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Editor: H.-J. Reulen
Assistant Editor: H.-J. Steiger
Neurosurgical Management
of Aneurysmal Subarachnoid Haemorrhage
Edited by
I. A. Langmoen, T. Lundar, R. Aaslid,
H.-J. Reulen
Acta Neurochirurgica
Supplement 72
Tryggve Lundar
Department of Neurosurgery, Rikshospitalet, The National Hospital, Oslo, Norway
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Preface
The small neck of the aneurysm afforded an easy surgical attack. An ordinary flat silver clip was placed over the
sac and tightly compressed obliterated it completely. The clip was flush with the wall of the carotid artery. The sac,
lateral to the silver clip, was then picked up with the forceps and thrombosed by the electocautery.
Walter Dandy reporting his successful operation of a posterior
communicating aneurysm on March 23, 1937.
Walter Dandy's patient left the hospital in good health 2 weeks later, and from his report one may gain the
impression that the operation was an easy task. Despite continuous developments during the following decades, it
was not until the introduction of the operating microscope and microsurgical techniques that surgical treatment
was generally accepted.
During the microsurgical era surgical results have continued to improve due to diagnostical, neuroanaesthesiological, and microsurgical refinements, and improved neurointensive care. Endovascular obliteration has
become an important treatment alternative but this has not been included in this particular volume.
The purpose of the present supplement of the ACTA NEUROCHIRURGICA is to review some of the elements
in the neurosurgical management of patients with aneurysmal subarachnoid haemorrhage that are important for a
successful outcome. Professor Helge Nornes has been a major force in the development of new techniques and
research strategies in this area for a number of years and has recently retired from the National Hospital in Oslo.
Helge Nornes has been a Co-Editor of ACTA NEUROCHIRURGICA since 1987. In this position he cooperated
closely with Fritz Loew and Luc Calliauw, the former and the present Chief Editor. With his strong engagement
and influence he played an important part in making ACTA NEUROCHIRURGICA one of the leading neurosurgical journals.
Some of his pupils, friends and colleagues decided to express their friendship, gratitude and respect by
dedicating this volume to him. He has all our good wishes.
Iver A. Langmoen
Tryggve Lundar
Rune Aaslid
Hans-J. Reulen
Luc Calliauw
Contents
27
Aaslid, R.:
Hemodynamics of Cerebrovascular Spasm. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
47
Lindegaard, K.-F.:
The Role of Transcranial Doppler in the Management of Patients with Subarachnoid Haemorrhage a Review.............................................................................
59
73
81
Dolenc, v. V.:
A Combined Transorbital-Transclinoid and Transsylvian Approach to Carotid-Ophthalmic Aneurysms
Without Retraction of the Brain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
89
Dolenc, V. V.:
Extradural Approach to Intracavemous ICA Aneurysms
99
107
Yonekawa, Y., Kaku, Y., Imhof, H. G., Kiss, M., Curcic, M., Taub, E., Roth, P.:
Posterior Circulation Aneurysms. Technical Strategies Based on Angiographic Anatomical Findings
and the Results of 60 Recent Consecutive Cases .............................................
123
141
Hiitter, B. 0., Kreitschmann-Andermahr, I., Mayfrank, L., Rohde, V., Spetzger, U., Gilsbach, f. M.:
Functional Outcome After Aneurysmal Subarachnoid Hemorrhage ..............................
157
175
177
Summary
This supplement of the Acta Neurochirurgica is dedicated to
professor Helge Nornes on the occasion of his retirement. Helge
Nornes started his neurosurgical training in Oslo in 1965. In 1980 he
was offered the neurosurgical chair of Bern, Switzerland, where he
stayed until 1983 when his old university called him back to the chair
at the National Hospital in Oslo, a position he filled until he retired
last year.
The present paper briefly reviews examples of his contributions to
neurosurgery and to the understanding of intracranial pathophysiology, including the transcranial doppler, the miniature transducer
for intracranial pressure monitoring, his observations on intracranial
pressure and internal carotid blood flow during subarachnoid haemorrhage, intracranial arterial blood flow in patients undergoing
aneurysm surgery, his studies of the pathophysiology of arteriovenous malformations, the introduction of intraoperative Doppler
recordings during surgery for aneurysms and arteriovenous malformations, and his methods for evaluating collateral circulation prior
to internal carotid artery occlusion.
Keywords: Cerebral aneurysm; subarachnoid haemorrhage; cerebral arteriovenous malformations; cerebral pathophysiology; transcranial Doppler; neurosurgery; biography.
Introduction
Helge Nomes grew up in Telemark, Norway where
he was born on July 26, 1930. In his young days he was
a fencing master with several national championships.
He graduated from the University of Oslo Medical
School in 1955, and thereafter focused on general surgery. While complementing his surgical training with a
short-term period in the Neurosurgical service at the
National Hospital in Oslo, his extraordinary talents
were soon appreciated by professor Tormod Hauge.
He therefore started his neurosurgical training in 1965
and became vice-chairman of the department in 1971.
In 1980 he was offered the position as professor and
director of the Neurosurgical Department in the University of Bern, Switzerland, where he stayed until
clinical investigation and published the first comparisons of intraventricular and epidural pressure recordings in 1972.
Subarachnoid Haemorrhage (SAH) and Intracranial
Aneurysms
was 78 (15-125). They further found that flow monitoring of the parent vessel was useful in some patients
in order to assess patency following occlusion of the
aneurysm neck. The average lower level of autoregulation was 62 mm Hg (35-85) in Grade I and II
patients and 76 mm (60-95) in grade III patients.
There was also a significant difference in control arterial blood pressure (110 vs 124 mm Hg). The average
lower autoregulatory range (the difference between
control blood pressure and lower level of autoregulation) was practically the same in the two groups.
The upper limit of autoregulation could not be studied
systematically but observations in a few patients
showing spontaneous blood pressure increases during
surgery indicated an upper limit of 150 mm Hg with a
total autoregulatory capacity of about 75 mm Hg.
References
1. Aaslid R, Huber P, Nomes H (1984) Evaluation of cerebrovascular spasm with transcranial Doppler ultrasound. J
Neurosurg 60: 37-41
2. Aaslid R, Huber P, Nomes H (1986) A transcranial Doppler
method in the evaluation of cerebrovascular spasm. Neuroradiology 28: 11-16
3. Aaslid R, Lindegaard KF, Sorteberg W, Nomes H (1989)
Cerebral autoregulation dynamics in humans. Stroke 20: 45-52
4. Aaslid R, Markwalder TM, Nomes H (1982) Noninvasive
transcranial Doppler ultrasound recording of flow velocity in
basal cerebral arteries. J Neurosurg 57: 769-774
5. Dahl A, Lindegaard KF, Russell D, Nyberg-Hansen R,
Rootwelt K, Sorteberg W, Nomes H (1992) A comparison of
transcranial Doppler and cerebral blood flow studies to assess
cerebral vasoreactivity. Stroke 23: 15-19
6. Lindegaard KF, Bakke SJ, Grolimund P, Aaslid R, Huber P,
Nomes H (1985) Assessment of intracranial hemodynamics in
carotid artery disease by transcranial Doppler ultrasound. J
Neurosurg 63: 890-898
7. Lindegaard KF, Grip A, Nome~H (1980) Precerebral haemodynamics in brain tamponade, part 1: clinical studies on blood
flow velocity. Neurochirurgia 23: 133-142
8. Lindegaard KF, Grip A, Nomes H (1980) Precerebra1 haemodynamics in brain tamponade, part 2: experimental studies.
Neurochirurgia 23: 187-196
9. Lindegaard KF, Grolimund P, Aaslid R, Nomes H (1986)
Evaluation of cerebral AVM's using transcranial Doppler ultrasound. J Neurosurg 65: 335-344
10. Lindegaard KF, Lundar T, Wiberg J, Sjoberg D, Aaslid R,
Nomes H (1987) Variations in middle cerebral artery blood flow
investigated with noninvasive transcranial blood velocity measurements. Stroke 18: 1025-1030
11. Lindegaard KF, Nomes H, Bakke SJ, Sorteberg W, Nakstad P
(1988) Cerebral vasospasm after subarachnoid haemorrhage
investigated by means of transcranial Doppler ultrasound. Acta
Neurochir [Suppl) (Wien) 42: 81-84
12. Lundar T, Lindberg H, Lindegaard KF, Tjonneland S, Rian R,
Bo G, Nomes H (1987) Cerebral perfusion during major cardiac
surgery in children. Ped Cardiol8: 161-165
13. Lundar T, Lindegaard KF, Froysaker T, Aaslid R, Grip A,
Nomes H (1985) Dissociation between cerebral autoregulation
and carbon dioxide reactivity during nonpulsatile cardiopulmonary bypass. Ann Thor Surg 40: 582-587
14. Lundar T, Lindegaard KF, Froysaker T, Aaslid R, Wiberg J,
Nomes H (1985) Cerebral perfusion during nonpulsatile cardiopulmonary bypass. Ann Thor Surg 40: 144-150
15. Lundar T, Lindegaard KF, Froysaker T, Grip A, Bergman M,
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
Am-Holen E, Nomes H (1986) Cerebral carbon dioxide reactivity during nonpulsatile cardiopulmonary bypass. Ann Thor
Surg41: 525-530
Nakstad PH, Nomes H (1994) Superselective angiography,
embolisation and surgery in treatment of arteriovenous malformations of the brain. Neuroradiology 36: 410-413
Nomes H (1972) Hemodynamic aspects in the management of
carotid-cavernous fistula. J Neurosurg 37: 687-694
Nomes H (1973) The role of intracranial pressure in the arrest of
hemorrhage in patients with ruptured intracranial aneurysm. J
Neurosurg 39: 226-234
Nomes H (1973) The role of the circle of Willis in graded occlusion of the internal carotid artery in man. Acta Neurochir
(Wien) 28: 165-177
Nomes H (1976) Electromagnetic blood flowmetry in small
vessel surgery. An experimental study. Scand J Thor Cardiovasc
Surg 10: 144-148
Nomes H (1977) Internal carotid artery blood flow during cerebral angiography. Neuroradiology 12: 219-225
Nomes H (1978) Cerebral arterial flow dynamics during aneurysm haemorrhage. Acta Neurochir (Wien) 41: 39-48
Nomes H, Aaslid R, Lindegaard KF (1977) Intracranial pulse
pressure dynamics in patients with intracranial hypertension.
Acta Neurochir (Wien) 38: 177-186
Nomes H, Angelsen B, Lindegaard KF (1977) Precerebral arterial blood flow pattern in intracranial hypertension with cerebral blood flow arrest. Acta Neurochir (Wien) 38: 187-194
Nomes H, Grip A (1980) Hemodynamic aspects of cerebral
arteriovenous malformations. J Neurosurg 53: 456-464
Nomes H, Grip A, Wikeby P (1979) Intraoperative evaluation
of cerebral hemodynamics using directional Doppler technique,
part 1: arteriovenous malformations. J Neurosurg 50: 145-151
Nomes H, Grip A, Wikeby P (1979) Intraoperative evaluation
of cerebral hemodynamics using directional Doppler technique,
part 2: saccular aneurysms. J Neurosurg 50: 570-577
Nomes H, Knutzen HB, Wikeby P (1977) Cerebral arterial
blood flow and aneurysm surgery, part 2: induced hypotension
and autoregulatory capacity. J Neurosurg 47: 819-827
Nomes H, Lundar T, Wikeby P (1979) Cerebral arteriovenous
malformations; results of microsurgical management. Acta
Neurochir (Wien) 50: 243-257
Nomes H, Magnaes B (1972) Intracranial pressure in patients
with ruptured saccular aneurysm. J Neurosurg 36: 537-547
Nomes H, Serck-Hanssen F (1970) Miniature transducer for
intracranial pressure monitoring in man. Acta Neurol Scand 46:
203-214
Nomes H, Wikeby P (1977) Cerebral arterial blood flow and
aneurysm surgery, part 1: local arterial flow dynamics. J Neurosurg 47: 810-818
Nomes H, Wikeby P (1979) Results of microsurgical management of intracranial aneurysms. J Neurosurg 51: 608-614
Seiler RW, Grolimund P, Aaslid R, Huber P, Nomes H (1986)
Cerebral vasospasm evaluated by transcranial ultrasound correlated with clinical grade and CT-visualized subarachnoid
hemorrhage. J Neurosurg 64: 594-600
Sorteberg A, Sorteberg W, Bakke SJ, Lindegaard KF, Boysen
M, Nomes H (1997) Cerebral haemodynamics in internal carotid artery trial occlusion. Acta Neurochir (Wien) 139: 10661073
Sorteberg A, Sorteberg W, Lindegaard KF, Bakke JS, Nomes H
(1996) Haemodynamic classification of symptomatic obstructive carotid artery disease. Acta Neurochir (Wien) 138: 10791086
Sorteberg A, Sorteberg W, Lindegaard KF, Nomes H (1996)
5
39. Stabell KE, Nomes H (1994) Prospective neuropsychological
investigation of patients with supratentorial arteriovenous malformations. Acta Neurochir (Wien) 131: 32-44
Correspondence: Professor Iver A. Langmoen, M.D., Ph.D., Department of Neurosurgery, Karolinska Hospital, S-171 76 Sweden.
