Bangladesh Journal of Neuroscience 2012; Vol. 28 (1) : 29-37
Intracranial Aneurysms: Acute VS Delayed Surgery - An
Analysis of 52 Cases
SHAMSUL ALAM1, ASIFUR RAHMAN1, AN WAKIL UDDIN1, KM TARIKUL ISLAM1,
MOSIUR RAHMAN MOJUMDER2 , MAHFUZUR RAHMAN2, ANIS AHMED2, ASM ABU OBAIDA2,
SAIF UL HAQUE2, MOHAMMAD NAJIM UDDIN2
Abstract:
Background: Aneurysm surgery is increasing day by day in our country but the exact
timing of surgery is still controversial. Objectives: The aim of this study was to determine
the results of early and late surgery for aneurismal subarachnoid haemorrhage. The
aim of microneurosurgical management of an aneurysm is the total occlusion of the
aneurysm sac by clipping at the neck of aneurysm with preservation of flow in the parent
artery and preservation of all its perforating arteries with minimal or no brain retraction.
Methods: There were 52 patients included in this study among them 3 patients expired
soon after the admission before surgery could take place. Hence 49 patients underwent
clip surgery from July 2005 to May 2012 for 52 aneurysms because 3 patients harboured
multiple aneurysms. Patient’s history, clinical findings, Hunt & Hess grading, Fisher
grading of CT scan, preoperative & postoperative CT angiography, postoperative outcome
were collected and analyzed. Results: Most of the clipping (57.14%) were done in
intermediate stage (4th to 10th days), because patients usually referred from peripheral
hospital on 2nd or 3rd day after the acute SAH Those who was admitted early and H&H
status good, was fit to do early surgery (within 3rd day), (28.57%). Overall outcome was
assessed at 3 months after SAH using the Glasgow Outcome Scale. Good outcome
were observed in 40 cases among them 22 cases (42.3%) were able to return premorbid
activities. Total mortality in this series were 10 cases (19.23%) which includes
preoperative death while waiting for clipping -3 cases and postoperative death- 7
cases( 14.2%). Conclusion: There is no reason to postpone clipping surgery in patients
who are eligible for surgery at day 5. Surgery after day 10 is associated with worse
outcome. Although these studies is having high rate of mortality which can be
progressively minimize by our continuous improvement of surgical skills and
postoperative critical care management of aneurysm patients.
Key word: aneurysm, craniotomy, clipping.
Introduction:
Aneurysms resemble bubbles or focal dilation of
arteries that occur at weak points of the artery wall
(figure-1). There are many factors for its formation.
These factors include genetic predisposition, the
anatomy of the artery and its branches, ‘wear-andtear’ on the wall of the arteries due to blood flow,
artery disease and cigarette smoking1. Aneurysms
are the most common at circle of Willis in the central
skull base. Approximately 80% of aneurysms arises
from anterior circulation of the brain, while 20%
form posterior circulation of the brain1.2.
It is uncommon to diagnose an aneurysm before it
has ruptured and most people with aneurysms are
unaware that they have an aneurysm until it bursts.
Overall 3.6-6% of normal population has aneurysm,
among them 1.4-1.9 % rupture in a year. Women
have more tendencies to rupture. There is seasonal
variation of rupture3.
1. Assistant Professor, Department of Neurosurgery, Bangabandhu Sheikh Mujib Medical University, Dhaka.
2. Resident, Department of Neurosurgery, Bangabandhu Sheikh Mujib Medical University, Dhaka.
It is known that the majority of aneurysms that have
ruptured are less than 10 mm in size3.4. Over the
next 5 years after diagnosis an average aneurysm
between 2 and 6 mm in size has a risk of bleeding
between 1 and 2%, an aneurysm between 7 and 9
mm size has a five year risk of bleeding of 6%, an
aneurysm between 10 and 24 mm in size has a
five year risk of bleeding of 11% and larger
aneurysms have a 28% chance of bleeding3.4.
