting into the carotid and interpeduncular or even the (59%) patients. Lateral or medial curvature was seen in 91
ambient and crural cisterns. (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°)
4. Imaging of ICAbifAs on the right and 38° (range, 4°-87°) on the left. Both the
course and lateral deviation of the ICA is important to asses
Digital subtraction angiography is still the present “gold from the preoperative images to allow for optimal head
standard” in many centers. Multislice helical CTA is the positioning and visualization of the ICAbifA.
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 5. Microneurosurgical strategy with ICAbifAs
imaging technique; (c) the comparable sensitivity and
specificity to DSA in aneurysms larger than 2 mm The ICAbifAs are challenging to approach because they
[19,30,31,68,73,80,82,83]; (d) the disclosure of calcifica- are located at the highest point of the ICA, overlaid by the
tions in the walls of arteries and the aneurysm [13,66]; and frontal lobe and surrounded by perforators. The surgical
(e) the quick reconstruction of 3D images that, for example, trajectory should provide optimal visualization of the whole
show the surgeon's view of the ICA bifurcation. Some ICA bifurcation and the ICAbifA with the least possible brain
ICAbifAs may be difficult to visualize by routine 3D CTA retraction. The aim of the microneurosurgical clipping is the
[30,66], usually due to very small size, so that subsequent total occlusion of the aneurysms sac with preservation of flow
rotational 3D DSA is required. Occasionally, ICAbifAs may in the main branches and the perforating arteries surrounding
be difficult to visualize by routine DSA or CTA, mostly the aneurysm dome. The perforators in the ICA bifurcation
small ones or those projecting backward, so that subsequent region (RAH, MLAs, LLAs, AChA, PCoA) may be adherent
oblique projections or rotational images are need. to the dome and may be severed during (a) retraction, (b)
For intraoperative navigation, 3D CTA and/or DSA dissection, (c) coagulation, (d) kinking, (e) compression for
reconstructions should be rotated to illustrate (a) the hemostasis, (f) temporary occlusion, or (g) final clipping. It is
angioarchitecture of the ICA bifurcation and its relation to important to familiarize oneself with the 3D angioarchitecture
the skull base, (b) projection of the ICAbifA dome and its of the ICA bifurcation complex in each case and to orientate
relationship to the A1 and M1 segments, and (c) the site of accordingly during the microneurosurgical dissection to
possible rupture. Other lesions of the ICA should be spare the vessels. The projection of the aneurysm dome has
differentiated and vascular aberrations should be looked to be considered during the head positioning to provide a
for, and their possible impact on flow conditions at the ICA clear view to the dome and to optimize the view to dissect the
bifurcation should be assessed. In giant and fusiform perforators, many of which are hidden behind the dome. The
ICAbifAs, MRI with different sequences, along with 3D CTA is helpful in evaluating the bony relations, trajectory of
CTA, helps to distinguish the true wall of the aneurysm and the ICA, and the height of the ICA bifurcation. High position
the intraluminal thrombosis. of the ICA tip will require a careful and clean dissection in the
In the workstation, 3D CTA images can be rotated narrow angle of the very proximal part of the sylvian fissure.
accordingly to evaluate the surgeon's view to the ICA In addition, the basal vein of Rosenthal with its tributaries and
bifurcation, which is not standard but is tailored according to the medial sylvian vein must be secured to avoid unpredict-
the dome's projection and relation to the M1 and A1 able postoperative complications.
segments. The prime concern is to find a view that best helps
5.1. Neuroanesthesiological principles
to preserve the perforators around the base and the dome of
the aneurysm. A general review of our neuroanesthosiological principles
has been published previously [55].
4.1. The CTA anatomy of the ICA bifurcations in
200 patients 5.2. Intracerebral hematoma
The regions of both ICA bifurcations were studied in 200 In the Kuopio series, ruptured ICAbifAs were associated
patients who underwent CTA for IAs from September 2007 with ICH in 19%. Occasionally, there was only the ICH with
to June 2008 at Helsinki University Hospital. no additional blood in the subarachnoid space. The ICH is
Below the ICA bifurcation, the mean diameter of the right usually located in the frontal lobe, in 73% in the Kuopio
ICA was 3.6 mm (range, 2.0-6.1 mm) and that of the left ICA series. In our practice, patients with massive ICH are
3.7 mm (range, 2.0-5.8 mm). Perforators were seen in 94% transferred directly to operating room after acute CTA for
in the right ICA bifurcation region (median, 3; range, 1-7) immediate removal of the ICH and aneurysm clipping. The
and in 97% in the left ICA bifurcation region (median, 3; relative close proximity of ICAbifAs to the ventricular
range, 1-5). system predisposes to IVH (Table 4), which is an
M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667 657

independent risk factor for poor outcome in aneurysmal the classical pterional approach by the senior author (JH).
