Neurol Med Chir (Tokyo) 47, 153158, 2007

Internal Carotid Artery Bifurcation Aneurysms:

Surgical Experience
Sunil Kumar GUPTA, Virender Kumar KHOSLA, Rajesh CHHABRA,
Sandeep MOHINDRA, Jaipali Rajeev BAPURAJ, Niranjan KHANDELWAL,
Kanchan Kumar MUKHERJEE, Manoj Kumar TEWARI,
Ashis PATHAK, and Suresh Naraian MATHURIYA
Department of Neurosurgery, Postgraduate Institute of Medical Education and Research,
Chandigarh, India

Abstract
Internal carotid artery (ICA) bifurcation aneurysms are relatively uncommon and frequently rupture at
a younger age compared to other intracranial aneurysms. We have treated a total of 999 patients for
intracranial aneurysms, of whom 89 (8.9%) had ICA bifurcation aneurysms, and 42 of the 89 patients
were 30 years of age or younger. The present study analyzed the clinical records of 70 patients with ICA
bifurcation aneurysms treated from mid 1997 to mid 2003. Multiple aneurysms were present in 15
patients. Digital subtraction angiography films were studied in 55 patients to identify vasospasm and
aneurysm projection. The aneurysm projected superiorly in most of these patients (37/55, 67.3%). We
preferred to minimize frontal lobe retraction, so widely opened the sylvian fissure to approach the ICA
bifurcation and aneurysm neck. Elective temporary clipping was employed before the final dissection
and permanent clip application. Vasospasm was present in 24 (43.6%) of 55 patients. Forty-eight
(68.6%) of the 70 patients had good outcome, 14 (20%) had poor outcome, and eight (11.4%) died.
Patients with ICA bifurcation aneurysms tend to bleed at a much younger age compared to those with
other intracranial aneurysms. Wide opening of the sylvian fissure and elective temporary clipping of
the ICA reduces the risk of intraoperative rupture and perforator injury. Mortality was mainly due to
poor clinical grade and intraoperative premature aneurysm rupture.
Key words: subarachnoid hemorrhage,
temporary clipping, surgical outcome

internal carotid artery bifurcation aneurysm,

Introduction

cranial aneurysms from June 1997 to July 2003 had

an aneurysm arising from the bifurcation of the ICA.
Twenty of the 89 patients (22.5%) were aged 20 years
or younger and 42 (47.2%) were aged 30 years or
younger. During the same period, only 12 (3.1%) of
387 patients with anterior communicating artery
(AComA) aneurysms, one (0.4%) of 254 patients with
middle cerebral artery (MCA) aneurysms, and two
(1.8%) of 111 patients with posterior communicating
artery (PComA) aneurysms were aged 20 years or
younger, and 46 (11.9%), 19 (7.4%), and 10 (9.0%),
respectively, of patients with these aneurysms were
aged 30 years or younger.
Complete clinical data were available for 70
patients. Forty (57.1%) of these patients were female,
two of whom were pregnant at the time of presentation. The Hunt and Hess grading scale was used to
assess the neurological status on admission and just
prior to surgery. The Hunt and Hess grade at sur-

Internal carotid artery (ICA) bifurcation aneurysms

account for approximately 5% of all intracranial
aneurysms.1,6,7,15) Various series of ICA bifurcation
aneurysms have been described,116) with the largest
series including 55 patients.16) These aneurysms
tend to occur in relatively younger patients,5,8,16) and
are considered difficult to treat surgically because
of the relationship with the perforators.7,9,15) We
present our experience with 89 patients with ICA
bifurcation aneurysms.

Clinical Materials and Methods

Eighty-nine of 999 patients (8.9%) treated for intraReceived
2007

October 19, 2005;

Accepted

sylvian fissure,

January 29,

153

S. K. Gupta et al.

154

gery was analyzed in this study. Forty-eight (68.6%)

of the 70 patients were in Hunt and Hess grades I
and II, whereas 22 (31.4%) were in grades III and IV.
Fifty-eight (82.9%) of these 70 patients had had one
episode of bleeding before surgery, whereas 10
(14.3%) were admitted after two episodes and two
(2.9%) after three episodes. Computed tomography
was performed in all patients and subarachnoid
hemorrhage (SAH) was graded according to Fisher's
scale. Forty-eight patients (68.6%) were in grades III
and IV.