Abstract
Between 20 and 30% of patients who suffer cerebral aneurysm
rupture are in poor clinical grade when first evaluated. Management
of these patients is controversial and challenging but can be successful with an aggressive proactive approach that begins with in the field
resuscitation and continues through rehabilitation. In this article we
review the epidemiology, pathology and pathophysiology, clinical
features, evaluation, surgical and endovascular management, critical
care, cost, and outcome prediction of patients in poor clinical grade
after subarachnoid hemorrhage.
Keywords: Aneurysm; clinical grade; subarachnoid hemorrhage.
Introduction
Epidemiological, population based and community
based studies demonstrate that less than one third of
people who suffer rupture of a cerebral aneurysm
return to their premorbid state. The effects of the initial
hemorrhage contribute to 60% of this death and disability following aneurysm rupture [11, 13, 117]. In
particular patients in poor clinical condition with a
depressed level of consciousness are expected to do
poorly. For example, in the International Cooperative
Study on the Timing of Aneurysm Surgery (COSTAS;
Table 1. The International Cooperative Study on the Timing of Aneurysm Surgery: Admission Level of Consciousness is Associated with Outcome*
Consciousness
level
Good
recovery %
Moderately
disabled %
Severely
disabled %
Vegetative
%
Dead %
Total, n
Alert
Drowsy
Stuporous
Comatose
Total
74.3
53.5
30.2
11.1
57.6
7.5
11.0
13.8
5.4
9.1
4.1
6.3
8.0
7.9
5.5
1.0
1.7
4.3
3.5
1.8
13.1
27.6
43.7
72.1
26.0
1722
1136
348
315
3521
Grade
o
II
III
IV
V
clinical findings
no SAH
asymptomatic or mild headache, mild nuchal rigidity
moderate to severe headache, nuchal rigidity, no neurologic deficit, except cranial nerve palsy
drowsiness, confusion, or mild focal deficit
stupor or mild to moderate hemiparesis; possible early
decerebrate rigidity
deep coma, decerebrate posturing, moribund
Grade
o
I
3
4
5
GCS* score
15
15
13-14
13-14
7-12
3-6
motor deficit
absent and no SAH
absent
absent
present
present or absent
present or absent
systems: the Hunt and Hess system [63] and the World
Federation of Neurological Surgeons Scale (WFNS;
23) based on the Glasgow Coma Scale (GCS; Table 2)
are most frequently used by clinicians to describe the
clinical severity of SAH. These two scales are comparable as predictors of outcome.
Poor grade patients are those classified as grade IV
or V in the Hunt and Hess or WFNS Scale. Clinical
grading should be performed at admission after initial
cardiopulmonary resuscitation and stabilization. Using the Hunt and Hess scale grade IV patients are
stuporous and have moderate or severe hemiparesis
whereas those in deep coma who exhibit extensor posturing and a moribund appearance are classified grade
V. When using the WFNS scale, grade IV patients
have GCS score between 7 and 12, and grade V patients a GCS between 3 and 6. In the original classification described by Hunt and Hess [63], patient grade
was increased by one level in the presence of a serious
medical condition such as heart disease or advanced
pulmonary disease. We do not reclassify grade III patients as grade IV in the presence of serious underlying
medical disorders since we believe this reflects anesthetic risk rather than the severity of SAH.
Epidemiology and Selection Bias
Intraventricular hemorrhage occurs in 15% of patients who survive aneurysm rupture, but in up to 80%
of poor grade patients [2, 81, 107]. Mortality from
aneurysmal SAH is commonly associated with IVH.
For example, Schievink et al. [141, 142] observed IVH
in 92% of the patients who died suddenly after aneurysm rupture. Among these patients, 38% suffered a
ruptured posterior circulation aneurysm. Any aneurysm can cause IVH if the SAH is large enough or from
extension of an ICH. However, IVH is most frequent
after posterior circulation and anterior communicating
artery aneurysm rupture. Internal carotid and posterior communicating artery aneurysm may rupture into
the temporal horn of the lateral ventricle particularly if
the aneurysms are large and have grown into the temporal lobe. Intraventricular hemorrhage is associated
with acute or chronic hydrocephalus, increased intracranial pressure, decreased cerebral blood flow and the
subsequent development of vasospasm. Acute hydrocephalus generally results from obstruction of CSF
flow whereas chronic hydrocephalus results from
ependymal, subependymal and arachnoid villi damage, fibrosis and blockage of CSF absorptive surfaces
[10, 39, 107, 128, 139]. Intracranial pressure is often
normal in chronic hydrocephalus.
Cerebral infarction is common in poor grade patients, particularly those surviving greater than 1 day
[17, 40]. In addition, the amount of subarachnoid
blood seen on CT scan, but not its rate of clearance is
associated with infarction [33]. The presence of hypotension and ICH increases the risk of infarction threefold [2, 17, 40]. In some patients ICH and resultant
brain herniation can lead to strangulation of the
posterior cerebral artery and consequent occipital infarction. Delayed infarction also can result from intractable intracranial hypertension or vasospasm.
Pathophysiology
10
oxide synthetase in macrophages, astrocytes, and endothelial cells, a process that is augmented by hemoglobin [60,86, 161]. Together these observations suggest that the administration of cerebral protectants to
poor grade patients may ameliorate the effects of cerebral ischemia.
Clinical Features
A depressed level of consciousness is the sentinel
neurologic finding of poor grade aneurysm patients.
Other neurologic findings may include a dilated pupil
and asymmetric motor or reflex responses. However,
the most consistent clinical observation in these patients is neck stiffness [1]. In comatose patients a history is often not available, consequently the diagnosis
of SAH should be suspected in non traumatic coma
patients, particularly females in their 4th and 5th decades. Some poor grade patients may present with
cardiac abnormalities, respiratory irregularity, neurogenic pulmonary edema or cardiorespiratory arrest
[85, 129, 149]. For example, in a population based
study of all SAH grades, Ramirez and Lassepas [129]
found 14% of the patients suffered cardiorespiratory
arrest. This represented 4.9% of all cardiorespiratory
arrest patients who were successfully resuscitated before arrival at the emergency room. The patients were
all grade V at admission and generally demonstrated
thick diffuse SAH, IVH or ICH on head CT scan [129,
149]. Clinical improvement after resuscitation is a
generally favorable prognostic sign in poor grade patients particularly if there are only minor changes on
head CT scan [81, 114].
11
cally ventilated. Following the initial neurologic assessment, mechanical ventilation can be maintained
using short acting drugs such as intravenous morphine,
midazolam or diprivan. These same medications also
can control severe hypertension in some patients. Each
patient should undergo a standard laboratory evaluation including electrolytes, blood glucose, complete
blood count, coagulation profile, chest xray and EKG.
Four units of blood should be crossmatched. After
initial stabilization in the emergency room a thorough
radiographic evaluation is undertaken. Some poor
grade patients particularly those demonstrating massive ICH may go directly to the operating room others,
however, should be admitted to the intensive care unit.
Intracranial pressure and invasive hemodynamic
monitoring, including an arterial line and Swan Ganz
catheter, are recommended.
Computed tomography is the investigation of choice
to diagnose aneurysm rupture. Additional information
can be obtained from infusion CT scan, or 3D spiral
CT [61, 77, 109]; these radiological tests are particularly useful in the unstable patient after aneurysmal
ICH and giant or complex aneurysms. MRI and MRA
presently playa limited role in the evaluation of poor
grade patients. Apart from moribund patients who
may go directly to the operating room for ICH evacuation, all other patients require four vessel angiography that should demonstrate: 1. the aneurysm sac
and orientation, 2. the aneurysm neck, 3. the relationship between the lesion and parent vessels, and 4. the
state of the cerebral vasculature. Angiography in poor
grade patients is best performed after intubation and
the insertion of invasive monitoring lines and with the
assistance of critical care nursing.
Management Strategies
There are several management strategies for poor
grade patients derived exclusively from clinical series:
1. no treatment, 2. treatment of select patients only,
3. delayed treatment after clinical improvement, or
4. aggressive proactive treatment including rapid resuscitation and ICP control, early aneurysm occlusion,
and prophylaxis against delayed ischemia. Without
question many patients in poor clinical grade following SAH and irreparably damaged, however, the published data suggest that an aggressive policy may provide these patients their most reasonable chance of
neurologic recovery (Table 3). Untreated greater than
90% of poor grade patients die or are severely disabled
12
Table 3. Summary of Published Data Describing Overall Management Outcome in Hunt and Hess Grade IV or V Patients
Another
Patients"
Age (yrs)
47(17.1%)
61 (26%)
80 (36%)
20 (6.3%)
NR
NR
mean 51.4
range 14-73
NR
42 (15.9%)
32 (34.7%)
14 patients> 70
80 (32.8%)
157 (24.8%)
108 (NR)
66 (24.4%)
NR
44% >60
Est 54
mean 47.2
range 20-74
mean 53.1
NR
Management
Outcome
%
favorable
poor
dead
NR
18
3.8
NR
24.6
8.8
78.7
57.4
87.4
20
75
23
71
15.6
9.5
15.6
18.4
68
72.9
25
9.5
25
29
15.2
21.3
46
75.2
53.7
19.6
12.2
68.2
7
20.8
17.8
5
15.7
16.4
88
63.5
65.8
50
67.4
42.2
56.9
42.5
41 (36%)
370 (22.8%)
54 (23.3%)
74(17.3%)
109 (39.4%)
116 (20.2%)
48 (24.5%)
mean 56
14pts >60
NR
Est 49.5
mean 53.1
range 31-77
42.6
20.2
21.1
35.3
21.3
7.4
12.2
36.7
7.8
36.2
28.1
20.1
51.8
159 (36.5%)
median 54
38.4
18.2
43.4
Average
Favorable independent including Glasgow Outcome Score of good and moderately disabled; Poor dependent, including Glasgow Outcome
Score of severe disability and vegetative; CCB calcium channel antagonists; EVD ventricular drainage; HVhypervolemia; ICH intracerebral
hemorrhage; selective aggressive emergency evacuation of ICH, early surgery on patients demonstrating clinical improvement or controllable
ICP after ventricular drainage; not all patients intubated and ventilated; N R not reported.
"The number of patients presenting in poor clinical grade after aneurysm rupture. This number is given in parentheses as a percentage of all
patients in all clinical grades treated at the same institution(s).
bvalue estimated from limited data.
Modifed from: Le Roux et al. [81].
sufficient to accurately predict outcome in the individual poor grade patient [7,9,12,77,81, 112, 159].
Reliable prognostic information requires additional
evaluation such as ICP monitoring, and continued
neurologic observation [7,77,81,112,147,159]. Outcome, however, is largely determined by the initial
hemorrhage and its immediate pathophysiologic consequences; a short time frame, therefore, exists in
which the deleterious effects of severe SAH may be
ameliorated [32]. In our experience, attempting to
select Grade IV and V patients for treatment based
only on admission clinical and diagnostic findings, including evidence of brainstem herniation, would result
in withholding treatment from a third of poor grade
patients who subsequently can experience a favorable
13
...