SAH [61]. The LSO craniotomy is a more subfrontal and less invasive
modification of the pterional approach for the anterior
5.3. Acute hydrocephalus circulation aneurysms [25]. The LSO craniotomy, described
in detail elsewhere [25], is demonstrated on video in our
In case of acute hydrocephalus, 38% in the Kuopio series
article on the aneurysms on the M1 segment of the MCA in
(Table 3), we have 3 primary treatment options: (a) opening
Surgical Neurology [9] (Table 6). This approach illustrates
the lamina terminalis for CSF removal before clipping; (b)
the philosophy of applying minimally invasive techniques to
placing ventricular drainage, often through the lamina
enhance a surgical exposure while minimizing the need for
terminalis, in most cases after securing the ruptured
brain retraction. Because the angle of approach toward the
aneurysm; and (c) in severe cases, we may insert external
ICAbifA is little less lateral than that provided by the
ventricular drainage before or in the beginning of the
pterional approach, patency of all the perforators hidden by
craniotomy. These procedures also allow removal of blood
the aneurysm dome needs to be checked even more
from the ventricular system.
meticulously once the final clip is in place. Proper choice
5.4. Approach and craniotomy of the length of the final clip plays an important role here.
Briefly, the head fixed to the head frame is (a) elevated
Exposure of the ICAbifA surgery depends on several clearly above the cardiac level, (b) rotated toward the
factors: (a) deviation of the ICAbifA base with respect to the opposite side according to the projection of the ICAbifA
A1 and M1 segments, (b) presence of ICH and/or IVH, (c) the dome, (c) tilted somewhat laterally to visualize the ICA
length of the supraclinoid ICA and the height of ICA tip from bifurcation complex, and (d) extended. The goal is to have the
the skull base, (d) lateral or medial deviation of the ICA very proximal part of the Sylvian fissure almost vertical.
bifurcation with respect to the optic nerve and the Because ICAbifAs are located higher than other ICA
occulomotor nerve, (e) size and orientation of the ICAbifA aneurysms, the head has to be extended more than for other
dome, (f) presence and extent of atherosclerotic plaques in the locations. It is our practice to adjust the position of the fixed
parent artery and the aneurysm base, (g) presence of head and body during the operation as needed [26]. We prefer
associated aneurysms, (h) preexisting neurological deficits, to use a Sugita head frame with 4-point fixation. Besides
and (i) possible earlier operations. The proper surgical providing good retraction force by its fishhooks, it allows the
approach requires a mental spatial view of the angioarchi- surgeon to rotate the head during microsurgery. If this feature
tecture of the ICA bifurcation and its relation to the is not available, the table can be rotated as needed [26].
surrounding structures. This affects the head position, the After minimal shaving, an oblique frontotemporal skin
extent of craniotomy, selecting the proper place for arachnoid incision is made behind the hairline (see also the video M1A-
opening, and the intrasylvian orientation. In addition, the 1 in Dashti et al [9]). The incision stops 2 to 3 cm above the
approach also depends on the personal experience. zygoma, and the temporal muscle is split vertically by a short
Generally, ICAbifAs are approached from the ipsilateral incision. The 1-layer skin-muscle flap is retracted frontally
side, especially if ruptured and associated with ICH. The by spring hooks until the superior orbital rim and the anterior
presence of other aneurysms may influence the surgical zygomatic arch are exposed. The extent of craniotomy
approach if clipping of all available aneurysms is attempted depends on the surgeon's experience, the projection of the
through the same exposure. Unruptured ICAbifAs with the ICAbifA, and the presence of ICH. Usually, a small LSO
dome projecting anteriorly or superiorly dome can be also craniotomy is all that is necessary. A single burr hole is
approached from the contralateral side over the midline, placed just under the temporal line in the bone, the superior
provided that the ICA tip is not too high and there are no large insertion of the temporal muscle. The bone flap of 3 × 3 cm is
venous structures obstructing the view (see video ICAbifA— detached mostly by the side-cutting drill, and the basal part
7 Hernesniemi). In all the posteriorly projecting ICAbifAs can be drilled before lifting. In case of ICH or backward
and large superiorly projecting ICAbifAs, proper visualiza- projecting ICAbifA, the lateral sphenoid ridge is drilled to
tion of the perforators attached to the posterior wall of the create a more lateral view to the ICA bifurcation complex.
aneurysm would be very difficult from the contralateral side The dura is incised curvilinearly with the base sphenoid-
and would lead to injury. The contralateral approach requires ally. Dural edges are elevated by multiple stitches, extended
more retraction/lifting of the frontal lobe, and we do not over craniotomy dressings. From this point on, all surgery is
recommend it in acute SAH and brain swelling. Reoperation performed under the operating microscope, including the
of a recently clipped ICAbifA can be performed from the skin closure.
same side as arachnoid scarring has not yet developed, but 5.5. Intracerebral hematoma
later, the contralateral approach should be considered.