Surgical Technique
ICA bifurcation aneurysms were routinely clipped
using the standard pterional craniotomy. However,
a few points need emphasis. In approximately half
of the patients, the fundus is pointed superiorly and
may be embedded in the frontal lobe. Frontal lobe
retraction starting with the retractor adjacent to the
carotico-optic space can cause premature rupture of
the fundus or the aneurysm may become avulsed
from the neck. In the beginning of this series, this
happened twice. Therefore, we stress wide splitting
of the sylvian fissure distal to proximal as the initial
and important step to release cerebrospinal fluid
and to expose the ICA bifurcation, which almost
completely avoids the need for frontal lobe retraction. Sylvian fissure splitting exposes the M1 portion
of MCA, which is traced to the ICA bifurcation.
Before dissecting the aneurysm, we also expose the
A1 segment so that we have complete proximal and
distal control.
Elective temporary clipping of the ICA before
final dissection of the aneurysm neck and fundus is
useful and can be helpful in preventing premature
rupture of the aneurysm and for better visualization
of the relationship between the neck and the perforating vessels. Before applying a temporary clip,
we give intravenous mannitol (0.5 gkg1body wt),
phenytoin (500 mg), and dexamethasone (4 mg) as
neuroprotective agents. It is important to avoid
injuring or including the perforators during application of the aneurysm clip. Exposure of the ICA, M1,
and A1 before clip application is very helpful in
avoiding perforator injury. After temporary
clipping, the aneurysm is dissected, especially for
identification and preservation of the perforators
and recurrent artery of Heubner. Most of the perforators are located on the posterior aspect of the
aneurysm. We faced most difficulty in dissection of
the neck of posteriorly oriented aneurysms. Dissection of the recurrent artery of Heubner was difficult
in patients in whom this artery was related to the
neck of the aneurysm and in patients with posterior-

ly oriented aneurysm.

Results
The ICA bifurcation aneurysm was located on the
left in 42 (60%) of the 70 patients, on the right in 26
(37.1%), and bilaterally in two (2.9%). Thirteen
patients had multiple aneurysms including other
aneurysms located on the MCA (8 cases), PComA (4),
AComA (3), anterior choroidal artery (3), carotidophthalmic artery (1), and basilar top (1). Two of
these patients presented with SAH from another
aneurysm, and the ICA bifurcation aneurysm was
unruptured.
Independent review of the digital subtraction
angiograms was possible in 55 patients. The size of
the aneurysm was 10 mm in 38 cases (69.1%),
1120 mm in 16 (29.1%), and 20 mm in one (1.8%).
The aneurysm projected superiorly in 37 cases
(67.3%), anteriorly in 11 (20.0%), and posteriorly in
seven (12.7%). The superiorly projecting aneurysms,
pointed directly superiorly in 23 cases (41.8%), tilted
medially towards the A1 in 11 (20.0%), and tilted
laterally towards the M1 in three (5.5%). The recurrent artery of Heubner was most often located on the
posterior aspect of the aneurysm, and was relatively
easier to separate from the aneurysm neck if the
aneurysm was tilted towards the M1.
Recurrent artery of Heubner was generally
present as one of the many perforators related to the
aneurysm. Among 20 patients, recurrent artery of
Heubner was specifically documented as arising
from the A1-AComA junction in 16 patients, from
the distal A1 segment in three, and from the proximal A2 segment in one (Fig. 1). The recurrent artery
of Heubner terminated posterior to the fundus of the
aneurysm in seven patients, posterior to the
aneurysm neck in five, and on the superior surface
of the aneurysm in five, and passed over the medial
border of the aneurysm fundus in three (Fig. 2).
Vasospasm occurred in 24 (43.6%) of 55 patients
examined. Twenty-one (30.0%) of the 70 patients
were operated within 72 hours of the last ictus, four
at 24 hours, seven at 2448 hours, and 10 at
4872 hours, whereas 49 (70.0%) were operated
more than 72 hours after the last bleeding episode,
22 at 47 days and 27 at 7 days, mainly because of
late referral to our hospital.
Forty-eight (68.6%) of the 70 patients had good
outcome (Glasgow Outcome Scale [GOS] score 5 or
4) whereas 14 (20.0%) patients had poor outcome
(GOS score 3 or 2). Eight (11.4%) patients died
(Table 1). Three (6.3%) died of the 48 patients with
Hunt and Hess grades I and II, two (13.3%) of the 15
with grade III, and three (42.9%) of the seven with