,-----'-----,
t
IVH &/or
SAH
ICH
Hydrocephalus
Ventriculostomy
ICPM
ICP > 30
(not controlled)
ICP < 30
(controlled)
Craniotomy
Clip Aneurysm
Craniotomy
ICH Evacuation
Clip Aneurysm
< 65 yrs
No Medical Problems
<65 yrs
No Medical Problems
Angiography
II
Endovascular
Aneurysm Occlusion
> 65
Consider
Endovascular
Aneurysm Occlusion
1----
Neurologically Improved
ICP Controlled
No Low Density on CT
Aggressive Care
~
Rehabilitation
L------,I
Aneurysm Remnant
Craniotomy
Clip Aneurysm
Fig. I. Algorithm illustrating management approach to poor grade aneurysm patients. CT Computed tomography; SAH subarachnoid hemorrhage; ICH intracerebral hemorrhage; IVH intraventricular hemorrhage; ICP M intracranial pressure monitor; ICP intracranial pressure
14
Etiology
Diagnosis
Neurologic
Rebleed
Vasospasm
Hydrocephalus
Cerebral edema
Arterial thromboembolism
Seizures
CT scan
TCD, angiogram, SPECT
CT scan
CTscan
angiogram
EEG
Intracranial hematoma
Perforator injury
Major vessel occ1uison
Inadequately occluded aneurysm
Infection
CT scan
CT scan, angiogram
angiogram
angiogram
culture wound or CSF
Systemic
Hyponatremia
Hyoglycemia or hyperglycemia
Endogenous toxins
Hypotension, hypovolemia
Infection
Hypoxia
serum electrolytes
blood glucose
hepatic and renal function
CVP,PCWP
white blood cell count, cultures
arterial blood gas, CXR
Timing of Surgery
Several clinical series have established that endovascular occlusion of ruptured aneurysms using GDC
coils is feasible and that in expert hands approximately
50% of aneurysms can be completely occluded [14, 41,
44, 126, 130, 168]. By contrast, routine postoperative
angiography following surgical obliteration of 637
aneurysms demonstrated complete occlusion in 94% of
the aneurysms [79]. In general adequate morphological
results using endovascular techniques are expected in
small aneurysms with small necks 4 mm) and those
at a right angle to blood flow [126, 130, 168, 177]. Endovascular procedures appear less effective in large or
wide necked aneurysms. Aneurysm location may also
influence the success of the procedure [98, 126, 130]. It
is important therefore that the surgeon and interventionist together select which patients require surgery or
coil embolization.
There are three potential limitations to the routine
use of endovascular techniques in repair of ruptured
aneurysms in poor grade patients. First, limited shortterm studies (6-12 months) suggest that aneurysm recurrence may occur after coil embolization [14, 91].
Furthermore 20% of patients undergoing endovascular aneurysm occlusion require a second procedure,
usually surgery, within 3 years [91]. By contrast, between 1 and 4% of aneurysms that are surgically occluded require a second operation [37, 79, 80]. Second,
using endovascular techniques only half the aneurysms
can be completely occluded at a primary procedure. It
is not clear whether the patient with a partially occluded aneurysm is still subject to the same risk as a
patient with an unsecured but ruptured aneurysm. It is
15
16
17
Elderly Patients
The association between advanced age and poor
outcome after SAH is well described, in part because
many elderly patients are in poor clinical grade or excluded from active treatment [29, 50, 55, 58, 66, 69, 73,
18
19
an association between outcome and medical complications after SAH. In addition, improved management
results are associated with a decrease in the incidence
of complications and secondary insults but not our
ability to respond to them [78]. These findings suggest
that critical care monitoring in specialized neurovascular intensive care units and proactive attempts to
avoid complications may contribute to improved outcome after poor grade SAH.
leu Monitoring
Poor grade patients should be managed in the ICU
for at least the period that corresponds to the maximum risk of vasospasm approximately 10-14 days after aneurysm rupture. There are many causes of deterioration following SAH in poor grade patients (Table
4); the key to management of these problems is prevention. The clinical exam in the poor grade patient,
however, can be difficult to interpret. We therefore
recommend that poor grade patients undergo invasive
cardiopulmonary and intracranial monitoring that is
supplemented with frequent head CT scans and
SPECT scans and daily transcranial Doppler [TCD].
Cardiopulmonary monitoring is best achieved through
an intrarterial blood pressure monitor, Swan Ganz
catheter to assess pulmonary artery pressure and cardiac output, chest xray and arterial blood gas analysis.
Frequent assessment of electrolytes, osmolality, glucose, hematocrit and urine output supplement invasive
monitoring. Invasive cardiopulmonary monitoring in
necessary to safely institute and maintain hypervolemic and hypertensive therapy since up to one third
of patients receiving hypervolemic therapy may suffer
cardiopulmonary complications including myocardial
ischemia or pulmonary edema [100]. An ICP monitor
is useful in all poor grade patients. In our experience
60% experience an episode of intracranial hypertension following aneurysm occlusion. In addition we
have found that failure ofICP to respond to Mannitol
administration rather than median maximum ICP is
significantly associated with an unfavorable outcome
[81]. ICP monitoring can also be used to detect the development of cerebral edema associated with hypervolemic therapy, allowing for appropriate adjustments
in intravenous fluid and pressor management [151].
The length of ICP monitoring is determined by a variety of factors including whether the patient is intubated, clinical condition, findings on postoperative
CT, and risk factors for vasospasm. The risks of ICP
20
monitoring are very low: in over 500 aneurysm patients treated at our institution between 1983 and 1993
using routine rcp monitoring, we had no significant
complications. A retrograde jugular catheter to determine venous oxygen saturation, AVD02 and lactate
may augment rcp monitoring. In head injury, these
parameters have been found to be useful in identifying
patients with compensated hypoperfusion who are at
risk for ischemia [82].
Vasospasm
Patients in poor clinical grade after SAH are at high
risk for cerebral vasospasm and delayed ischemic neurologic deficits (DIND). Specific management of vasospasm is discussed elsewhere in this supplement,
however there are two important considerations in
poor grade patients: prevention and detection. Maintenance of an adequate intravascular volume, that is
frequently reduced after SAH, is important in preventing the development of DIND [47]. In poor grade
patients we believe this is best achieved by early hypervolemic therapy using non-glucose containing isotonic electrolyte solutions and colloids to achieve a
pulmonary capillary wedge pressure of 14-16 mm Hg
and cardiac output between 6 and 81Jmin. Mineralocorticoids such as fludrocortisone acetate may help
maintain intravascular volume and reduce the incidence of delayed ischemia [46]. If cardiac output falls
b-adrenergic agonists such as dobutamine can be administered. In some patients, hypervolemia can lead to
resolution of delayed ischemic deficits [116, 165],
however, we frequently add induced hypertension
when symptomatic vasospasm develops. In the subgroup of patients who demonstrate progressive clinical
deterioration despite maximal medical therapy, percutaneous transfemoral angioplasty or selective intrarterial papaverine, in some patients can reverse an ischemic deficit after it has developed [56, 71, 83, 108].
Transcranial Doppler studies demonstrate that balloon angioplasty is superior to papaverine infusion in
producing sustained resolution of vasospasm and is
associated with fewer treatment failures [27]. Hypervolemic therapy can be associated with potential cardiac, pulmonary and hematologic complications
therefore pulmonary artery catheter monitoring is advocated to optimize therapy.
An important factor in the management of delayed
ischemia is early and accurate diagnosis of vasospasm.
Clinical features of vasospasm are unpredictable and
depend on several variables including severity and location of arterial narrowing, patient age and clinical
condition, presence of complicating factors such as
raised ICP, and extent of collateral circulation. Angiography is the definitive diagnostic test for vasospasm but is invasive and can not be repeated each
time the patient develops a neurologic deficit. Instead
we have found a combination of daily TCD and frequent SPECT examinations useful in the evaluation of
poor grade patients [81, 85, 87]. Although there are
limitations in the use of TCD, elevated cerebral arterial blood velocities in the setting of SAH, are highly
correlated with angiographic vasospasm. In addition,
the ratio of middle cerebral to cervical carotid artery
velocity can differentiate vasospasm from increased
cerebral blood flow from hyperdynamic therapy or
predict the development of symptoms [42, 64, 145]. A
prominent increase or rapid rise in TCD velocities
during the first week after SAH is characteristic of
vasospasm and often precedes the onset of clinical
symptoms. Similarly return of TCD velocities to normal usually signals the remission of vasospasm and
can help determine the duration of hypervolemic therapy. In prospective studies routine TCD examinations
have been found to make a positive contribution to the
management of patients after SAH. SPECT studies
provide an assessment of regional cerebral blood flow
and provides a measure of the degree of compensation
in the microcirculation in the face of proximal vasospasm [87, 153]. In some poor grade patients alterations in TCD or SPECT may be used to institute
appropriate therapy before symptoms develop or
when an adequate neurologic assessment cannot be
performed.
Nimodipine is a lipid soluble calcium channel
blocker that was developed to selectively relax smooth
muscle of vasospastic vessels. The use ofnimodipine in
Hunt and Hess grade III - V patients has been assessed
in a multicenter randomized, placebo-controlled,
double-blind study [123]. Nimodipine treatment was
associated with a significant increase in good outcome
at 3 months: 29.2% ofnimodipine treated (n = 72) and
9.8% of placebo-treated (n = 82) patients experienced
a good outcome. In addition, the incidence of delayed
ischemic deficits were significantly lower in nimodipine
treated patients (6.9%) than patients receiving placebo
(26.8%). However, there was no difference in the incidence or severity of angiographic vasospasm. The
association between calcium influx and cell death in
cerebral ischemia is well described; it possible therefore
21
Systems Approach
Prehospital and emergency department management of head trauma patients can have a profound
impact on outcome. Many individuals, including
emergency medical technicians, paramedics, emergency physicians, anesthesiologists, and ER nurses
provide important care soon after head trauma.
Several lines of evidence suggest that an organized
responsive trauma system that includes prehospital
management and triage, organization of facilities, and
immediate availability of a surgeon can prevent death
at relatively low cost [101]. Several investigators have
compared organized and non-organized trauma systems; in all comparisons better patients outcome is
observed using organized trauma systems [101, 136,
148, 154]. The improved survival is attributed to prehospital and hospital care integration and expeditious
surgery. Similarly, improved outcome results are observed after ischemic stroke when patients are treated
within 3 to 6 hours of symptom onset; this hyperacute
treatment, however, requires a systems approach
[166]. Poor grade SAH has many parallels to severe
head injury and ischemic stroke. The experience with a
systems approach in these disorders suggests that SAH
management may benefit from a multidisciplinary
systems approach. Neurosurgeons must become
actively involved in identifying, streamlining and implementing SAH treatment protocols into prehospital
and hospital care and making the care of SAH patients
an integral part of a "Brain Attack" organization. In
many instances SAH treatment may be integrated into
severe head injury or "Brain Attack" management
schemes that are already in place in many cities.
Cost
Health care is presently undergoing significant reorganization and often is driven by cost containment.
Successful management of poor grade SAH requires a
multidisciplinary approach that incorporates intensive
paramedic and hospital care and utilizes technological
advances; factors that are frequently portrayed as
responsible for a significant portion of health care
Median
LOS (days)
Mean LOS
(days)
Hospital charges
(1995 US dollars)
10
15
18
23
28
16
14
18
20
24
27
21
52,064
65,949
83,232
99,369
108,690
96,194
2
3
4
5
Conclusion
In this chapter we have reviewed the management of
patients in poor clinical grade after SAH. Management of these patients is controversial and challenging
but can be successful with an aggressive proactive
approach that begins with in the field resuscitation and
continues through rehabilitation. Advances such as
a systems approach, critical care techniques, neuroanesthesia, innovative neuroimaging, interventional
techniques and technical advances in surgical management can improve the outcome for patients in poor
clinical condition after SAH. The successful and costeffective use of these advances requires a dedicated,
knowledgeable, multidisciplinary team and a commitment to ongoing research.
22
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148.
149.
150.
151.
152.
153.
154.
155.
156.
157.
158.
159.
160.
161.
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Summary
Cerebral vasospasm is a gradual onset and prolonged constriction
of the cerebral arteries in the subarachnoid space after subarachnoid
hemorrhage. The principal cause is the surrounding blood clot. The
significance of vasospasm is that flow through the constricted arteries
may be reduced sufficiently to cause cerebral infarction. Subarachnoid blood clot is sufficient to cause vasospasm; it does not require additional arterial injury, intracranial hypertension or brain
infarction, although these elements are often coexistent. The blood
released at the time of aneurysmal rupture into the alien subarachnoid environment is an extraordinarily complex mix of cellular
and extracellular elements that evolves as clotting occurs; cells disintegrate; local inflammation, phagocytosis and repair take place;
severe constriction alters the metabolism and structure of the arterial
wall as well as the balance of vasoconstrictor and dilator substances
produced by its endothelium, neurogenic network and perhaps
smooth muscle cells.
Keywords: Vasospasm; hemoglobin; endothelin; nitric oxide.
Introduction
The etiology of vasospasm is subarachnoid blood
clot. There are sporadic reports of arterial narrowing
occurring in the absence of subarachnoid hemorrhage
(SAH). These usually involve hemorrhage into the
cerebrospinal fluid elsewhere such as into the ventricles, raising the possibility that the subarachnoid
arteries are bathed in blood products. In cases of
meningitis and after surgery for intracranial tumors or
unruptured aneurysms, the pathology of the arterial
narrowing may differ from vasospasm in that it may be
true vasculitis with meningitis, or there may be unrecognized SAH occurring at the time of surgery [50].