The standard pterional approach, introduced by Yaşargil In case of large ICH and lack of space, even after removal
et al [84,86], has been widely used for ICAbifAs by many of CSF from the basal cisterns, a small cortical incision is
authors [5,14,22,37]. In our practice, the LSO as a more made accordingly, avoiding the Broca area, and some
direct and simple approach for the ICAbifAs is preferred to 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 the sphenoparietal or cavernous sinuses. These veins are
through the ICH cavity. In removing ICH clot, before or after generally running on the temporal side of the sylvian fissure.
clipping, minor force should be applied not to sever the Principally, we prefer to dissect the arachnoid covering of the
perforating arteries. Intracerebral hematoma in the immedi- sylvian fissure on the frontal side. In the presence of multiple
ate vicinity of the aneurysm should be left in place until the large veins or anatomic variations, however, dissection plan
proximal and distal control has been obtained. Finally, more should be tailored. Dissection of the sylvian fissure is more
ICH can be removed at the end of operation. difficult in acute SAH with swollen brain or due to adhesions
from previous SAH or microsurgery. Preservation of the
5.6. Cerebrospinal fluid drainage dissection plane is mandatory.
We usually open a small window in the arachnoid with a
In most unruptured ICAbifAs, the carotid cistern and the
pair of jeweler forceps or a sharp needle acting as arachnoid
chiasmatic cistern are opened to gradually release CSF. In
knife and then expand the sylvian fissure by injecting water
ruptured ICAbifAs, we begin the subfrontal dissection from
using a handheld syringe, that is, the water dissection
the suprasellar cistern toward the chiasm and open the
technique of Toth [48]. The idea is to get relatively deep into
lamina terminalis for additional CSF removal. The only
the sylvian fissure to enter the cistern of sylvian fissure from
exception is very few cases in which the aneurysm does not
this small arachnoid opening. Once inside the sylvian cistern,
allow approach toward lamina terminalis. For the anteriorly
the dissection proceeds proximally by gently spreading the
projecting ICAbifAs (see below), retraction of the frontal
fissure in an inside-out manner. In our experience, this
lobe may risk rupture of the aneurysm. In these cases, we
technique has proven to allow easier identification of the
advise not to retract the frontal lobe and not to open the
proper dissection plane. Cottonoids are often soft means of
lamina terminalis until proximal control of the ICA has
dissection and retraction during this stage. Pressure on both
been established. Intraoperative ventricular puncture is
walls of the fissure will stretch the overlying bridging tissues,
rarely adopted.
facilitating their sharp dissection. All arachnoid attachments
5.7. Dissection toward ICAbifA and strands are cut sharply by microscissors, which can be
also used as a dissector when the tips are closed. To preserve
The first and most important precaution when approach- larger veins, some small bridging veins may be coagulated
ing the ICAbifAs is to prepare a site for proximal control of and dissected if needed. It is very important not to retract the
the ICA, usually just above the origin of the AChA. All the frontal lobe because the dome of the aneurysm is usually
initial steps of the dissection are oriented toward this goal. buried in subfrontal cortex. Bipolar forceps and suction act
Dissection of carotid and optic cisterns at the very early steps both as dissection instruments and also as delicate micro-
of surgery is continued with the identification of proper place retractors [26].
for the temporary clips on the proximal ICA. The shape and Once the proximal part of the MCA (M1 segment) is
size of anterior clinoid process and its relation with the ICA identified, the dissection should continue along its lateral
should once more be evaluated under magnification of the surface to identify the anterolateral wall of the ICA. At this
operating microscope. A small branch of intracranial ICA is point, the arachnoid of the sylvian cistern is converging the
usually arising from the superomedial aspect of the artery carotid, olfactory, lamina terminalis, and optic cisterns,
and penetrating the dura covering the anterior clinoid which may all be in contact with the aneurysm to various
process. This artery should be identified and either preserved degrees. We do not start to dissect the aneurysm base at this
or coagulated because it may be torn at its origin producing a point yet. Instead, we proceed with further dissection of the
hole in the parent artery, a situation usually difficult to carotid cistern and the optic cistern and identify the lateral
manage. In addition to the proximal control, it is advisable to branches of the ICA, that is, AChA and PCoA, and we
have distal control of both the M1 and A1 segments as well. enhance mobilization of the frontal lobe and remove tension
Especially with large ICAbifAs, it may initially prove on the sylvian veins.