Neurol Med Chir (Tokyo) 47, April, 2007

ICA Bifurcation Aneurysms

grade IV (Table 1). Death could be attributed to poor
clinical grade (grade IV) in three patients, with the
added complication of septicemia and chest infection in one and MCA infarct in another. Death was
due to premature intraoperative rupture before any
dissection was done in two patients, possibly due to
MCA infarct in two, and the cause could not be
ascertained in one.
Further analysis of the patients who died observed
that all deaths occurred during the years 19972000,
and there were no deaths after 2000. Complete

155

clinical data was available for 40 patients from mid

1997 to 2000, whereas clinical details were available
for 30 patients from 2000 to mid 2003. Therefore,
there was definitely an improvement with experience. We believe that this was largely due to the
change in strategy from retracting the frontal lobe to
working along the sylvian fissure towards the ICA
and aneurysm neck.

Discussion
A total of 822 patients with ICA bifurcation
aneurysms have been reported in 43 series from
1933 to 2000, of whom 507 were treated surgically.7)
The reported incidence of ICA bifurcation
aneurysms varies from 5% to 10%.5,7,12,16) In our
series, the incidence was 8.9% of all patients operated for intracranial aneurysms. The most striking
clinical feature of ICA bifurcation aneurysms is the

Fig. 2
Fig. 1

Table 1

Line diagrams showing the variations in the

origin of recurrent artery of Heubner: A1
segment to anterior communicating artery
junction (A, n 16), distal A1 segment (B,
n 3), and proximal A2 segment (C, n 1).

Line diagrams depicting the various

relationships of the recurrent artery of
Heubner with the aneurysm: termination
posterior to the aneurysm fundus (A, n 7),
on the superior surface of the aneurysm (B,
n 5), and posterior to the aneurysm neck
(C, n 5), and passing over the medial
border of the aneurysm fundus (D, n 3).

Surgical outcome and preoperative clinical grade

Glasgow Outcome Scale

Hunt and Hess grade

before surgery

I
II
III
IV
Total

Good

Moderate disability,
independent

Severe disability,
dependent

Vegetative

Dead

16
32
15
7

10
18
6
0

3
10
1
0

1
2
4
2

0
1
2
2

2
1
2
3

70

34 (48.6%)

14 (20.0%)

9 (12.9%)

5 (7.1%)

8 (11.4%)