When the SAH results from rupture of an aneurysm,
there is usually little surrounding arterial injury but the
SAH will be accompanied by varying degrees of intracranial hypertension and brain ischemia. These latter
processes are not by themselves accompanied by
vasospasm with any consistency which leads to the
28
B. Weir et at.
peak 7 days ~
50
~----
angiographic vasospasm
symptomatic spasm
o
~
100
,S
'~
1l
Indma:
IEL:
Media:
nitrite/nitrate, TAT
7
Time
vacuolated endothelium
loss of tight iunctions, corrugated
fragmented
corrugated
smooth muscle cells contracted
markedly thickened, vacuoles,
some necrosis
(Days)
15
21
fibrotic, thickened
foamy
regenerating smooth
muscle cell.
Fig, I, Graph of the time course of angiographic and symptomatic vasospasm and pathological changes in arteries. Angiographic vasospasm is
maximal 7 days after a single SAH whereas symptoms from vasospasm (symptomatic vasospasm) have their most frequent onset at 8 days.
Pathological changes in the cerebral arteries over time are shown at the bottom. Initially, there is contraction of the smooth muscle cells. During
the second week after SAH, there is some necrosis of smooth muscle and endothelial cells and possibly fibrosis of the arterial wall and infiltration with inflammatory cells, Weeks after SAH, there is fibrosis in the tunica media and adventitia and varying degrees of endothelial proliferation, TAT thrombin-antithrombin III complex; ET endothelins; IEL internal elastic lamina
Clinically-evident symptoms and infarction from ischemia due to vasospasm alone are more likely with
increased volume of SAH, in elderly patients, in patients with long-standing hypertension and when the
patient presents in poor neurological grade [72]. In
addition, increased intracranial pressure, low blood
oxygen or glucose, hyponatremia, hypovolemia, increased blood viscosity, hypotension, hyperthermia,
absence of favorable communicating or collateral arteries or the presence of preexisting stenoses or arterial
occlusions will tip the scales toward infarction. Since
infarction develops when a region of brain is subjected
to a critically reduced blood flow for an excessive time,
systemic physiological factors come into play. To
avoid infarction, the blood must be adequately oxygenated, the hematocrit must be sufficient and cardiac
function must provide a safe pressure and flow to the
brain. The intracranial pressure must not be so elevated that blood flow is interfered with.
If angiography is performed around a week following SAH about two-thirds of patients will show angiographic vasospasm. However, this will be sufficient
to cause symptoms in only one-third. The time course
of vasospasm is the same regardless of its severity. If a
patient does develop symptomatic vasospasm, then
recovery, permanent deficit or death can be anticipated
(in the absence of effective therapy) in about one-third
each.
Many studies have indicated that vasospasm is an
important but far from the only prognositc factor for
adverse outcome after SAH. Others include age,
neurological condition immediately after SAH, preexisting medical conditions especially hypertension,
aneurysm size and site, intraventricular/intracerebral
29
30
B. Weir et al.
OxyH,b
erythrocyte
.---
4 glo\ in chains
4 herr e moities
~!~~~~:e
membrane stroma
other cytosol
proteins
OxyHb + Deoxy Hb
PyrroJe
"'-Fe>+ -
PyrroJe
/
l'~-i' .""""00
PyrroJe
'"
0,
PyrroJe
02
A~
Heme
~l
~
Globin
chains
Free radical
reactions
heme
oxygenase types 1,2
NADPH
NADP"
~
? vasodilation
Bilirubin IXa
Fig, 2, Diagram of the metabolic pathways for breakdown of
hemoglobin
Pathophysiology of Vasospasm
Potential Spasmogens
It is not surprising that evidence for a single, universal spasmogen has not been forthcoming. It is likely
that hemoglobin (Fig. 2, the most abundant vasoconstrictor released from decaying erythrocytes) or its
derivatives is at least one of the factors, but other
compounds such as adenosine triphosphate (ATP) also
are found in high concentrations and under some experimental conditions can lead to constriction [52,82].
An imbalance between physiological vasoconstrictors
such as endothelins (ETs) and prostaglandins and
physiological vasodilators such as nitric oxide (NO) or
prostacyclin (PGIz) could also playa part. There is
some evidence for a significant alteration in prosta-
glandin metabolism after SAH in that there is increased production of vasoconstricting prostaglandins
and thromboxanes and decreased synthesis of PGIz
(Fig. 3).
After SAH, erythrocyte hemolysis (physical disruption) begins almost immediately and continues until
all the red cells are phagocytized or lysed. In animals,
erythrocytes may cross into the bloodstream intact
after SAH but it is not known if this happens in man.
Red cells incubated in CSF in vitro at body temperature release large amounts of hemoglobin over hours
to days. The rate of hemolysis and of conversion from
ferrous (Fe2+) to ferric (Fe3+) hemoglobin depends on
the conditions of incubation such as temperature, agitation, whether incubation is in vitro or in vivo and
the presence of plasma proteins. After SAH, lumbar
puncture shows that CSF is clear of red blood cells
within a few days to a month. The rate of clearance of
SAH depends mainly on the volume of SAH and perhaps is faster in youth.
With SAH, there is influx of blood elements into the
subarachnoid space (Fig. 4). Each element is a potential spasmogen (Table 1) although the most extensively studied are hemoglobin, eicosanoids and free
radicals [17, 18,47,48]. SAH may also tip the balance
of physiological regulators of cerebrovascular tone
(Table 2) from normal towards a state of contraction.
The criteria that would be expected of any spasmogen
accounting for vasospasm are listed (Table 3). Since
vasospasm is dependent on the continuing presence of
subarachnoid blood clot (unpublished observations),
processes occur continually to produce spasm. There
could be ongoing release or formation of the same or a
series of spasmogens over time. Other potential interactions with brain and the cerebral arteries may be
postulated (Fig. 4).
Since red cells are the most numerous, since hemoglobin is their principal protein, since it is progressively
released in an appropriate time course as the cells disintegrate and since it is a vasoconstrictor in a wide variety of in vitro and in vivo model systems, it is a key
suspect as the main spasmogen [46, 47] (Table 4).
Several clot fractionation experiments have also demonstrated that erythrocytes are the blood component,
and not white blood cells, platelets, plasma, or erythrocyte ghosts alone, that cause vasospasm in vivo, although the vasospasm that was produced usually was
not as severe as that caused by whole blood [47]. We
suspect hemoglobin is not the sole factor because hemolysate of red cells, which contains numerous sub-
31
Phospholipids
cyclo-oxygenase
PLA2, PLC
Arachidonic Acid
5-lil'H"yg,~~
15-lipo-oxygenase
PGG2
, peroxidase
PGH2
PGI2~XA2
15-HPETE
LipoxinA
LipoxinB
5-HPETE
/
LTA4
A
JI
LTB4
(prostacyclin/KmboXane)
+
~
15-HETE
glutathione
~5-transferase
LTC4
I glutamyl
transferase
LTD4
~ aminopeptidase
LTE4
+IN-acetyl
transferase
N-acetyl-LTE4
RELAXATION
CONTRACTION
I INFLAMMATION I
Fig. 3. Diagram of metabolic pathway of arachidonic acid production of eicosanoids (prostaglandins, thromboxanes, leukotrienes). PLA 2
Phospholipase A2 ; PLC phospholipase C; PG prostaglandin; HP ETE hydroperoxyeicosatetranoic acid; LT leukotriene
ICH
ICP
1 brain damage
..
?
inflammatory _ _~~rl
cells
final common
pathway of ischemia
spasm
stantial impurities including methemoglobin, endotoxin and other substances. Ultrapure hemoglobin in
some of our recent experiments is not a very potent
constrictor in vivo. The ability of fresh erythrocyte
hemolysates to increase intracellular Ca++([Ca++U in
smooth muscle cells was more related to the ATP
content of the hemolysate than to any other compound
[99]. Aoki, et al., also noted that the contractile activity
of hemoglobin was low until a low-molecular weight
fraction of hemolysate (0.5 to 2 kD) was added to the
hemoglobin [2]. This suggests that hemoglobin alone
may not be the cause of vasospasm and that low molecular weight substances may be involved (Table 5).
Smooth Muscle Contraction
32
B. Weir et al.
Table 1. Potential Spasmogens Released after SAH and Their Possible Role in Vasospasm
Spasmogen or process
Possible role
Compound
2. Platelet contents
serotonin
adenosine nucleotides
vasoconstriction
unknown
provide lipid for lipid peroxidation,
unknown
possible vasoconstriction early
after SAH
vasoconstriction
Amines
norepinephrine
serotonin
histamine
dopamine
acetylcholine
Lipids
eicosanoids
leukotrienes
platelet-activating
factor
Peptides
sympathetic
other constrictors
parasympathetic
trigeminal sensory
other vasodilators
Purine nucleotides
adenosine
ADP and ATP
Gases
nitric oxide
carbon monoxide
Action
33
Table 5. Evidence for a low Molecular Weight Spasmogen ( LMWS), Possibly ATP, as a Cause of Vasospasm
"
- isolated rat basilar artery smooth muscle cells develop increased [Ca++]i in a dose-dependent fashion when exposed to LMWS from fresh
human erythrocyte hemolysate but the effect diminishes with time, being absent after 21 days of incubation
- effect was potentiated by a high molecular weight fraction of he moly sate and also by pure hemoglobin that did not affect [Ca++]i independently
- erythrocytes contain ATP (1.6 mmol/L) in concentrations that contract vascular smooth muscle
- rat femoral arteries contract after 7 days exposure to substances containing ATP such as dog hemolysate or ATP itself but not pure hemoglobin
- chronic vasospasm in monkeys resulted from subarachnoid placement of ATP, hemolysate or pure hemoglobin
- dog hemolysate containing ATP, 34 J.lIllol/L, produced concentration-dependent contractions of dog basilar artery that were inhibited by
suramin, a P 2 -purinoceptor antagonist
- hemolysate increases rCa ++]i in both rat basilar artery smooth muscle and bovine middle cerebral artery smooth muscle cells by releasing
Ca++ from internal stores and causing Ca++ entry by voltage-independent Ca++ influx, effects which are identical to ATP
- nucleotides such as ATP and UTP activate G-proteins coupled to P2u -purinoceptors to mobilize [Ca++]i in rat basilar artery smooth muscle
cells
34
B. Weir et al.
Norepinrphrin. An~iotcnsin II .
...----- Endothelin, SHT. ATP
Ca2+
d...I"';=,;oo
C+ca,.~~
Ca2+~ I_~
I Receptor.gated
Ca" channel
independent of
G'protein
Ca"
Ca" calmodulin
ATPase
myosine light
chain kinase
G protein
'.5,~;;;;,u.
Intracellular
Cal + stores
(sarcolemma)
~. ADP.
'--(
M'
---':::::====111
~_
)"T
PLC
Phosphotidylinositol
Ca" calmodulinMLCK
ATP\
-=
ft
Myosin P Actin
IP)-sensitive
1Ca" release
PKC
I alternative
contraction
regulation system
~Or:I===A=ct=in=!=~=;o=C:=I~n=,p==_===C:=:::O=N=T=RA=C=T=IO=N=/==~
Ca2+V~Na+
Na+Ca++ exchange
Fig. 5. Diagram of pathways of smooth muscle contraction. See text for discussion. PLC Phospholipase C; DA G diacyl glycerol; PKC protein
kinase C; MLCK myosin light chain kinase; ADP adenosine diphosphate; ATP adenosine triphosphate
but one theory is that an intracellular second messenger signals plasma membrane channels about the state
of filling of the stores [60]. Luminal Ca++ in the sarcoplasmic reticulum activates a tyrosine phosphatase
that shifts a 130 kD protein towards a dephosphorylated state. Depletion of the Ca++ stores favors phosphorylation of the 130 kD protein, which then gates a
Ca++ -permeable membrane channel. Other theories
are that sarcoplasmic Ca ++ content is signalled to the
plasma membrane by a cytochrome P450-dependent
mechanism or by a cyclic GMP-mediated signalling
system.
Although Ca++ is an important intracellular second
messenger mediating contraction, there is only an indirect relationship between [Ca++]j and smooth muscle
contraction (Fig. 5) and contraction to agonists can
develop without any change in [Ca++Ji, Most tonic
contractions persist after [Ca++]j has returned to basal
or near-basal levels and after myosin light chain
phosphorylation also has decreased [20, 93]. Processes
postulated to explain prolonged tension development
in the absence of increased [Ca++]j and myosin light
chain phosphorylation are the latch state or another
regulatory mechanism such as one due to phosphorylation of other cytoplasmic proteins by, for example,
protein kinase C [20, 93].