The history of intracranial aneurysm surgery is not
a long one. The first direct operation on an
intracranial aneurysm was performed by Norman
Dott, who wrapped a ruptured aneurysm in 1933,
and the first clipping of an aneurysm was performed
by Walter Dandy in 19385.6. The results of surgery
improved dramatically when the operating
microscope was introduced in the 1960s and a
subsequent improvement followed the use of the
calcium antagonist nimodipine and the
maintenance of a high fluid intake to lessen the
risk of delayed cerebral ischemia7. For many years
clipping for the aneurysm was regarded as the
definitive mode of treatment, but the development
of the GDC coil in 1990 allowed an alternative
approach that avoided the hazards of open
surgery7.
After an aneurismal subarachnoid haemorrhage,
there are two major sources of morbidity and
mortality: rebleeding and delayed ischemia
secondary to cerebral vasospasm. The incidence
of rebleeding is greatest immediately after the initial
haemorrhage, and the incidence of vasospasm is
highest between the 5th and 9th days after the
ictus8. It thus seems logical to proceed with early
surgery, such an approach is certainly the best
means for eliminating rebleeding as a source of
morbidity and mortality. Early surgery also facilitates
the management of cerebral vasospasm by volume
expansion and induced hypertension manoeuvres
that are quite risky in the patient with an untreated
aneurysm8.
The anterior communicating artery (AcomA) is a
recognized site of aneurysm predilection
accounting for more than one fourth of all cerebral
aneurysms in several large studies9. Because of
30
Fig.-1: Showing various dimensions of an
aneurysm
the complexity and diversity of the geometry and
flow conditions in the AcomA, it is not surprising
that aneurysms of the AcomA are considered the
most complex of the anterior circulation. It is widely
believed that the initiation, growth, and, ultimately
rupture of cerebral aneurysms are related to the
interaction between hemodynamic forces with the
arterial wall biology, resulting in a localized
weakening of the wall. Aneurysms of the AcomA
complex are more likely to have asymmetric A1
segments and furthermore, to have exclusive filling
angiographically from A1 segment in up to 78%
cases.9
Posterior communicating artery (PCOM)
aneurysms are another most common aneurysms
encountered by neurosurgeons and neurointerventional radiologists and are the second most
common aneurysms overall (25% of all aneurysms)
representing 50% of all internal carotid artery (ICA)
aneurysms10 . Not only these aneurysms can
present with a typical subarachnoid haemorrhage,
but also they can present with an isolated
oculomotor nerve palsy (OMNP) or a non-traumatic
subdural hematoma (SDH).
Jane et al, evaluated the risk of rehaemorrhage in
ruptured ACOM and PCOM aneurysm, finding a
50% risk of rerupture within the initial six months
followed by 3.5% per year thereafter11.
The surgical treatment of basilar tip aneurysms
remains one of the most difficult tasks in
neurosurgery because the view is obscured due
to the depth of the aneurysm, overlapping
neurovascular and bony structures, and the
proximity of perforators12.
Despite the many studies about timing for surgery
in subarachnoid haemorrhage (SAH), the optimum
time is still in debate. The aim of this study was to
determine the results of early and late surgery for
aneurysmal subarachnoid haemorrhage. The
proponents of early surgery focused on reduction
of the devastating effects of aneurysmal re-bleeding
within the first 2 weeks and its high mortality. On
the other hand, some authors believe that delayed
surgery may be better choice, because operating
on the acutely injured brain may be associated
with high risk for surgical morbidity and mortality13.
Some studies advocates surgery neither early nor
late, and indicate that the intermediate period in 4
to 10 days after the SAH is a risky time for surgery,
because during this period the risk for cerebral
vasospasm and ischemia may be very high14.
Unlike the authors, it is our belief that early aneurysm
surgery is a technically more challenging procedure
than delayed surgery. Despite the use of osmotic
agents, hyperventilation, and cerebrospinal fluid
drainage, it is our opinion that the brain is more
friable and difficult to retract safely.
However, Shabepour et al. study in Iran had some
results different from most previous studies; they
evaluated 110 aneurysmal SAH and reported that
the complications of late surgeries were
significantly lower than early surgeries; the
complication rate in surgeries performed during
first 3 days after SAH was 66.7%. This rate was
54.57% for surgeries in 3 to 14 days after SAH,
and 22.9% for surgeries after 14th days15.
Fig.-2: CT scan shows of SAH, Fisher grade 2.