difficult to expose the A1 without risking rupture of the When approaching the superiorly or posteriorly oriented
aneurysm, and it may be necessary to wait for later stages of ICAbifAs, our technique is to first identify the proximal M1
the surgery before the A1 can be adequately uncovered. segment inside the sylvian fissure and then move along the
The next step is dissection of the proximal one third of the M1 toward the ICA bifurcation. From there, the dissection is
sylvian fissure. For most ICAbifAs, only the very proximal oriented along the ICA to prepare site for proximal control.
part of the sylvian fissure, some 1 to 2 cm, needs to be Finally, we dissect deeper and visualize the A1 segment
opened. In large or giant ICAbifAs, a more extensive more medially. For the anteriorly oriented ICAbifAs, the
opening of the sylvian fissure may be required. The exact dissection starts with opening of the very proximal part of the
point of entry into the sylvian fissure is not critical, and the sylvian fissure to identify the ICA bifurcation directly. The
most advantageous spot is usually where transparent dissection then continues proximally along the ICA to
arachnoid is present. The venous anatomy on the surface prepare a site for the proximal control, and then the M1
of the sylvian fissure is highly variable. Multiple large veins segment is exposed to gain distal control. The A1 remains
often follow the course of the sylvian fissure, draining into often hidden behind the aneurysm dome at this stage. During
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the exposure of the ICA, the M1, and A1, the goal is also to hidden behind the dome, it may be necessary to first place a
locate and identify all the branches and perforators in the area pilot clip at the aneurysm base and with that in place to
so that their location and course is clear before applying continue dissection of the perforators. A small cottonoid can
temporary clips or final clips. be used to protect and mobilize perforators during the final
At this stage of dissection, a proper place for temporary dissection. Good proximal and distal control together with
clip application should be prepared. We prefer to apply the checking of the patency of the surrounding perforating
temporary clip distal to the origin of the AChA in a branches is key to the successful clipping of the ICAbifA.
perforator free zone. Presence of associated aneurysm on the 6.2. Dissection under temporary clipping of arteries
ipsilateral ICA, severe atherosclerosis, and calcifications or
large size of the ICAbifA necessitate more proximal location. Nowadays we use temporary clipping nearly always both
With the sites for proximal control of the ICA and distal during the dissection and clipping of the ICAbifA. Their use
control of M1 secured, dissection and preparation of the reduces intraluminal pressure and facilitates sharp dissection
ipsilateral A1 segment for temporary clipping are the next of both the aneurysm and the adjacent arteries. Dissection and
advisable step. This may facilitate control of contralateral preparation of the sites for the temporary clip(s) in the
flow to the aneurysm. Our practice is to direct the dissection perforator free zones of the ICA, M1, and A1 should be
medially toward the olfactory and lamina terminalis cistern performed with sharp dissection with fine-tipped bipolar
to identify the A1 segment, its perforators, and RAH. This is forceps or with microdissector. Blunt tip forceps can simulate
usually applicable for posteriorly or superiorly projecting placement of temporary or pilot clip. One temporary clip,
ICAbifAs. However, in case of anterior projecting ICAbifAs usually a small one, curved or straight, is applied proximal to
or large and giant aneurysms, the risk of premature rupture of the aneurysm on the ICA. We prefer the location just
the aneurysm is a real challenge. proximal to the ICA bifurcation, distal to the AChA. Care is
During the exposure of the ICA, the M1, and the A1, the needed not to include perforators or the AChA inside the
goal is to locate the point of origin and trajectory of all the temporary clip. Using as short temporary clips as possible,
perforators, which may be adherent to the posterior wall of only enough to occlude the whole ICA, can often prevent this.
the aneurysm and to preserve them during various stages of The second small straight temporary clip is applied on the M1
dissection, temporary, or final clipping. Furthermore, the trunk avoiding the LLAs. The third clip is placed on the A1
course of the PCoA and the AChA must be determined and where extreme care is needed not to involve the RAH or the
the relationship of their branches to the aneurysm dome perforators. If the A1 trunk cannot be reached safely due to,
noted. The temporopolar and the anterior temporal arteries for example, large aneurysm sac, dissection has to proceed
should be mobilized over few millimeters so that they will with temporary clips placed on the ICA and the M1 only. A
not be torn by retraction. The dissection then always small cottonoid can be placed over the temporary clip to
continues to visualize the ICA perforators. In case of small gently press it aside and to protect it from dissecting
ICAbifA, these perforators will usually be free, but they may instruments. To prevent ischemic brain injury, temporary
be involved with large or giant ones; usually, perforators are occlusion should be as short as possible, each period less than
better seen after temporary and/or pilot clipping. In addition 5 minutes.