Some compounds thought to cause vasospasm can
35
increase [Ca++]j in smooth muscle cells, including hemoglobin, erythrocyte hemolysate and ATP [84, 86,
88]. Measurements of [Ca++]j in vasospastic dog basilar artery have shown either an increase [6], no change
or a decrease [78, 95]. The manipulations required to
make such measurements are extraordinarily difficult
and the significance is uncertain since there is not a
direct relation between [Ca++]j and contraction. For
example, calmodulin was reduced in vasospastic arteries and the calmodulin-inhibitor, trifluoperazine,
had minimal effect on vasospasm in vivo in dogs
suggesting that vasospasm is not due to persistently
elevated Ca++ -calmodulin complex [71]. The ability of
the smooth muscle to regulate [Ca++]j may be disrupted during vasospasm in the absence of changes in
[Ca++]j, or the contractile apparatus may be more
sensitive to [Ca++]j leading to contraction [60]. Wang
et al. reported that the plasma membrane Ca++ATPase that pumps Ca++ out of cells and lowers
[Ca++]j, was significantly decreased in basilar artery
smooth muscle after SAH in dogs and Kim, et al.,
found an increased permeability of smooth muscle to
Ca++ in the same model [41, 92].
Investigators also have examined changes in other
components of contraction during vasospasm. Most
but not all [6] studies of vasospastic arteries found
levels of myosin light chain phosphorylation were not
markedly elevated [49]. ML-9, an inhibitor of myosin
light chain phosphorylation, also had only a modest
effect on vasospasm [42]. Levels of contractile proteins
were decreased during vasospasm, perhaps reflecting
activation of proteolytic enzymes such as the calpains.
The cal pains are neutral proteases that are activated
by increased [Ca++]j. They catalyze break-down of
cytoskeletal and contractile proteins and protein kinases, leading in part to activation of these kinases,
including protein kinase C [43, 49]. Some of the pathways that are activated may lead to smooth muscle
contraction. The decrease in contractile proteins and
in caldesmon, the demonstrated activation of calpain
proteolysis, and the efficacy of inhibitors of calpeptin
against vasospasm in rats, dogs and rabbits, supports a
role for Ca++ -activated proteolysis in vasospasm [43].
Calponin is a troponin-like protein that inhibits the
actin-myosin interaction [10, 93). Its action is accentuated when it is phosphorylated by protein kinase C
or Ca++ -calmodulin-dependent protein kinase II. A
decrease in calponin that was noted in vasospastic arteries could promote vasoconstriction [10].
The activation of protein kinase C that may occur
36
B. Weir et al.
Agonists Ach
Thrombin,
bradykinin.
shear stress,
5HT,ADP
- - - - - - t..~
arachidonic acid
1\
~
....,
EDHF
:: )
~_
. . . . . . /NO
} ~~~: __~--~------'--J~_~
.,
"~_O
Endothelial Cen
// t tK + ~,
/
?
"'
,,"'''''"','~,;..
"
-'~~~
'
~@
',__! _
ATP
Smooth
muscle
cell
~---''=--'--=-
cAMP
On'
RELAXATION
~--
Fig. 6. Diagram of pathways of smooth muscle relaxation. EDHF Endothelium-derived hyperpolarizing factor; AC adenylate cyclase; GC
guanylate cyclase; ATP adenosine triphosphate; cGMP cyclic guanosine monophosphate. See text for discussion
Endothelins
The ETs are 3 2l-amino acid peptides synthesized
by endothelium and other tissues (Fig. 7). They are
proteolytically cleaved from preproET precursors.
Once released from cells as proETs (big ETs), they are
cleaved by ET converting enzyme(s) to the active ETs.
Endothelin-l and -3 are found in brain and endothelial
-i
r
Thrombin
-~~-------------~.
Vasospasm
------....
Angiotensin II
Big endothelin-l
TGFJ3
37
Bigendothelin-3
endothelin converting
enzyme(s)
Receptors
[G protein coupled)
? opens voltage-gated
Ca 2+ channels
? activates PLC
;:l
Contraction
(slow onset,
long-acting, potent)
ET-l
ET-3
ET! '\T"
:0
~
In anterior
pituitary cells only
contraction
relaxation
Fig. 7. Diagram of pathways for endothelin (ET) synthesis and actions on ETA and ET B receptors.
phospholipase C
TGB~
~;
PLC
the blockade of the ET system would decrease vasospasm. ET-l production also is normally under inhibition by NO which if lost after SAH could further
enhance the effects of the ETs, perhaps in the absence
oflarge changes in ET mRNA or protein.
Nitric Oxide
38
B. Weir et al.
Endothelial
Neuronal
Inducible
Location
endothelial cells
membrane associated
calcium-calmodulin
tetrahydrobiopterin
NADPH
constitutive
neurons
cytosolic
calcium-calmodulin
tetrahydrobiopterin
NADPH
constitutive
picomolar levels of NO
picomolar levels of NO
Cofactors
Activity
~rg0inine~
;--
::
'4
NADPH
- acetylcholine
- serotonin
acts on
cell membrane
receptor
- substance P
- adenosine nucleotides
bradykinin
histamine
A23187
arginine vasopressin
Fig. 8. Diagram of pathway for NO synthesis. Some forms of NO synthase require Ca++ and calmodulin
39
Free Fe2+/FeJ+
(Fenton catalysis)
Auto-oxidation of hemoglobin
Inftammation
leukocyte myeloperoxidase
..
~ .NO,!.OH
t
Arachidonic Acid
Metabolism
- 5-Upoxygenase
- Prostaglandin Synthase
---- .. ? Apoptosis
~
~
1'--- W
ONOo-
~O;
proteins~
~~
contractile proteins
regulatory proteins
suchasmembrnne
ion channels
~\1
Cell Membrane
NO
Cell Death
Free Radicals
A free radical is any molecule with an unpaired
electron in its outer orbital. This renders the molecule
very reactive in that it will donate (reduce) or remove
(oxidize) electrons to or from other biological molecules. This alters that molecule's chemical properties,
may create other reactive species, and may alter the
biological function of that molecule. Most free radicals
of biological importance are oxidizing agents. There
are a number of sources of free radicals after SAH
(Fig. 9) but the principle process in vasospasm is
probably the spontaneous oxidation of oxyhemoglobin to methemoglobin in the subarachnoid space,
leading to production of 02~. The oxygen-derived
radicals include superoxide (02~), hydroxyl (OH') and
hydrogen peroxide (H202). H202 is not a free radical
but is a reactive oxygen species capable of reacting
Fe++ + H 202
--+
Fe+++
+ OH' + OH-
40
B. Weir et al.
Vasospasm
angiographic
clinical
33%
30%
33%
Outcome
good recovery or
moderate disability
dead
Comments
13%
70%
82%
90%
71%
8%
5%
20%
66%
66%
64%
71%
21%
19%
22%
12%
73%
66%
71%
16%
16%
injurious frec radical reactions. Products of hemoglobin metabolism such as bilirubin may actually be antioxidants [48]. Finally, the body has natural defences
against free radicals, including the enzymes superoxide
dismutase, catalase and glutathione peroxidase and
other compounds such as vitamin E (a-tocopherol),
glucose and some serum proteins. These are not found
in very high levels in CSF, rendering the environment
susceptible to uncontrolled free radical attack. One
feature missing from the free radical story is smooth
muscle contraction. While there is evidence from study
of cardiac myocytes and the role of free radicals in
myocardial reperfusion injury, there is little to suggest
how the above noted reactions might cause contraction [48]. Although free radicals were shown to mediate changes that might cause contraction in smooth
muscle [84] and injection of large doses of lipid peroxides into the CSF caused arterial narrowing, there
also are reports of how free radicals cause vasorelaxation [4, 48]. On the other hand, lipid peroxidation theoretically damages cell membranes making
them more permeable to ions such as Ca++ which
would cause contraction.
There is abundant evidence that free radicals are
formed in the subarachnoid space after SAH in animals and man. Free radicals can be detected by direct
methods such as electron spin resonance spectroscopy,
chemiluminescence or by reaction with spin-traps
to produce stable products. All studies of vasospasm
have used indirect measurement of products of free
radical reactions, principally lipid peroxide levels
13%
41
42
There may be changes in gene expression in the cerebral arteries and in the brain after SAH. The changes
in the brain may be secondary to ischemia or to subarachnoid blood. In general, the change that is ultimately important is a change in the protein product of
the gene. Thus, changes in protein levels may be
measured. Changes in levels of the mRNA, the stability of the mRNA, or in the rate of transcription of the
gene of interest might also be determined. A particular
physiological or pathological system known to mediate vascular tone might be assessed or a method to
look at changes in a variety of gene products, such as
mRNA differential display, might also be used.
In the spastic arteries, changes in gene expression
have been assessed by studying changes in genes that
are thought to modulate vascular tone. These are reviewed above under sections pertaining to the system
in question. Several investigators used mRNA differential display to examine genes whose expression is
altered during vasospasm. Seven days after SAH in the
double hemorrhage dog model, there were 16 mRNAs
that were altered compared with normal dog basilar
artery [65]. The control arteries were from dogs that
did not undergo surgery so the effect of surgical stress
cannot be excluded. Six of the 16 mRNAs corresponded to known sequences and all were increased by
SAH. There were 2 stress proteins (BiP protein, protein disulphide isomerase-related protein), 2 protease
inhibitors (inter a trypsin inhibitor family heavy chain
related protein, cystatin protein), I phosphodiesterase
(sphingosine phosphodiesterase) and serum amyloid A
protein. The significance of the findings is uncertain
but a detailed study of changes in mRNA and protein
levels over time might lead to new information on the
pathogenesis of vasospasm.
Other pathways that have been investigated are the
stress gene and hemoglobin metabolism systems (Fig.
B. Weir et al.
The cerebral arteries have sympathetic, parasympathetic and sensory nerves arising from extrinsic
sources in their tunica adventitia and outer tunica
media [27]. These are distinct from the intrinsic system
of neurons arising in the brain parenchyma and in
some way innervating or exerting effects on mainly
intraparenchymal cerebral vessels. The sympathetic fibers release norepinephrine that acts predominately on
a receptors and neuropeptide Y, both of which cause
contraction. Parasympathetic nerves release acetylcholine and the 2 products of the preprovasoactive
intestinal polypeptide (VIP) gene, VIP and peptide
histidine methionine. The action of acetylcholine is
to cause endothelium-dependent relaxation through
release of NO and cGMP and to cause endotheliumindependent contraction probably by direct activation
of muscarinic receptors. The VIP products seem to
relax via a cAMP endothelium-independent mechanism. Sensory nerves containing substance P, neurokinin A and calcitonin gene related peptide (CGRP) the first 2 are products of ~ preprotachykinin and
cause endothelium-dependent relaxation through a
NO mediated pathway whereas CGRP causes endothelium-independent relaxation that is associated with
increased cAMP [13]. In the pial arteries, serotonin is
present but there is controversy as to whether there are
serotonergic nerve fibers or whether the serotonin is
present because of rapid uptake of exogenous serotonin from blood into catecholaminergic nerves at the
time of tissue processing [8, 27]. ATP may be released
from sympathetic nerves and causes endotheliumdependent relaxation and endothelium-independent
contraction [99]. Other neuropeptides that may modulate cerebral blood flow have been identified in the
central nervous system but they arise from brain
Acknowledgements
The authors thank Lydia Johns for preparing the figures.
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46
88.
89.
90.
91.
92.
93.
94.
Summary
An understanding of the hemodynamics of cerebrovascular spasm
following subarachnoid hemorrhage is important for the diagnosis
and treatment of this potentially dangerous condition. An overview
model is presented which includes the main elements determining the
overall effect of vasospasm. The model included realistic pressureflow-velocity-diameter relationships encountered in a geometry resembling that of vasospasm of the middle cerebral artery. Viscosity
was adjusted to that expected of human blood. Furthermore, a realistic model the cerebral autoregulation was included. The effects of
induced hypertension as well as hypotension were studied.
It was found that the friction pressure loss in the spastic segment
was 3.5 times as high as that predicted by using the Hagen-Poiseuille
formula. The reason for this discrepancy was probably the 'inlet
length effect' considerably increasing the friction. Furthermore, including the Bernoulli kinetic pressure energy, a formula was proposed that accurately described the experimental data.
From this hemodynamic perspective, strong support was found
for the present trend to use aggressive hypertensive therapy in patients with vasospasm. The results also confirmed that TCD velocity
measurements in the spastic segment when taken alone may not be a
good index of the degree and effect of the spasm. These measurements must be combined with other techniques such as extracranial
Doppler or CBF to assess the degree of spasm.