The aim of microneurosurgical management of an
aneurysm is the total occlusion of the aneurysm
sac by clipping at the neck of aneurysm with
preservation of flow in the parent artery and
preservation of all its perforating arteries with
minimal or no brain retraction.
Methods:
There were 52 patients included in this study among
them 3 patients expired soon after the admission
before surgery could take place. Hence 49 patients
underwent clip surgery from July 2005 to May 2012
for 52 aneurysms because 3 patients harbored
multiple aneurysms. Patients’ history, clinical
findings, Hunt & Hess grading, Fisher grading of
CT scan (figure-2), preoperative & postoperative
CT angiography, postoperative outcome were
collected and analyzed.
About 90% of aneurysms were accessible via a
standard frontotemporal (pterional) craniotomy
centered over the pterion. Only occasional cases,
aneurysms of the distal anterior cerebral artery
and the lower vertebrobasilar trunk, require different
surgical approaches. The risk of intraoperative
rupture of the aneurysm, which occurs in 5-10%
of cases, can be minimized by induction of
hypotension. This seems a safe measure provided
that the anaesthetist ensures maintenance of a high
blood volume. We preferred not to apply temporary
clips to the main artery proximal to the aneurysm
because it was associated with a high incidence
of ischemic cerebral damage. Temporary clipping
was certainly not tolerated if the blood pressure is
lowered at the same time.
Surgical steps
Acom aneurysm: Pterional craniotomy is
commonly done for this. We prefer to approach
from right side however sometimes it needed to
approach from left side when. Left A1 is dominant
and Ipsilateral and contralateral A2 is well visualized
from left side. We prefer 5-10 degree rotation to
the contralateral side to keep the figure of H in
vertical position. Wide sylvian fissure dissection
was done for gentle retraction of frontal lobe.
Anterior interhemispheric fissure was dissected to
avoid gyrus rectus resection (figure-3A,3B,3C).
31
A
B
C
Figure-3: CT angiogram shows ACOM aneurysm (A), Peroperative clipping of ACOM aneurysm (B) &
Post clip angiogram shows no residual aneurysm (C).
Pcom aneurysm: Pterional craniotomy with
rotation 60-75 degree to contralateral side for
posteriorly directing aneurysm which allows the
aneurysm to be seen in profile with carotid artery.
The oculomotor nerve should be identified and
protected. It is not necessary to expose the
aneurysm dome. When the inferior and superior
aspect of aneurysm has been identified and
adjacent arteries made free, then the aneurysm
can be safely clipped.
MCA aneurysm: Pterional approach with turning
the patient head 45 degrees to contralateral side means the operative pathway will be almost vertically
downward along the sphenoid ridge. This reduces
the need for retraction of temporal lobe , and often
only needs the frontal lobe to be retracted. The
head is also extended to allow the frontal lobe to
fall. Finally the rotated, extended head is elevated
upward to facilitate venous return.
Basilar top aneurysm:
Pterional craniotomy with head is positioned in
a Mayfield head holder with the head elevated
above the shoulder level and 20 dergree rotation
to the contralateral side away from the operative
side. The head is extended until the maxillary
eminence is highest point in the field. A pterional
craniotomy is then performed followed by drilling
of sphenoid ridge and orbital roof until a flat
surface is achieved so that straight trajectory to
the proximal carotid can be visualized along the
skull base.
For preexisting hydrocephalus or in case of brain
swelling during surgery we are in need of brain
relaxation. This can be done by a ventricular
catheter placed in “paine’s point”. This is done by
aiming perpendicularly to the triangle 2.5 cm back
along the sylvian fissure and 2.5 cm superiorly.
A
B
Figure 4: CT angiogram shows left MCA aneurysm (A) & Post-clip angiogram shows no residual
aneurysm (B).
32
Results:
The mean age group of our study was 45.7 years.
Age varies from 16- 70 years. Male: female ratio
was 1:08. In our study male are commoner then
female.
Hunt and Hess grades at admission are
summarized in Table I. Thirty seven patients
(71.2%) were classified as Grade I-II, Twelve
patients (23.0%) as Grade III-IV. 3 patients (5.7%)
as Grade V.