to the MLAs originating from the A1, also the RAH has to be Under temporary clipping, the dissection of the ICAbifA
visualized. The dome of the ICAbifA is often adherent to or can proceed safely. Arachnoid adhesions can be further
buried in the orbitobasal frontal lobe, so retraction of the separated by microscissors. The dissection continues around
frontal lobe should be minimal during the dissection. In case the aneurysm base to prepare site for the pilot clip. All the
of acute SAH or when the ICAbifA is embedded in the perforators should be freed from the base, most of them will
frontal lobe, a small resection at the frontobasal cortex may be on the posterior aspect of the aneurysm. Occasionally, the
be necessary. aneurysm dome is partially or fully buried in the fronto-
Use of mechanical retractors should be avoided until orbital lobe. The pia mater will then be opened around the
dissection is completed and aneurysm base is exposed. At aneurysm dome, and a few millimeters of subpial tissue is
this stage, retractors may help clipping by retaining space. 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
6. Dissection and clipping of the ICAbifA aneurysm neck. If significant venous bleeding occurs during
the dissection of the inferior-posterior aspect of the
6.1. General principles
aneurysm, injury to the basal vein of Rosenthal should be
The close proximity of several perforator groups makes suspected. When the main part of the aneurysm base is freed,
the dissection of the ICAbifA tedious in the narrow working a short, straight pilot clip is applied along the direction of the
channel in the proximal part of the sylvian fissure [9] (Figs. 4 M1 trunk to prevent perforators accidentally slipping into the
and 6). The aneurysm base with the adjacent arterial clip. Temporary clips should be removed in distal to
branches should be visualized before clipping. If the proximal order. When removing temporary clips, they are
ICAbifA is obstructing the view toward the perforators 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 the arteries and bipolar shaping of the aneurysm dome is
difficulties in placing the clip back. While removing the used. To prevent kinking or occlusion of adjacent branches,
temporary clips, even the slightest resistance should be noted the smallest but adequate final clip should be selected. If
as possible involvement of a small attached branch in the clip bipolar reshaping is not considered, then the blade of a single
or its applier. occluding clip should be one and a half times the width of the
6.3. Clipping of the ICAbifA base base as suggested by Drake. Frequent short-term application
of temporary clips during the placement and replacement of
A proper selection of clips with different shapes and aneurysm clips is routine in our practice. We prefer inserting
lengths of blades, and applicators, suiting the imaged first a pilot clip to the ICAbifA dome, preferring Sugita clips
ICAbifA anatomy, should be ready for use. A limited for their wide opening and blunt tips. In large or complex
selection of final clips is needed when temporary clipping of ICAbifAs, stepwise clipping of the aneurysm dome toward
M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667 661

the base with further dissection facilitates complete occlu- pilot clipping under local flow arrest. A small and thin-
sion. The pilot clip is later exchanged for a smaller and walled ICAbifA may rupture at its neck during dissection. In
lighter final clip after reshaping of the dome by bipolar such a case, under temporary clipping, reconstruction of the
coagulation to make the neck smaller. base by including a small part of the parent artery inside the
The clip is generally best introduced across the neck of clip should be attempted.
the aneurysm along M1 trunk, slowly wiggling the blades
between the neck of the aneurysm and the ACA and the 6.5. Very small ICAbifAs
MCA as well as their branches to avoid crimping of the Very small (2-3 mm) ICAbifAs may be difficult to
parent artery or “dog earing” of the aneurysm. As the clip is identify preoperatively and intraoperatively due to super-
slowly closed, the surrounding arteries and perforators are imposition of the ICA and its branches. In very small
inspected for kinking, twisting, and compromised flow. With ICAbifAs, clipping is difficult because their wall is thin and
the final clip in place, the whole aneurysm dome should be fragile. Without temporary clipping, the final clip would
freed and checked that no perforators or other arteries (RAH, easily tear the whole aneurysm off and leave a hole in the
MLAs, LLAs, AChA) are attached to its wall and involved ICA, which would be very difficult to control. Temporary
inside the final clip. After the clipping, the aneurysm dome is clipping reduces intraluminal pressure and softens the dome
punctured and the collapsed sac can be mobilized, so that a straight or gently curved microclip can be placed
coagulated, transected, and removed. The clip blades should over the aneurysm without compromising the perforators.
completely close the neck of the aneurysm. To ensure With minimal reduction of the arterial lumen, a thin portion
complete occlusion, under temporary clipping, the final clip of the healthy arterial wall is taken inside the clip for safe
is opened and the escaping remnants of the aneurysm sac are closure of the neck. If the first clip slides exposing some of
pulled inside the final clip with suction or ring forceps to the neck, double clipping may be applied (see above).
ensure complete occlusion. Adequate dissection, proper
sizes of clips, and careful checking that the clip blades are 6.6. Intraoperative verification of clipping
well placed up to their tips are required to preserve the We routinely use microvascular Doppler to check the flow
adjacent branches. If the first clip slides, exposing some of in the proximal and distal arteries and branches after
the neck, another clip may be applied proximal to the first clipping, but unexpected occlusions are still sometimes
one for final closure (“double clipping”). Multiple clipping seen in the postoperative angiography [32]. Nowadays, we
using 2 or more clips is occasionally required for wide-based routinely use noninvasive ICG infrared angiography [53,54].