Neurol Med Chir (Tokyo) 47, April, 2007

156

S. K. Gupta et al.

younger age of the patients at the time of rupture,

compared to aneurysms at other locations. Patients
with rupture of aneurysms at other locations (i.e.
AComA, MCA, and PComA) were aged between
40 and 60 years. The mean age of patients with
ruptured ICA bifurcation aneurysms was reported
as 41 years7) and 48.3 years,2) but was significantly
lower at 31.5 years in our patients. In a series of 1012
patients, only 41 patients were aged less than 20
years.16) Among the 55 patients with ICA bifurcation
aneurysms, 32 were aged less than 30 years and 16
patients were under the age of 20 years. Almost half
(40 of 89) of our patients were 30 years of age or
younger, and 20 were 20 years of age or younger.
The youngest patient in our series was a 9-year-old
girl.
The incidence of multiple aneurysms ranges from
19% to 22%.48) In contrast, multiple aneurysms
occur in 1547% of patients with ICA bifurcation
aneurysm (mean 30%).5,7,16) In our series, 15 (21.4%)
of 70 patients had additional aneurysms, two of
whom had bilateral ICA bifurcation aneurysms. The
presence of male or female predominance varies
with the aneurysm site. A series of 1104 cases of
ICA aneurysms showed the highest female predominance (1:7.3) in patients with intracavernous
aneurysm, and lowest (1:1.6) in patients with ICA
bifurcation aneurysms.6) Previous studies have
reported male predominance,2,3,11,16) no predominance,7) and female predominance.4) In our series,
40 of 70 patients (57.1%) were female, thus supporting a slight female predominance (1.33:1).
The aneurysm fundus may project in the superior,
posterior, or inferior directions.16) The aneurysm is
usually located more on the MCA or anterior
cerebral artery, although no specific relationship to
the size of the arteries was recorded.16) The superior
projection has been most commonly reported
(54.4%), followed by posterior projection (40.4%),
and rarely anterior projection (5.3%).2,3,5,1113)
However, one series of 25 cases contained 12 superior, seven anterior, and six posterior projection
aneurysms.7) In our series, most aneurysms (37/55,
67.3%) had superior projection, which we feel is important in planning surgical strategy.
Our surgical strategy requires opening of the
sylvian fissure widely from distal to proximal, to
identify the MCA and work towards the ICA
bifurcation. We believe that this is the most
important step to avoid intraoperative rupture of the
aneurysm. We experienced aneurysm rupture secondary to frontal lobe retraction in the early part of
the series, and since then have performed wide
opening of the sylvian fissure rather than frontal
lobe retraction to reach the ICA and the aneurysm

neck.
Elective temporary clipping of the ICA prior to the
final dissection of the neck and placement of the
aneurysm clip is a useful strategy which makes
dissection of the aneurysm much safer and easier,
and allows better identification of the perforators
before final placement of the clip. With experience,
we have found that perforator injury is rather
uncommon with this technique and ICA bifurcation
aneurysms are usually easier to clip. Elective temporary clipping is much better than emergency temporary clipping, which may be needed in the event
of intraoperative aneurysm rupture, as the risk of
perforator injury is lower. Temporary clipping was
previously used in two of nine cases,13) 28 of 29
cases,3) three of 18 cases,4) and eight of 25 cases.7)
Temporary clipping must be utilized in difficult
cases8) but possibly there is no need to place
temporary clips on the parent vessel.11) Induced
hypotension is useful even for large aneurysms with
no need for temporary clipping.12) We did not use
intraoperative hypotension to facilitate clipping in
this series.
Mortality rate in some of the older series was high,
ranging up to 30%,10) but the introduction of
microsurgery has resulted in remarkably low rates
ranging from 0% to 12%.2,8,9,11,1416) The most
important factor affecting outcome is the clinical
grade of the patient prior to surgery. In our series,
the overall mortality rate was 11.4%. Patients with
good preoperative clinical grade had mortality rate
of 6.3%, whereas patients with poor clinical grade
had higher mortality. Vasospasm was present in less
than half of the patients and there were no statistically significant correlations between the presence
or absence of spasm, preoperative clinical grade,
and postoperative outcome. The outcome in patients
with ICA bifurcation aneurysm is related only to the
clinical grade.16) However, vasospasm is elsewhere
considered to be the main causative factor of unfavorable outcome.2,3,8,9,11,12) Unfavorable outcome
was due to primary brain damage (4/25), vasospasm
(2/25), and pneumonia (1/25) in one series.7)
Mortality in the present series was caused by poor
preoperative grade, intraoperative premature
aneurysm rupture, chest infection, and postoperative MCA infarct.
We recommend wide opening of the sylvian
fissure from distal to proximal, to identify the MCA
and approach the ICA bifurcation. Temporary
clipping of the ICA prior to final dissection of the
aneurysm neck and clip placement is also useful.