Table-I
Distribution of Hunt & Hess Grading: (n=52)
Hunt & Hess Grading
No. of cases
I – II
37 (71.215%)
III-IV
12 (23.07%)
V
3 (5.76%)
The subarachnoid clot thickness -Fisher grading
at admission were summarized in Table-II. 84.4%
of cases were in grade I-II. 4 cases(7.6%) were
in grade III-IV. Only 4 cases (7.6%) were grade V.
Table-II
Distribution of Fisher grade of
Aneurysms: (n=52)
Fisher Grading
No. of cases
I – II
44 (84.61%)
III-IV
4 (7.69%)
V
4 (7.69%)
Cerebral CT angiography was performed at
admission in all patients (angiography was
performed within 48 hours of haemorrhage onset
in most of the cases). The location and size of
the ruptured aneurysm were obtained from a
review of angiographic images. Commonest
aneurysm found in ACOM location which was
42.30%. Next commoner the PCOM which
constitute 26.92% and MCA aneurysms were
9.61% . Basilar top aneurysms were found only
in 4 cases ( 7.6% ) (Table-III). The aneurysm
was single in 92.9% and multiple aneurysms were
found in 3 cases (5.76%).
Table-III
Distribution of CT angiographic findings of
Location of Aneurysms:(n=52).
Location of Aneurysms
No. of aneurysms
ACOM aneurysm
PCOM aneurysm
MCA aneurysm
ICA aneurysm
DACA aneurysm
Basilar top aneurysm
Paraclinoid aneurysm
Vertibrobasilar junctional aneurysm
Total
22 (42.30%)
14 (26.92%)
5 (9.61%)
5 (9.61%)
2 (3.84%)
4 (7.69%)
2(1.92%)
1(1.92%)
52 (100%)
Aneurysm size was categorized in three groups.
Small sizes were between 4-10 mm - constitute
the commonest size which were 84.6%. Large
sizes were between 11-25 mm constitute 11.5%
and >25 mm were giant aneurysm which was only2
cases(Table IV).
Table-IV
Distribution of Size of Aneurysms, (n=52)
Size of Aneurysms
4mm – 10mm
11mm – 25mm
<25mm
Total
No. of Aneurysms
44 (84.61%)
6 (11.53%)
2 (3.84%)
52
Pterional craniotomy (91.8%) was the most
common approach for most of the aneurysm both
for almost all anterior and some posterior circulation
aneurysm. Contralateral pterional approach were
done in 3 cases(6.12%). For vertebrobasilar
junction retrosigmoid suboccipital craniectomy was
choiced. For DACA aneurysm anterior
interhemispheric approach was chosed.(Table-V).
Table-V
Distribution of Name of Surgery (n=49)
Name of Surgery
No. of cases
Pterional Crainotomy
45 (91.83%)
Orbitopterional Crainotomy
1 (2.04%)
Contralateral Pterional Crainotomy
3 (6.12%)
Retrosigmoid suboccipital approach 1(2.04%)
Total
49 (100%)
Most of the surgery(57.14%) were done in
intermediate stage(4th to 10th days), because
33
patients usually referred from peripheral hospital
on 2nd or 3rd days after the acute SAH. Those who
was admitted early and H&H status good , was fit
to do early surgery (within 3rd day) (28.57%).
Those who were poor H&H grade at admission and
or CT angiogram reveled sign of vasospasm and
those having medical co-morbidity such as asthma,
coronary ischemia, were not able to do early or
intermediate surgery hence they were selected
for late surgery(after 11th day onward)(table-VI).
Two patients who died from rebleeding while waiting
for surgery although they were fit for surgery at
anytime. Another one patients died from severe
vasospasm so soon after admission that surgery
could not have been performed.
Table-VI
Distribution of Day of Aneurysm Surgery (n=49)
Day of Aneurysm Surgery
1st
No. of aneurysms
3rd
day –
day
th
th
4 – 10 day
>11th day
Total
14 (28.57%)
28 (57.14%)
7 (14.28%)
49 (100%)
Overall outcome was assessed at 3 months after SAH
using the Glasgow Outcome Scale. Good outcome
were observed in 40 cases among them 22 cases
(42.3%) were able to return premorbid activities. Poor
outcome was defined by the Glasgow Outcome Scale
criteria of death, vegetative state, or severe disability.