aneurysms. Previously coiled ICAbifAs (see video ICAbifA The ICG angiography reduces the need of intraoperative
—6 Hernesniemi) pose additional difficulties for adequate catheter angiography for clipping control. It allows intrao-
clip placement because there may not be enough free base for perative confirmation of the patency of the main arterial
safe application of the clip. In such a situation, one should branches and of the perforators deep inside the surgical field
consider removing some or all of the coils under temporary [70]. In giant and complex ICAbifAs, catheter angiography
clipping to provide extra room for the clip at the base [72]. under the digital C-frame guidance with memory is needed
Removal of the retractors and cottonoids may cause kinking for intraoperative assessment of the flow.
of the parent artery or compression of the perforators by the
clip. The flow in the branches should be checked once more 6.7. Resection of the ICAbifA dome
and papaverin applied.
The dome can be resected for the final check of closure
6.4. ICAbifA rupture before clipping and for research purposes [15,36,74]. In some large and giant
aneurysms, clipping is not possible without opening the
The ICAbifA may rupture during any step of the
aneurysm and emptying the aneurysm sac, which makes it
approach or the dissection. The 2 most common causes of
possible to adapt the resected walls together with final clips.
intraoperative rupture are lifting of the frontal lobe and
This policy teaches one to dissect the aneurysm domes more
dislocation of the ICA while the aneurysm dome is still
completely, thereby avoiding unexpected closure of the
adherent to the frontal lobe. The risk is highest for the
perforators (see above). It also allows inspection of the
anteriorly projecting ICAbifAs. In case of rupture, control
posterior surface of the aneurysm to ensure that the final clip
should be first attempted via suction and compression of the
has not caught any of the perforators.
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 7. Considerations for individual ICAbifA
pilot clip in case of uncontrolled bleeding. If the rupture dome projections
takes place before completing the dissection, there is no
7.1. Anteriorly projecting ICAbifA
point in trying to clip the aneurysm because this might
produce severe lesion in the bifurcation or the aneurysm. 7.1.1. Planning
Temporary clips must be applied to the parent vessels The anteriorly or “forward” projecting ICAbifAs
proximally and distally, and the aneurysm is prepared for 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 7.1.2. Head positioning and craniotomy
generally easier to visualize during dissection, and they are The head is extended, rotated about 20° to 30° toward the
less involved with perforators than other ICAbifAs. The contralateral side with a moderate lateral tilt to get the
anteriorly projecting ICAbifAs are often embedded in the proximal part of the sylvian fissure into almost vertical
fronto-orbital gyrus, so even slight retraction and elevation position. The head is extended to expose the ICA bifurcation,
of the frontal lobe can cause intraoperative rupture, for which would otherwise remain behind the frontal lobe. The
example, during subfrontal dissection toward the lamina LSO craniotomy is performed in the standard fashion, and
terminalis. Therefore, in the ruptured anteriorly projecting the sphenoid ridge may be partially drilled off.
ICAbifAs, we prefer not to approach the chiasm and the
lamina terminalis until the aneurysm dome has been 7.1.3. Dissection toward the aneurysm
dissected free. Unruptured anterior projecting ICAbifAs The proximal part of the sylvian fissure is entered, and
can be also approached from the contralateral side, but our CSF is released from the carotid cistern. The goal is to
preference is ipsilateral. identify the anterolateral wall of the ICA proximal to the
M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667 663

aneurysm. In acute SAH with tight brain, further CSF can be and 8A-F; see video ICAbifA—3 Hernesniemi). Because of
released from the optic cistern. The frontal lobe should be their vertical dome orientation, they are located higher than
retracted and elevated as little as possible during the initial other ICAbifAs so that complete dissection of the dome
steps of the dissection to prevent intraoperative rupture. requires slightly more elevation of the frontal lobe. The
Once site for the proximal control on the ICA has been posterior and lateral walls are often involved with perfora-
prepared, dissection proceeds toward the aneurysm. The M1 tors, which have to be identified and separated before
is identified, and the aneurysm dome is dissected free from it. clipping. Because of the dome orientation, the base can be
The A1 is usually hidden by the aneurysm. With good approached relatively safely and controlled before dissecting
proximal and preferably also distal control, the dissection the entire dome free. Unruptured superiorly projecting
can be now continued toward the chiasm, with the goal to ICAbifAs can also be approached from the contralateral
open the lamina terminalis with sharp forceps to further side, but then, the visualization of the perforators may be
release CSF. Ventriculostomy may also be considered if the more tedious. We do not see any particular advantage in the
brain is swollen due to SAH, leaving no room to reach contralateral approach, although we have a large experience
lamina terminalis safely, but it might be difficult to perform with this approach. The superiorly projecting ICAbifAs
because of the complex head position. occasionally present with a frontal ICH but no blood in the
subarachnoid space.