Keywords: Cerebrovascular spasm; hemodynamics; subarachnoid
hemorrhage; transcranial Doppler.
"Hence it plainly appears, that there is a communication between the
Vessels watering the whole Head; and although every Artery is carried
to one only Region, as its peculiar Province, and provides for it apart;
yet, lest that any part should be deprived of the influence of the blood,
more ways lye open to every part by the ingraftings of those vessels; so
that if the proper vessels by chance should be wanting in their office, its
defect may perfectly be compensated by others neighbouring. "
Introduction
The work of Willis [36] is remarkable not only for
the artistic and detailed anatomical drawings - but
even more so by the apt functional description of the
48
R . Aaslid
Uenous
Sinus
Jugular
Uein
Fig. 1. Schematic drawing of the cerebral circulation with vasospasm affecting the middle cerebral artery (MCA). Abbreviation:
ABP arterial blood pressure; cABP cerebral arterial blood pressure;
rABP regional (post-spasm) arterial blood pressure; ICP intracranial pressure; CVP central venous pressure; ICA internal carotid
artery; ACA anterior cerebral artery. See text for description
49
[Equation 1]
50
R. Aaslid
= 0.057r . Re
Bemoulli
Bemoulll l. SPoI_me
[Equation 4]
Po lseume
[Equation 5]
II1l
1 HgI
+ F k 8I!Lj (nr4 )
[Equation 7]
51
350
150
DiaMeter:
2. DAM
1~_Ar_fon_ad
1. 5 MM
_ __
120
300
~,:'O"
.~
E:
.....
"E:
250
90
200
E
E
CI
.....
...J
....
z:
150
...J
100
::::I
CI
:::0
1. 0 MM
250,
60
200
~ E.~
150
50
J1
i L.1
PaCO,33
100
50
\'
~\AN
[MMHg]
Cerebral Autoregulation
The mechanism that maintains a constant cerebral
blood flow (CBF) within a wide range of perfusion
pressures is called cerebral autoregulation. The first
studies in humans [17] documented that this mechanism was remarkably effective. Perhaps one of the
most illustrating examples of the ability of this mechanism to maintain constant flow in situations where
52
R. Aaslid
300
"
250
"
200
.....
....
150
==
.....
100
.~
.....
"
3
C
....
:z:
50
0
50
CEREBRAL PERFUSION
100
150
PRESSURE [MMHg]
53
""
on
RBP: 140
200
150
~
""-'w
=>
'"
""
...-'
100
50
250
"
:::;"
.~
200
~
3
~
""
=>
'"
5:>
150
100
50
3.0
0.5
3.5
54
before it enters the skull) to get a more complete assessment of the effects of cerebral vasospasm. We also
proposed that the rate of velocity increase per day in
the first stage of vasospasm - when flow is not yet reduced - might be a better prognostic index that absolute velocities at later stages. Lindegaard et al. (19)
proposed to use the VMCA/V'CA index - i.e. the ratio
between these velocity readings - to assess the severity
of the spasm. This was found to correlate much better
than velocity alone to the degree of spasm as seen on
angiography. Other groups have used CBF measurements combined with TCD to assess both flow and
velocity [IS, 20, 2S]. In spite of these findings and
ignoring the basic hemodynamic principles, many
authors continue to evaluate cerebral vasospasm based
on the intracranial velocity measurement alone. The
addition of at least a careful measurement in the extracranial ICA - which only takes a few minutes to
perform with the same TCD equipment (3) - allows a
more accurate evaluation of the degree and the effects
of vasospasm.
It should be noted that the upper panel in Fig. 6
shows the cross-sectional mean velocity within the
lumen. TCD is normally used to measure maximum
velocity, which is somewhat higher than the mean. The
relationship between the two is complicated in a short
segmental narrowing where parabolic velocity profiles
have no chance to develop, and the complex problems
of blunt velocity profile flow are outside the scope of
this chapter.
R. Aaslid
250
"
~
200
..,
=
.......
150
=>
'"'
=
....
RBP: 140
100
50
250
."
-.
.....
200
....=
150
=>
....
100
...
=
=>
50
0.5
1.0
1.5
2.0
2.5
3.0
3.5
Fig. 7. Influence of collateral circulation via leptomeningeal anastomoses as schematically illustrated in Fig. I on the total flow and
the velocity in vasospasm. Compared to Fig. 6 which shows these
relationships without such collateral circulation, the main effect is an
increase in total flow at the most severe degrees of spasm, as well as a
decrease in the maximum velocities encountered. Note strong effect
on simulated induced hypertension on maintaining flow at the most
severe degrees of spasm (diameter less than 1 mm)
levels which are typically compatible with tissue survival. Again this is hemodynamic evidence for potential beneficial effects of such therapy.
The effects on the velocity are not nearly as marked,
but the maximum velocities do drop from 240 to just
under 200 cm/s for the hypertensive example. If the
collateral circulation originates form the ACA and
the spasm is in the MCA, the VMCA/V'CA index may
underestimate the actual degree of spasm as seen on
angiography because MCA velocity will be lower and
the ICA velocity (and flow) will be higher than without
collaterals.
55
..
250
E
0
200
.....
)0-
150
-1
00
SO
,.>
-'
u-
"
2000
1000
)0-
W
Z
a=>
w
a::
u-
0
1000
2000
Fig. 8. Spectral display of a musical murmur (lower) and the Doppler signal (upper) from a 54 years old male patient with an aneurysm of the anterior communicating artery. The recording was made
from the right middle cerebral artery, slightly distal of the bifurcation of the internal carotid artery. Three sound modes are recognized
in the lower tracing: A systolic bruit (1 ) , a musical murmur displayed as a narrow hand in early diastole (2) , and a silent phase in
late diastole (3). The second harmonic of the musical murmur is also
seen in the recording, this is probably an artifact from the ultrasonic
modulation/demodulation process. From Aaslid and Nornes [5] Fig.
2, reproduced with permission
the signal can be associated with an anatomicallocation. In the case of Fig. 8 it occurred in the vicinity
of, and distal to the high-velocity jet in the spastic
segment.
This example shows no such bruits during the latter
half of the cardiac cycle with the lowest flow velocities.
This also means the lowest Reynolds numbers and the
highest stability of the flow. The complete absence of
bruits suggests laminar flow in this regime. In contrast,
during systole, the bruits are characteristic of most
vascular sounds having a broad-banded noisy character. These are indicative of random chaotic vortex
formation which is generally recognized as turbulence.
This phenomenon occurs during the highest Reynolds
numbers, indicating the flow being the least stable.
An interesting phenomenon of a musical murmur
occurs in the transition of the turbulent and the laminar flow regimes. In the spectral analysis it is seen as
a narrowing of the spectral bruit into single spectral
lines. The frequency of the sound is proportional to
the velocity, even reproducing the dicrotic notch. Vortex shedding in jets coming from nozzles are characterized by the dimensionless Strouhal number StD:
[13]
StD=2fr/V
Equation [8]
In SAH patients with musical murmurs, the frequency (f) of the first harmonic of the murmur divided
by the velocity was 2.35 [5]. The Strouhal number most
conducive to periodic vortex shedding is 0.4 according
to Hussain [13]. For this value, the diameter of the
corresponding nozzle was 1.7 mm to match the relationship between frequency and velocity observed in
our patients. This is very close to what we would expect in terms of vasospasm in this group of patients
given the increase in velocity observed. So the most
likely explanation for the relatively frequent musical
murmurs in SAH patients is the flow stability becoming neutral or borderline unstable favoring shedding of
a von Karman vortex street. These regularly spaced
vortices in turn impinge upon the wall of the postspastic segment, setting up the vibrations which can be
detected as the musical murmur. If the Strouhal number for vortex shedding can be verified for this situation, this phenomenon opens up an intriguing possibility for accurate determination of vessel diameter in
cerebral vasospasm. However, this has limited clinical
application since it can only be used in those patients
(about 40%) who exhibit such murmurs.
56
Conclusions
R. Aaslid
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455-460
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(1989) Cerebral vasospasm diagnosis by means of angiography
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12-24
20. Martin NA, Patwardhan RV, Alexander MI, Africk CZ, Lee
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transcranial Doppler flow velocities after severe head injury:
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123-127
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263-330
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57
35. Tiecks FP, Lam AM, Aaslid R, Newell DW (1995) Comparison
of static and dynamic autoregulation measurements. Stroke 26:
1014-1019
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Montreal
Correspondence: R. Aaslid, University of Washington, Department of Neurological Surgery, Harborview Medical Center, Seattle,
USA.
Summary
Introduced 15 years ago, transcranial Doppler (TCD) recordings
of blood velocity in patients with recent subarachnoid haemorrhage
(SAH) have two objectives: to detect elevated blood velocities suggesting cerebral vasospasm (VSP) and to identify patients at risk for
delayed cerebral ischemic deficits (DID). The pathophysiological
cascade causing DID is complex. Discrepancies between blood velocities and DID (presuming that there actually is an "ischemic
threshold" for blood velocity in absolute terms, which seems most
unlikely) have been demonstrated, particularly in patients with elevated intracranial pressure (ICP) levels. Furthermore, the vessel
showing the highest blood velocity is not always the one perfusing
the area where ischemic symptoms arise, nor does the site of the
greatest subarachnoid blood clot always relate to the ischemic brain
region. Moreover, it is probable that the complex haemodynamic
changes following SAH and the subsequent development of VSP
may be underestimated if only considering the crude intracranial
artery blood velocities. Cerebral blood flow measurements combined
with TCD to assess both flow and velocity have emphasised this
point. Despite these findings and ignoring the basic principles of cerebral haemodynamics, cerebral vasospasm is still being assessed
from the intracranial velocity measurement alone. The addition of at
least a careful measurement from the extracranial internal carotid
artery - using the same TCD equipment and taking only a few short
minutes to perform - allows a much more accurate assessment of the
degree and the effects of vasospasm.
This probably explains why the clinical value of TCD is still debated. There is still uncertainty as to the best method to prevent and to
treat VSP, and the overall outcome after SAH depends on so many
factors besides VSP. Conclusive evidence may therefore be hard to
obtain, and it appears sound to conclude that even with advanced
investigation technology available, proper selection, pre- peri- and
postoperative care and timing of surgery remain cornerstones in the
management of these patients,- equal in importance to their treatment in the operating room or in the interventional angiography suite.
Introduction
60
K.-F. Lindegaard
[Equation la]
thus:
YMCA
and:
VrCA
[Equation lc]
Const (DMCA)-2
[Equation 2]
61
Comparing angiograms and blood velocity recordings in 80 patients with SAH we found that compared
with the MCA blood velocity, the hemispheric index
showed less variation with age and gender [59]. This
agrees with studies in normal persons [8, 28]. With
angiographical VSP of the MCA mainstem scored as
severe, moderate, suspected, or absent, the better correlation was obtained with the hemispheric index,
suggesting an index of> 3.0 as denoting the presence
of angiographical MCA spasm, with values :2: 6.0 indicative of severe VSP [58, 59].
The advantage of the index was most evident in
patients in poor clinical condition, Grade III-IV [39].
Some of these patients had a YMCA about 120 cm . s-1
despite severe angiographical MCA spasm. In these
patients the VrcA was very low, about 20 cm . s-l,
suggesting reduced hemispheric blood flow, nonetheless the VMCA/VrCA index was about 6.0. We
interpret this as confirming that the hemispheric index
adds relevant information, and therefore maintain that
to reduce misjudgement it is essential to obtain an
insight into the blood flow in the artery system of
interest.
62
Distal Cerebral Artery Spasm
K.-F. Lindegaard
YMCA ~
63
anterior and posterior cerebral arteries as well. To obtain a better insight into the haemodynamics of DID it
is therefore important to consider the circle of Willis
and its inlets and outlets as a system having the potential for redistributing the blood flow to the neuronal
pool. The average hemispheric index, i.e. the average
of the ipsilateral MCA and ACA values suggested by
Sekhar et al. [91] may be useful. Jakobsen's spasm index (VMCAjCBFMCA) is very interesting, but sacrifices
the technical simplicity and the short response time,
which are important advantages with the stand-alone
TCD approach.
Indices of Pulsatility
Two studies have addressed specifically the pulsatility of the blood velocity signal in VSP. Steinmeier et
at. [97] found an inverse relationship between the
VMCA and the pulsatility index, PI or
(Vsystolic -
Vdiastolic) / V mean,
Vdiastolic) / Vsystolic.