Total mortality in this series were 10 cases (19.23%)
which includes preoperative death while waiting for
clipping -3 cases and postoperative death -7 cases(
14.2%) (Table -VII).
Table-VII
Distribution of Glasgow outcome scale (N=52)
Good outcome
No. of cases
1. Return to premorbid occupation
22(42.30%)
2. Neurologically normal, not
returned to premorbid occupation
10(19.23%)
3. Independent, mild neurological deficit
5(9.61%)
Poor outcome
4. Dependent, significant deficit
5(9.61%)
5. Dead(preop-3cases + (14.2%)
postop-7cases
10(19.23%)
Total
52 (100%)
34
Commonest complication of aneurysm sugery were
rerupture during dissection of aneurysm sac which
occurred 7.6% cases. Incompletely clipped
aneurysm also reruptured in postoperative period
which occurred 3.8% cases. Postoperative severe
hypotension developed in 5.7% cases. Most
common causes of postoperative mortality in our
series were from hypotension and improper
management of vasospasm. Rerupture from
incompletely clipped aneurysm were accounted 2
cases which lead to death(table-8). Postoperative
vasospasm & limb weakness were another
common problem for which we need to manage by
ionotrophic agent like dopamine, adrenaline &
dobutamine. Subdural hematoma , meningitis , and
acute and late hydrocephalus were some minor
complications (Table- VIII).
Table-VIII
Distribution of Complications of
Aneurysm (n=52)
Complication
No. of cases
Re-rupture while waiting
2 (3.84%)
Preop severe vasospasm
1(1.92%)
Intraoperative rupture
4 (7.69%)
Post operative rupture
2 (3.84%)
Post operative hypotension
3 (5.76%)
Pre operative vasospasm
6 (11.53%)
Newly developed Post operative
5 (9.61%)
vasospasm & hemiplegia
Post operative subdural haematoma 2 (3.84%)
Meningitis
5 (9.61%)
Hydrocepalus
3 (5.76%)
Tension pneumocephalus
1(1.92%)
VP shunt
3 (5.76%)
No complications
15(28.84%)
Total
52(100%)
Discussion:
Pterional craniotomy was the most common
approach for both anterior and posterior circulation
aneurysm 16 . However some author choose
orbitopterional craniotomy in case of ACOM
aneurysm in acute setting. In one study overall
outcomes at discharge using the Glasgow outcome
scale of those who underwent pterional craniotomy
were good in 52 (69.4%) patients, fair in 13
(17.3%), and poor in 10 (13.3%) among 75 cases
of ACOM aneurysm. At last follow-up after 6 months
of surgery, outcomes were good in 63 (84%)
patients, fair in 6 (8%), and poor in 6 (8%).
Disability included mild in 10%, partial in 18.8%,
moderate in 8.6%, moderately severe in 1.4%,
severe in 2.9%, extremely severe in 2.9%, and
vegetative state in 1.4%. Overall 74% of patients
returned to work after 4 months, 83% of previously
unemployed patients returned to baseline, and 25%
were disabled17. In this study good outcome were
observed in 40 cases among them 22 cases
(42.3%) were able to return premorbid activities.
Poor outcome were observed in 15 cases among
them 7 cases were died following surgery(14.2%)
Here our postoperative mortality was quite high
(14.2%), this was probably from interaction of
many factors –such as patient factor-delay
admission, hesitation regarding giving consent for
operation in good H&H status, postoperative poor
nursing management , and surgeons skill.
ACOM aneurysms) amongst anterior circulation
aneurysms20 .
A strong correlation was found between
rehaemorrhage and residual aneurysm. Risk of
rehaemorrhage increased from 1.1% in completely
occluded aneurysm to 17.6% in a partially treated
aneurysm where residual filling of the dome was
left untreated. Also the median time to rerupture
was only three days19. In our series 2 cases
developed reruptured in early postoperative period
among 49 cases of operatively treated aneurysm
(table-VIII)
Aneurysm surgery are increasing day by day,
probably because of improvement of motivation of
the patient party, availability of investigation and
availability of aneurysm clip of various size and
shape in our country.(Diagram-1)
Samson et al. reported that the outcome and
complications of early surgery on first 8 days after
SAH were not different from late surgery in 9 to
31days after SAH, but ischemic events after early
surgery were significantly higher18.