7.1.4. Clipping
It is safer to dissect the aneurysm dome free under 7.2.2. Head positioning and craniotomy
temporary clipping. Attention should be paid to identify the The head has to be extended little more than for the other
branches and perforators of the ICA, M1, and A1 trunks, ICAbifAs to get higher from the skull base. Rotation and
including the RAH. Large anteriorly projecting ICAbifA lateral tilt are similar as for the other ICAbifAs. The LSO
may initially obstruct the view toward the A1 trunk, craniotomy and drilling of the sphenoid ridge is performed in
preventing temporary clipping of the A1. The pilot clip is a standard fashion.
inserted with the temporary clips on. The temporary clips 7.2.3. Dissection toward the aneurysm
should be short and light so that they do not obstruct the view The dissection starts along the orbital roof toward the
toward the aneurysm base and do not damage the perforators. suprasellar and optic cistern to release CSF. In acute SAH
The aneurysm sac is then opened and eventually reshaped with tight brain, the dissection is continued subfrontally
with bipolar coagulation, and the final clip is inserted. After toward the lamina terminalis, which is opened and further
the temporary clips have been removed, the perforators are CSF is released. Once the brain has been relaxed and there is
rechecked once again. more room, the proximal part of the sylvian fissure is entered.
7.2. Superiorly projecting ICAbifAs Dissection of the sylvian fissure continues along the M1 trunk
toward the ICA, and the ICA trunk is followed to the proximal
7.2.1. Planning direction, and the site for a proximal clip is prepared. The A1
The superiorly or upward projecting ICAbifAs originate trunk is then visualized and also prepared for temporary
from the superior aspect of the ICA bifurcation (Figs. 6A-E clipping. Finally, the base of the aneurysm is dissected free.

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.
664 M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667

7.2.4. Clipping prepared proximal to the ICA bifurcation, and the


A pilot clip is inserted over the aneurysm base under perforator free zones of the A1 and M1 trunks are prepared
temporary clipping. The ideal direction for final clipping for distal temporary clipping.
would be along the M1 trunk to prevent perforator occlusion.
7.3.4. Clipping
However, the pilot clip has to be often inserted perpendicular
Under temporary clipping, the slack dome is dissected
on the bifurcation because the dome is not yet mobile. When
free from all the perforators in its vicinity. The RAH will
inserting the pilot clip, utmost care is needed not to include
probably run in front of the aneurysm, but it may also be
any perforators in the clip. The longer and wider the clip
hidden behind the dome. A pilot clip is inserted avoiding the
blades are, the higher the risk of perforator occlusion. With the
perforators, and the dome is further dissected. Finally, the
pilot clip on, the aneurysm dome can be dissected from its
clip is exchanged for as small and light final clip(s) as
surroundings, and in particular, the back wall has to be
possible. The perforators have to be once again checked by
checked to ensure that no perforators are attached to it. The
manipulating and shifting the clipped aneurysm. Coagula-
final clip, as short as possible to minimize perforator damage,
tion and reshaping of the aneurysm are not recommended
is placed over the neck avoiding the perforators, and other
due to high risk of perforator injury.
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 8. Associated aneurysms
reshaping of the aneurysm due to high risk of perforator injury.
The ICAbifAs are often associated with other IAs. In the
7.3. Posteriorly projecting ICAbifAs Kuopio series, 43% of all ICAbifA patients and 26% of
those with a ruptured ICAbifA had at least 1 additional IA
7.3.1. Planning
(Table 5). Bilateral ICAbifAs were seen in only 6%. Our
The posteriorly or backward projecting ICAbifAs
strategy is usually to clip all the IAs that can be exposed
originate from the superior and posterior aspect of the
through the same craniotomy. It is advisable to clip the
ICA bifurcation (Fig. 5). They are usually the most
ruptured IA first, and if this succeeds without particular
challenging ICAbifAs but fortunately also the least frequent
difficulties, additional IAs can be treated in the same
ones. They are heavily involved with the perforators, posing
session. We do not prefer to clip the associated IAs if the
the greatest risk for perforator injury. The dome is partially
brain is swollen due to acute SAH. In particular, the
obstructed by the ICA so that proper visualization of the
contralateral approach is not advisable if there is lack of
perforators, even if the aneurysm dome is small, is
space in the suprachiasmatic area. We do not recommend
particularly difficult. While clipping, an aneurysm remnant
multiple craniotomies in acute SAH. The technique of
is easily left unnoticed at the dead angle behind the ICA
clipping multiple IAs at different locations is not recom-
trunk. The contralateral approach to the posteriorly project-
mended at early learning curve. The ICAbifA may also be
ing ICAbifAs is not advisable because it is extremely
accompanied by mini blebs, not seen in the preoperative
difficult to get a proper visualization of the perforators that
images, with poorly known natural history. Depending on
envelope major part of the aneurysm dome.
the patient's age and sclerosis of the parent arteries, these
7.3.2. Head positioning and craniotomy blebs may be reduced with bipolar coagulation under the
The head position is similar to that for the superiorly temporary clipping and covered by small piece of cotton to
projecting ICAbifAs, with somewhat less head extension. induce scarring.