Neurol Med Chir (Tokyo) 47, April, 2007

ICA Bifurcation Aneurysms

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Address reprint requests to: Sunil Kumar Gupta, M.D.,

Additional Professor, Department of Neurosurgery,
PGIMER, Chandigarh160 012, India.
e-mail: drguptaskyahoo.com

Commentary
The authors are congratulated on a careful analysis of
outcome of a large surgical series of internal carotid
bifurcation aneurysms. Their wise conclusion relates
to the importance of wide opening of the sylvian
fissure, and elective temporary clipping to reduce the
risks of aneurysm rupture and perforator injury. They
share sobering complication rates, with 31.4% of
cases resulting in severe disability, vegetative state, or
death. Most complications in high grade patients
occurred from vasospasm or as direct effect of poor
initial clinical grade. But there were 7 of 42 cases in
good clinical grade (I or II), or 14.5%, which also
resulted in such poor outcome. These complications
among good grade patients mostly resulted from
premature rupture during surgery and postoperative
infarcts.
With regard to prevention of premature rupture,
the importance of modifying surgical exposure cannot
be overemphasized. Bony exposure must include
frontal base exposure absolutely flush with the floor
of the anterior cranial fossa, and radical resection of
the sphenoid ridge as far medially as the superior
orbital fissure (we use an orbitozygomatic exposure
for giant or particularly ``high'' lesions). The head is
initially elevated, and basal cisterns are not emptied
early. The frontal lobe is not retracted at all, and in
fact not even allowed to fall by gravity, until the
sylvian fissure is widely split. This is accomplished
from lateral to medial by manipulation of the temporal lobe and with no manipulation of the frontal
lobe until after the middle cerebral and internal
carotid arteries are exposed and control is established. Only then, and with arachnoidal tethers
released, is the frontal lobe gently mobilized and the
head of the bed lowered, to allow gravity to help us as
we complete the exposure of the neck and the anterior
cerebral artery, all the while ensuring that each move
does not stretch the aneurysm dome (which is often
buried into the frontal lobe). Except in a minority of

158

S. K. Gupta et al.

cases where the dome is fully mobilizable in the

subarachnoid space, temporary clips are used, not
only on the internal carotid artery, but also on the
middle cerebral artery. Temporary clipping of the
anterior cerebral artery is rarely needed, as the
aneurysm will soften enough for clear manipulation
to define and sweep away the perforators on the
posterior wall and behind the neck. A lateral to medial
view through the sylvian fissure is most useful for
this. The softening also allows safer clip placement.
With these steps, we have been fortunate (and lucky)
not to encounter premature rupture during exposure
of these lesions in recent years.
Sparing the perforators is the next essential step.
These occur in three groups, and all three must be
looked for and avoided. The first group of perforators
arises from the anterior choroidal distal segment of
the internal carotid artery, behind the aneurysm neck,
and they course superiorly, medially, or laterally. A
second group of perforators may include one or more
recurrent arteries coursing from the anterior cerebral
artery in a medial to lateral direction (i.e. Heubner
artery). And a third group of perforators may include
one or more arteries coursing from the M1 segment of
middle cerebral artery medially. These can usually be
easily swept away, so they are not fettered by clip
application. The lesson here is to look and see all the
way behind the neck and dome.
The final task is a clipping strategy to preserve and
verify patency of the middle cerebral and anterior
cerebral artery orifices, while avoiding residual ``dog

ears'' at the neck. We have been using short tandem

clips (including a custom made ultra-short fenestrated
clip) more and more for precise reconstruction at such
bifurcations. Intraoperative micro-Doppler insonation is essential in every case, and intraoperative
angiography in more difficult cases, to ensure patency
of these critical parent vessels.
These technical challenges and outcome caveats
beg the question of whether endovascular treatment
can deliver a better outcome for these lesions.
Aneurysms at this location, especially when medium
or large sized, may often exhibit a broad neck, incorporating the origin of the middle or anterior cerebral
arteries. These features and the direct water hammer
effect of flow at the carotid summit, often make their
endovascular coiling suboptimal or less durable.
Newer techniques incorporating a small stent may
help in this regard, but morbidity rates and technical
feasibility have not been systematically reported. And
the risk of early or late parent artery compromise by
stent complications or stenosis can be devastating and
most unforgiving in this location. The article by Gupta
et al. defines a reasonable surgical bar to meet or
exceed when assessing these emerging modalities.
Issam A. AWAD, M.D., M.Sc., F.A.C.S., M.A. (Hon.)
Evanston Northwestern Healthcare
Department of Neurological Surgery
Northwestern University
Feinberg School of Medicine
Evanston, Illinois, U.S.A.

Neurol Med Chir (Tokyo) 47, April, 2007