Temporary clipping and projection of the aneurysm
did not affect the outcome. Causative factors of
unfavorable outcomes were primary brain damage
by haemorrhage in cases of small and large
aneurysms and perforator damage in the case of
giant aneurysm. Poor clinical H&H grade and
vasospasm are the causative factors of poor
outcome in patients with ruptured aneurysm. The
poor outcome could also have been correlated with
poor clinical condition at admission, early
rebleeding , or early deterioration from other
causes19.
Once the neck of the aneurysm was adequately
exposed, then we must pay significant attention to
preservation of the parent artery, perforators
without significant manipulation of the fundus19.
Leipzig et al, reviewed a large series of aneurysm
clipping looking for risk factors of intraoperative
rupture. PCOM aneurysms had the second highest
rate of intra-operative rupture (second only to
Diagram-I Bar diagram of aneurysm cases in
year. (n=52).
There are 3 possible explanations for the observed
better outcomes among SAH patients treated within
72 hours of admission: (1) the death and disability
associated with rebleeding is reduced; (2) the death
and disability related to cerebral vasospasm is
reduced because more intensive measures can
be undertaken with secured aneurysms; and (3)
early treatment is a marker of higher performance
on several quality care parameters 20.
The international cooperative study on the timing
of aneurysm surgery recruited 3521 patients with
aneurusmal SAH. There was no difference in good
35
outcome defined by Glasgow outcome scale at 6
months in early (0-3day ) and delayed (11-14 day)
surgery group but lower rate were observed in
intermediate (7-10 day) surgery group. The rate
of rebleeding in early surgery group 5.7% in
compared with 13.9% delayed surgery group21. A
subgroup analysis on north American
population(772 patients ) demonstrates high rate
of good outcome in early vs delayed group (70.9%61.7%) respectively even though there is no
mortality. A recent data reevaluate the definition of
early treatment (0-2 days vs 0-3 days) proposed
by international cooperative study trail. A major
benefit of early surgery lies in the decreasing
frequency of rebleeds that occurs in the interim
period before aneurysm treatment is performed22.
In our study the hospital stay in early surgery group
was significantly lower than late group. This finding
is concordant with Ross et al. 23 and Bolander et
al. studies24.
Conclusion:
In conclusion, this study revealed that most of the
aneurysm surgery were done between 4th to 10th
days of post acute SAH, which reflects that timing
of surgery should be individualized for each patient
based on clinical situation such as age, H&H
Grading, Fisher Grading, size and site of
aneurysm, presence or absence of vasospasm and
other medical comorbid factors. There is no reason
to postpone clipping surgery in patients who are
eligible for surgery at day 5. Surgery after day 10
is associated with worse outcome. Although this
study is having high rate of mortality which can be
progressively minimize by our continuous
improvement of surgical skills and postoperative
critical care management of aneurysm patients.
References:
1. McDougall CG, Spetzler RF, Zabramski JM,
Partovi S, Hills NK, Nakaji P, et al. The Barrow
Ruptured Aneurysm Trial . J Neurosurg .
2012;116:135–44
2.
36
Juvela S, Porras M, Poussa K. Natural history
of unruptured intracranial aneurysms:
probability and risk factors for aneurysm
rupture. Neurosurg Focus. 2000;8(5)
3.
Andaluz N, Zuccarello M. Recent trends in
the treatment of cerebral aneurysms: analysis
of a nationwide inpatient database. J
Neurosurg. 2008;108(6):1163-9.
4.
Ishibashi T, Murayama Y, Urashima M,
Saguchi T, Ebara M, Arakawa H, et al.
Unruptured intracranial aneurysms: incidence
of rupture and risk factors . Stroke .
2009;40:313–6
5.
Dott NM. Intracranial aneurysms cerebral
arterio-radiography and surgical treatment.
Edinb Med J 1933;40: 219-34.
6.
Dandy WE. Intracranial aneurysm of the
internal carotid artery cured by operation. Ann
Surg 1938;107: 654-9.