The LSO craniotomy is performed in the standard fashion.
It might be necessary to drill the sphenoid ridge more 9. Giant ICAbifAs
profoundly to provide a somewhat more lateral view
toward the ICA bifurcation and, in particular, to its Giant ICAbifAs comprised 7% of all ICAbifAs in the
posterolateral portion. Kuopio series. The dome of a giant ICAbifA is usually at
least partially covered by the frontal lobe and extends also
7.3.3. Dissection toward the aneurysm into the sylvian fissure. Giant ICAbifAs often involve the
The dissection starts in the same way as for the origins of the A1 and the M1. Perforating arteries frequently
superiorly projecting ICAbifAs. After the release of CSF, follow and/or arise from the base region of these IAs, and it
the proximal part of the sylvian fissure is entered, and the may be very difficult, even impossible, to dissect them free.
M1 trunk is followed toward the ICA bifurcation. The large size, distorted anatomy, origins of the perforating
Dissection continues along the ICA trunk with the arteries and other arterial branches directly from the
identification of all the branches originating form it. As aneurysm, calcifications at the base, and intraluminal
with the superiorly projecting ICAbifAs, a small resection thrombus make microneurosurgical management of giant
in the fronto-orbital gyrus may be necessary. Here, the exact ICAbifAs very difficult. Importance of the whole ICA
course of the AChA in relation to the aneurysm dome has to bifurcation complex generally also prevents proximal
be identified. The site for proximal control on the ICA is occlusion or trapping of the aneurysm even if bypass is done.
M. Lehecka et al. / Surgical Neurology 71 (2009) 649–667 665

Comprehensive preoperative imaging by CTA, DSA, and intraluminal thrombus may induce quick rethrombosis, and
MRI is mandatory. The 3D reconstructions of the CTA and therefore, we also advocate early postoperative angiography
DSA data help to show the aneurysm orientation with respect to find surprise occlusions.
to the bony landmarks and to identify calcifications in the For the ICAbifAs, which significantly involve perfora-
aneurysm wall. In addition, DSA provides important tors, direct surgical clipping or trapping may not be
information about the flow dynamics of the ICA bifurcation feasible. Parent vessel sacrifice with distal revascularization
complex. In giant and complex ICAbifAs, we prefer by high-flow bypass may be the only treatment option in
intraoperative DSA to disclose surprise occlusions. these cases [78].
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 10. Fusiform ICAbifAs
as the adjacent arteries. The size of the craniotomy should be
Fusiform ICAbifAs are extremely rare, only 1 of 3005
adapted accordingly. In general, the bone flap needs to be
patients in the Kuopio series (Table 2). They lack a definable
larger and extend more toward the temporal lobe than in the
neck, which could be clipped while preserving the afferent or
standard LSO approach. For adequate visualization of the
efferent arteries (see video ICAbifA—6 Hernesniemi ). The
aneurysm base, a more extensive exposure of the sylvian
parent artery is either circumferentially involved in the
fissure is needed. If the lamina terminalis can be reached
aneurysmal dilatation or it ends in a large thrombosed sac,
over the bulging mass of the aneurysm, it is opened and CSF
and its distal branches arise from the base of the sac [79].
released. The surrounding arteries and perforators need to be
Wrapping, trapping, excision, and bypass surgery can be
identified before clipping attempts. Calcifications in the
considered [64].
aneurysm wall or intraluminal thrombus may prevent
adequate clipping of the giant ICAbifA neck (see video
ICAbifA—4 Hernesniemi). Intraluminal thrombus can be Acknowledgment
removed under temporary clipping, using repeated irrigation
We thank Mr Ville Kärpijoki for excellent technical
with saline, suction, forceps, or an ultrasonic aspirator. The
assistance.
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 Appendix A. Supplementary data
clamp(s) for final clipping may be considered [49], but
utmost care is needed not to severe the surrounding Supplementary data associated with this article can be found,
perforators. Once the dome is decompressed and if the in the online version, at doi:10.1016/j.surneu.2009.01.028.
aneurysm wall is not heavily calcified, it is usually reduced
by bipolar coagulation to allow for final dissection of the References
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