64
K.-F. Lindegaard
Comparisons with angiograms are necessary to validate the TCD findings [5, 35, 91]. Three studies have
questioned the sensitivity of TCD to detect VSP, particularly following rupture of aneurysms on the anterior cerebral artery complex [15, 52, 79]. However, in
order to assess how TCD and angiographical findings
correlate (using angiography as the standard of reference) we need answers to the following questions:
1. How should angiographical VSP be defined, and
2. how accurate is the assessment of VSP from the
angiograms?
1. Standardised measurement points for basal brain
arteries have been devised [24], but these points may
not coincide precisely with the narrowest vessel segments in VSP. The calibre of cerebral arteries is individually variable, and the assessment of angiograms
obtained after an SAH is difficult since only very exceptionally will patients with recent SAH have had
angiography performed before the bleed. It therefore
seems realistic to assume that when comparing with
the corresponding vessel on the other side, only diameter differences exceeding 20% will be recognised [98].
Diffuse VSP, involving all basal cerebral arteries, will
complicate this estimation.
2. Two studies have addressed the issue of interobserver variability in reading angiograms using
Kappa statistics (the correlation of categorical data
with correction for agreement occurring by chance).
Eskesen et al. [21] confirmed that two independent
judges may read one and the same angiogram very
differently. This may explain why the reported incidence ofVSP after SAH shows considerable variation:
from 21 to 78% [12]. Even when angiographic VSP is
evident, deciding if it is moderate or severe may be intricate. Hence, Lindegaard et al. [59] found agreement
between two independent judges (neuroradiologist and
neurovascular surgeon from the same institution) in
lO5/124 hemispheres (Kappa = 0.67 or good agreement) for VSP of the MCA and in 62/124 (Kappa
= 0.43 or moderate agreement) for the ACA. There
seem to be no reports on intra-observer variability.
Since the assessment of angiograms by eye is categorical (VSP being present/absent or either severe,
moderate, mild or absent) while blood velocities and
velocity indices are reported on continuous scales,
these two methods of evaluation are difficult to reconcile. It may be suggested that at least for research purposes judgement by eye should be replaced by measurements of the contrast-filled column on angiograms
and corrected for magnification [18]. This would be
65
66
Special Considerations
K.-F. Lindegaard
Clinical Implementation
Microsurgical Aneurysm Clipping
67
68
K.-F. Lindegaard
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(1991) Cerebral vasospasm evaluated by transcranial Doppler
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Correspondence: K.-F. Lindegaard, University of Oslo, Department of Neurosurgery, Rikshospitalet, The National Hospital, N0027 Oslo, Norway
Abstract
This paper briefly reviews some basic principles of neurosurgical
intensive care of patients with aneurysmal subarachnoid hemorrhage. The importance of early identification of secondary insults are
underlined. Special attention is paid to the newly introduced method
for neurochemical monitoring by means of intracerebral microdialysis. It is concluded that a well functioning neurointensive care
unit constitutes an important organisational frame for the detection,
prevention and treatment of secondary insults, after aneurysmal
subarachnoidal hemorrhage and that improved results can be expected by applying a modern neurointensive care strategy also for
patients with aneurysmal subarachnoid hemorrhage.
Keywords: Neurointensive care; subarachnoid hemorrhage; intracranial hypertension; intracerebral microdialysis.
Introduction
Neurointensive care (NIC) has emerged into a subspeciality of the clinical neurosciences and is an integrated part of neurosurgery, neurology and anaesthesia. NIC should be viewed upon as a general
concept, or an organizational frame for patient care,
rather than a specific mode of treatment. The scientific
rationale for NIC is that permanent brain damage
after a number of acute neurosurgical and neurological
disorders, to a greater or lesser extent, are caused by
secondary insults, which mainly are the result of disturbances of the intracranial dynamics (i.e. intracranial pressure, cerebral blood flow, cerebral metabolism) set in motion by the primary event. NIC is thus
devoted to the control of the intracranial dynamics
and emerged from research and clinical management
of traumatic brain injury (TBI). Registration of the
intracranial pressure (ICP) in clinical practice and the
use of artificial hyperventilation [14,15] were the basic
methods forming NIC. Clinical research on TBI also
formulated the concept of "secondary insults" and
most important was the observation that they to a
74
Increased lep
Rebleeding
- ICH
-IVH
Hydrocephalus
Oedema
Seizures
Pyrexia
Decreased CBF
---+-
I. Increased lep
0Chaemi"'0 .....--1 .
1/
Hypoxaemia
aSAH, the ICP may reach the level of the mean arterial
blood pressure, thereby causing a brain circulatory
arrest and global cerebral ischemia [9, 17, 18]. About
15% of the aSAH population are thought to die instantly by this mechanism [13, 25]. In most cases
though, intracranial compensatory mechanisms, e.g.
CSF movement to the spinal canal allows the ICP to
decrease and the brain circulation to return. [16].
However, a global ischemic insult causing brain damage of varying degree appears to develop in most cases
and its severity is clinically reflected by the initial loss
of consciousness. Figure 2 shows two CT scans in a
patient with a severe aSAH, who survived the initial
bleed, but died a few days later as a direct consequence
of the rupture. Note the widespread cortical lesions
apparently caused by global ischemia. It has also been
hypothesized that this initial primary global insult
renders the brain susceptible to subsequent ischemic
insults. This means that the initial effects of the bleed
may increase the risk for cerebral infarction when
delayed arterial vasospasm and/or other secondary
insults emerge (Fig. 2) [12, 28, 29, 30].
Acute Hydrocephalus
Intracranial Hematoma
About 20% of the patients with aSAH have an expansive intracerebral hematoma (ICH) and sometimes
an aneurysm rupture also causes a subdural hematoma
(SDH). Both ICH and SDH may give raise to intracranial hypertension and global ischemia. Moreover,
an intracranial hematoma may produce focal cerebral
ischemia and it is a rather common observation that a
large infarction of the affected MCA territory follows
after a Sylvian hematoma from a ruptured ICA or
MCA aneurysm. One should also note that an expanding cerebral infarction also may lead to intracranial hypertension. Intraventricular hemorrhage,
which occurs in about 15% of aSAH patients [2], is
75
Fig. 2. CT-scans obtained immediately upon admission (upper row) and about 18 hours later (lower row) in a patient with severe aneurysmal
subarachnoid hemorrhage. Note the widespread cortical ischemic lesions on the second scan
About 20% of the aSAH patients are thought to develop seizures at the time of hemorrhage or soon after.
It is difficult to differentiate between true epilepsy and
other form of jerks, perhaps related to disturbed brain
stem function. However, epileptic seizures increase
CBF and cerebral blood volume and may cause intracranial hypertension, if compensatory mechanisms are
exhausted. Furthermore, seizures increase cerebral
metabolism and oxygen demand, and this mechanism
may also aggravate cerebral ischemia.
76
Neuromonitoring
Systemic Insults
Already Crompton noticed that arterial hypotension in the acute phase after SAH was a risk factor
for cerebral infarction. There are extensive experimental and clinical evidence that hypotension aggravates cerebral ischemia. Hypovolemia is not an
uncommon finding in the aSAH patient and this
may increase the risk that sedative and narcotic drugs
elicit hypotension. Nimodipine has potent hypotensive
properties when given intravenously, and drastic hypotension may follow the institution of this therapy.
The role of hypoxemia has not been studied in detail
77
78
Excitotoxicity
Membrane degradation
Oxygen radicals
glucose
lactate/pyruvate ratio
lactate/glucose ratio
hypoxanthine
glutamate
aspartate
glycerol
hypoxanthine, xanthine
uric acid and its oxidation products
(e.g. allantoin)
Biochemical markers with potential value for clinical use in neurosurgical patients with intracerebral microdialysis. The left column
indicates the phenomena the markers are reflecting.
Discussion
NIC Treatment
79
brain, may in selected cases aggravate cerebral ischemia and elicit infarction.
Increased ICP due to CSF resorption disturbance is
common and several studies have demonstrated clinical improvement after CSF drainage. An advantage of
CSF drainage appears to be that more patients become
amenable to surgery because the preoperative neurological condition may improve or deterioration is
avoided. CSF drainage of patients with untreated
aneurysm is somewhat controversial, because the risk
of rebleeding may be augmented by drainage. However, we found no association between more abundant
use of preoperative CSF drainage and rebleeding [2].
Expansive hematoma is an important cause of intracranial hypertension and swift evacuation is paramount. In some patients, ICP-registration is used to
define the surgical indication. In unconscious or severely obtunded patients, intubation and artificial
ventilation secure airway control and oxygenation.
There is no data available propagating regular hyperventilation and generally moderate hyperventilation or
normoventilation is used. In life-threatening intracranial hypertension, the use of hyperventilation,
mannitol, barbiturates, induced hypothermia, and
surgical decompression with removal of expansive
cerebral malacic tissue is warranted. Recently, hemicraniectomy has been proposed to counteract intracranial hypertension from large and expansive infarctions in the MCA-territory.
Treatment of vasospasm is a central part of NIC. It
is our general impression that vasospasm is less of a
problem today and there may be several explanations
for this. One is probably the use of nimodipine. Moreover, the NIC unit provides a better environment for
the overall care, especially in detecting and preventing
other secondary insults, such as increased ICP, hypotension, hypoxemia, pyrexia etc, which probably also
are involved in the development of delayed ischemic
deterioration. The NIC environment also enables safe
use ofhypervolemia-, hemodilution- and hypertension
therapies. Newer methods such as angioplasty and intraarterial papaverine infusions may in selected cases
also playa role in reducing the effects of vasospasm.
In conclusion, a well functioning NIC unit constitutes an organizational frame for the detection of
secondary insults and can mobilize the personal resources which is a prerequisite for successful treatment. During the last years new pharmacological
agents for neuroprotection against ischemic brain
damage have been developed and given hope that
80
9.
10.
II.
12.
13.
14.
15.
16.
17.
18.
19.
Keywords: Aneurysm clip; cerebral aneurysm; computed tomography; magnetic resonance imaging; titanium alloy.
There is little doubt that a small percentage of aneurysms is not adequately eliminated after surgery and
might rebleed sooner or later [6, 9, 11]. Routine postoperative digital subtraction angiography (DSA) is
certainly charged with a non-negligible rate of morbidity due to the fact that these exams have to be performed during the phase of vasospasm. Delaying DSA
until after vasospasm, which means for 3 to 4 weeks,
cannot be the answer since an incompletely clipped
aneurysm might already have re-ruptured within the
waiting period. Recent improvements of MRA and
CTA as well as the availability of titanium aneurysm
clips potentially render these methods non-invasive
alternatives to DSA for postoperative control [1, 3, 4,
10, 14, 15, 16, 17]. Therefore we introduced titanium
alloy aneurysm clips (Aesculap AG, Tuttlingen,
Germany) into clinical routine in 1995 [2, 5, 7, 8, 12,
13]. In the meantime over 300 patients have been
treated using titanium alloy clips. The purpose of the
actual report is to describe the CT and MR imaging
properties as studied initially and to review our clinical
expenence.
Introduction
Summary
This report describes the imaging characteristics of titanium alloy
aneurysm clips and our clinical experience with these clips in more
than 300 patients. Phantom and clinical investigations showed that
clip artifacts on CT and MR are minor as compared to the cobalt
alloy clips used previously. Spiral CT angiography (CTA) in combination with titanium alloy clips could be shown to be a feasible mode
of postoperative control and can be used to determine completeness
of aneurysm elimination, patency of adjacent arteries as well as vasospasm. In contrast, magnetic resonance angiography (MRA)
proved to be unfeasible as a method of postoperative vascular
imaging since the titanium clips still produce a shadow in the order of
size of the entire aneurysm. Therefore, completeness of aneurysm
elimination cannot be judged on magnetic resonance angiography.
The clinical experience in more than 300 cases showed that the titanium alloy clips essentially performed well. However, the limits of
elastic deformation appear to be somewhat inferior to cobalt alloy
clips. The standard appliers do not open the blades of the titanium
clips quite as far as with the comparable cobalt alloy clips and the
corresponding appliers. Therefore the titanium aneurysm clips are
not quite as well suited for large broad based aneurysms. Furthermore, the increased susceptibility of the new clips with regard to
abuse suggests to follow the recommendations of the manufacturer
not to recycle and re-sterilize clips that have been tried but not permanently implanted.
82
titanium would be reached. Since TiAI6V4, as far as
body compatibility, corrosion resistance and reaction
in the MR surrounding are concerned, is comparable
to pure titanium, the use of the alloy with the higher
mechanical characteristics appears preferable in order
to guarantee the required properties.