7.
Sahs AL. Cooperative study of intracranial
aneurysms and subarachnoid hemorrhage.
Report on a randomized treatment study. I.
Introduction. Stroke. 1974;5(4):550-51.
8.
Suzuki J, Onuma T, Yoshimoto T. Results of
early operations on cerebral aneurysms. Surg
Neurol. 1979;11(6):407-12.
9.
Suzuki J, Yoshimoto T. Early operation for
the ruptured intracranial aneurysm. Jpn J
Surg. 1973;3(3):149-56.
10. Norlen G, Olivecrona H. The treatment of
aneurysms of the circle of Willis. J Neurosurg.
1953;10(4):404-15.
11. Jane JA, Kassell NF, Torner JC, Winn HR.
The natural history of aneurysms and
arteriovenous malformations. J Neurosurg.
1985;62:321–3.
12
Tytus JS, Ward AA Jr. The effect of cervical
carotid ligation on giant intracranial
aneurysms. J Neurosurg. 1970;33(2):184-90.
13. Kassell NF, Torner JC, Haley EC. The
International Cooperative Study on the timing
of Aneurysm Surgery. Part 1: overall
management results. J Neurosurg 1990;73:
18-36.
14. Mahaney KB, Todd MM, Torner JC. Variation
of patient characteristics, management, and
outcome with timing of surgery for aneurysmal
subarachnoid haemorrhage. J Neurosurg.
2011;114(4):1045-53.
15. Shabehpoor M, Arjmand A, Safdari H, Azhari
Sh,Naebaghaee H, Mohammadi H. Outcome
of cerebral aneurysm surgery (early surgeryrelated complication and outcome after
aneurysm clip placement). Iran J Surg
2006;14(2).
16. Clatterbuck RE, Tamargo RJ. Contralateral
approaches to multiple cerebral aneurysms.
Neurosurgery. 2005;57(1 suppl):160-63.
17. Adams CB, Loach AB, O’Laoire SA.
Intracranial aneurysms: analysis of results of
microneurosurgery. BMJ 1976; 607-9.
18. Samson DS, Hodosh RM, Reid WR, Beyer
CW, Clark WK. Risk of intracranial aneurysm
surgery in the good grade patient: early versus
late operation. Neurosurgery. 1979;5(4):
422-6.
19
Spetzer V, Gilsbach JM. Results of early
aneurysm surgery in poor-grade patients.
Neurol Res 1994;16: 27-30.
20. Ljunggren B, Brandt L, Sundbarg G, Saveland
H, Cronqvist S, Stridbeck H. Early
management of aneurysmal subarachnoid
haemorrhage. Neurosurgery. 1982;11(3):
412-8.
21. Intracranial Subarachnoid Aneurysm Trial
(ISAT) Collaborative Group. Intracranial
Subarachnoid Aneurysm Trial (ISAT) of
neurosurgical clipping versus endovascular
coiling in 2143 patients with ruptured
intracranial aneurysms—a randomised trial.
Lancet 2002;360: 1267-74.
22. Molyneux AJ, Kerr RS, Yu LM. International
subarachnoid aneurysm trial (ISAT) of
neurosurgical clipping versus endovascular
coiling in 2143 patients with ruptured
intracranial aneurysms: a randomised
comparison of effects on survival, dependency,
seizures, rebleeding, subgroups, and
aneurysm occlusion. Lancet. 2005; 366
(9488): 809-17.
20. Leipzig TJ, Redelman K, Horner TG.Reducing
the risk of rebleeding before early aneurysm
surgery: a possible role for antifibrinolytic
therapy. J Neurosurg. 1997;86(2):220-5.
23. Ross N, Hutchinson PJ, Seeley H, Kirkpatrick
PJ. Timing of surgery for supratentorial
aneurysmal subarachnoid hemorrhage: report
of a prospective study. J Neurol Neurosurg
Psychiatry. 2002 Apr;72(4):480-4.
24. Bolander HG, Kourtopoulos H, West
KA.Retrospective analysis of 162 consecutive
cases of ruptured intracranial aneurysms.
Total mortality and early surgery. Acta
Neurochir (Wien). 1984;70(1-2):31-41.
37