The alloy TiAI6V4 is a so-called a + ~ alloy, which
is used as basic material for the manufacturing of clips
in form of annealed, extended wire. The annealing
procedure is used to create a homogenous equiaxial
texture. Phase a shows a hexagonal crystal structure
with a grid distance of a = 0.2925 nm, and in the c-axis
a distance of 0.4670 nm which results in an axis ratio of
1.58. This axis ratio is markedly lower than that of
other hexagonal metals such as zinc and magnesium.
The cubical surface centred ~ phase has a grid constant
of approx. 0.3 nm.
According to ISO 5832-3, the material has to meet
the following characteristics:
The tensile strength has to be a minimum of 860
MPa.
The 0.2% extension stress has to be above 700 MPa.
The failure extension has to be a minimum of 8%.
The elastic modulus is in the range of 110 GPa.
CT Imaging Properties
In order to evaluate the streak artifacts on CT, titanium alloy mini clips and titanium alloy standard clips
were compared to the corresponding cobalt alloy clips.
The clips were mounted on a plastic phantom in such
a way that the clip blades were perpendicular to the
standard axial imaging plane. The material density
was compared at the level of the springs and at the
level of the blades (Fig. 1). The CT images using standard cranial window and level settings did not show
any streak artifacts with this strictly orthogonal clip
orientation, neither with titanium nor with cobalt alloy
clips. Therefore, even with cobalt alloy clips, streak
artifacts are only observed if the longitudinal axis of
the clips lies more or less within the imaging plane.
However, the contrast intensity of the titanium alloy
clips was substantially less prominent than the contrast
intensity of the cobalt alloy clips. The contrast intensity
of a standard titanium alloy clip grossly corresponds to
the contrast intensity of a cobalt alloy mini clip.
In order to assess the artifacts during practical use, a
number of patients with similar aneurysms and identical clip sizes, who had either been treated using titanium or cobalt alloy clips, were matched and po stop-
Fig. I. Phantom CT imaging density study with standard and minititanium and cobalt alloy clips mounted perpendicular to the image
plane. Outer circle: optical image and clip designation. Inner circle:
corresponding CT image with the imaging plane through clip blades.
Titanium alloy clips are significantly less dense. Note: streak artifacts
are not noted with either alloy with this clip orientation
83
Fig. 2. Similar ruptured middle cerebral artery aneurysms (A, B) clipped with titanium or cobalt alloy mini clips. (C) Postoperative CT of A (2
titanium mini clips). (D) Postoperative CT ofB (1 cobalt mini clip). Note: streak artifacts occur only with cobalt alloy clips
84
Fig. 3. Ruptured anterior communicating artery aneurysm as visualized with magnetic resonance (MRA) and spiral CT angiography (CTA)
prior to surgery and after clipping with a titanium alloy mini clip. (A) Preoperative MRA. (B) Preoperative CTA. (C) Postoperative MRA.
Note: clip shadow obscuring the area of interest. (D) Postoperative CTA showing aneurysm elimination and vasospasm in the right A2 segment
artifacts. The CTA proved to be sufficient for postoperative determination of all these parameters (Figs.
3-5). In contrast, the titanium alloy clips resulted in a
shadow on the MRA images extinguishing at least the
area of the aneurysm neck and sometimes the entire
aneurysm (Fig. 3). From these results it was concluded
that at the present stage CTA is a viable alternative to
DSA for postoperative control in patients treated with
titanium alloy aneurysm clips while these clips do not
allow adequate vascular imaging by MRA.
85
Fig. 4. CT A of small ruptured basilar bifurcation aneurysm and postoperative CTA control. (A, B) 3-D surface reconstructions of aneurysm.
(C, D) Two different projections of the postoperative control after clipping with titanium alloy mini clip
86
Fig. 5. Giant unruptured carotid bifurcation aneurysm. (A) Preoperative DSA. (B) Preoperative contrast CT. (C, D) Postoperative contrast
CT demonstrating aneurysm elimination (titanium standard clip)
87
Fig. 6. Example of practical use of titanium alloy clips in a case of multiple aneurysms. (A) Vertebral DSA showing small ruptured aneurysm
at the right P I/P2 junction (arrow). (B) Right carotid DSA showing incidental middle cerebral artery aneurysm (arrow) and incidental small
carotid artery aneurysm (arrowhead). (C) Dissected neck of the ruptured right PI / P2 aneurysm through transsylvian approach and (D) application of titanium mini clip. (E) Complex right middle cerebral artery trifurcation aneurysm and (F) combined treatment by polytetrafluorethylene ( PTFE) wrap and titanium mini clip. (G) Small carotid aneurysm clipped with titanium mini clip. (H) Postoperative CT showing two
clips on this slice
88
H.-J. Steiger and J. J. L. van Loon: Virtues and Drawbacks of Titanium Alloy Aneurysm Clips
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5. Kato Y, Sano H, Katada K, Ogura Y, Ninomiya T, Okuma I,
Kanno T (1996) Effects of new titanium cerebral aneurysm clips
on MRI and CT images. Minim Invasive Neurosurg 39: 82-85
6. Kassell NF, Torner JC, Haley EC Jr (1990) The international
cooperative study on the timing of aneurysm surgery, part I:
overall management results. J Neurosurg 73: 18-36
7. Lawton MT, Ho JC, Bichard WD, Coons SW, Zabramski JM,
Spetzler RF (1996) Titanium aneurysm clips, part I: mechanical,
radiological, and biocompatibility testing. Neurosurgery 38:
1158-1164
8. Lawton MT, Heiserman JE, Prendergast VC, Zabramski JM,
Spetzler RF (1996) Titanium aneurysm clips, part III: clinical
application in 16 patients with subarachnoid hemorrhage. Neurosurgery 38: 1170-1175
9. Macdonald RL, Wallace MC, Kestle JRW (1993) Role of
angiography following aneurysm surgery. J Neurosurg 79: 826832
10. Marchal G, Bosmans H, Van Fraeyenhoven L, Wilms G, Van
Hecke P, Plets C, Baert AL (1990) Intracranial vascular lesions:
optimization and clinical evaluation of three-dimensional timeof-flight MR angiography. Radiology 175: 443-448
11. Mayberg MR, Batjer HH, Dacey R, Diringer M, Haley EC,
Heros RC, Sternau LL, Torner J, Adams HP, Feinberg W,
Thies W (1994) Guidelines for the management of aneurysmal
subarachnoid hemorrhage. A statement for healthcare professionals from a special writing group of the stroke council,
American Heart Association. Circulation 90: 2592-2505
12. Payner TD, Tew JM Jr, Steiger HJ (1995) Aneurysm clips. In:
Wilkins RH, Rengachary SS (eds) Neurosurgery, 2nd edn.
McGraw Hill, New York, pp 2271-2276
13. Piepgras A, Guckel F, Weik T, Schmiedeck P (1995) Titanium
aneurysm clips and their advantages in diagnostic imaging.
Radiologe 35: 830-833
14. Ross JS, Masaryk TJ, Modic MT (1990) Intracranial aneurysms: evaluation by MR angiography. AJNR Am J Neuroradiol II: 449-456
15. Schmid UD, Steiger HJ, Huber P (1987) Accuracy of high resolution computed tomography in direct diagnosis of cerebral
aneurysms. Neuroradiology 29: 152-159
16. Schwartz RB, Tice HM, Hooten SM, Hsu L, Stieg PE (1994)
Evaluation of cerebral aneurysms with helical CT: correlation
with conventional angiography and MR angiography. Radiology 192: 717-722
17. Tampieri D, Leblanc R, Oleszek J, Pokrupa R, Melan90n D
(1995) Three-dimensional computed tomographic angiography
of cerebral aneurysms. Neurosurgery 36: 749-755
18. van Loon JJL, Yousry TA, Fink U, Seelos KC, Reulen HJ,
Steiger HJ (1997) Postoperative spiral computed tomography
and magnetic resonance angiography after aneurysm clipping
with titanium clips. Neurosurgery 41: 851-857
Correspondence: H.-J. Steiger, M.D., Klinikum Gro13hadern,
Neurochirurgische Klinik und Poliklinik, Marchioninistr. 15, D81377 Munich, Germany.
Summary
A series of 138 patients with 143 carotid-ophthalmic aneurysms
(COAs) have been treated by direct surgical approach over the past
15 years. In 5 cases the COAs were bilateral and in 15 cases either
one or more aneurysms were associated with a COA. Of the 143
COAs, 87 were small, 41 large and 15 were giant. Seventy-four
COAs bled, while 69 were diagnosed either incidentally or else manifested themselves through neurological deficits resulting from compression of the adjacent structures by the aneurysms. Visual deficits
were diagnosed in all the patients with large/giant COAs and in 27
patients with small COAs.
Of the whole series of patients operated on for COAs, 2 died after
surgery. Two patients had endocrinological deficits, 2 had hemiparesis, 36 had the same visual deficits as prior to surgery, whereas in
47 patients the visual function improved. Of all the 138 patients, 96
remained without neurological deficits, and the 36 patients with the
same visual deficits as preoperatively also showed no neurological
deficits after surgery and hence they were able to resume their previous way of life. Vasospasm did not occur in patients with COA(s)
only, but was observed in 6 out of 15 patients with multiple aneurysms where subarachnoid hemorrhage (SAH) had occurred due to a
rupture of an aneurysm other than the COA.
There has been a major change in the surgical approach to COAs,
from the classical pterional intradural approach to the transorbitaltransclinoid and transsylvian approach which is described in this report. The latter approach provides ample space for proximal and
distal control of the internal carotid artery (ICA) and makes it possible to deal with demanding large/giant COAs safely. In the series
presented, there was no case of premature rupture of the aneurysm.
Moreover, since we started using the described approach to COAs,
retraction of the brain has not been necessary, regardless of the size
of the aneurysm.
Keywords: Internal carotid artery; ophthalmic artery; aneurysm;
carotid-ophthalmic aneurysm.
Introduction
Drake described COAs as a specific subgroup of intracranial intradural ICA aneurysms as early as 1968
[13]. However, controversy still exists regarding the
90
V. V. Dolenc
Small (87)
rupture (60)
incidental (27)
finding
Large (41)
rupture (10)
mass effect (31)
Giant (15)
rupture (4)
143
Clipping
Aneurysm
resection and
reconstruction
of the ICA
60
27
Patency of ICA
in follow-up
angiography
New neurological
deficits
22
29
same as
preoperatively
hemiparesis 1
died I
endocrinological
disorders I
hemiparesis 1
endocrinological
disorders I
died I
better than
preoperatively
II
14
20
II
60
27
Visual function
121
22
137
36
47
aneurysms, some authors advocated indirect treatment, i.e. ligation of the common carotid artery [25,
43, 46], while others favoured a direct approach with
complete exclusion of the lesion [1,5, 7, 10,20,22,25,
38, 44, 49, 51]. The development of endovascular
interventional procedures, where the aneurysm is occluded with balloon(s) and/or coils, has challenged the
direct surgical approach [21, 28]. On the other hand,
the surgical approach was made even safer by combining it with the Dallas technique where temporary
occlusion of the ICA is obtained with a balloon proximal to the COA, thus ensuring an easier and safer exclusion of the aneurysm and reconstruction of the ICA
wall [3, 42]. This combined endovascular/surgical
method probably represents the optimum approach as
it enables complete exclusion of the lesion and immediate cure.
Clinical Presentation of COAs and the Diagnostic
Work-up
COAs are presented according to their size, symptoms and signs in Table I. Like other intracranial
aneurysms, COAs mostly manifest themselves with
SAH. When the aneurysm is large, it can produce local
signs i.e. slowly progressive visual deficits due to the
compression of the optic nerve (ON), the optic chiasm
and the optic tract. The extent of visual deterioration (visual field deficits) depends on the size and
location of the aneurysm. Sub-optochiasmatic (Figs.
I b, c) and global sub-optochiasmatic aneurysms
(Fig. Ie) affect the visual apparatus much more than
Ophth. A.
ON
Vz
Ophth. A.
III'IVV,
ON
ICA(AL)
- DR
- PCP
PCP
III
- III
ON
Vz
III IVV,
- PR
Ophth. A.
ON .
ICA(AL)
V2
IIIIVY,
PR
- ICA(AL)
- DR
DR
- PCP
PCP
' III
III
c
Ophth. A.
- PR
ICA(AL)
- DR
Ophth. A.
..-_ IIIIYV,
d
V2
Opnth. A.,
- IIIIVV,
- PR
V2
IIIIVV,
ON
PR
~.~~~!--- - ICA(AL)
- ICA(AL)
- DR
DR
- PCP
' III
Fig. 1. Types of COAs. (a) A small COA, located at the branching of the ICA and the ophthalmic artery, is in most cases inferolateral to the
ON. The initial position of the small COA and the direction of its further growing dictate the type of the COA. (b) A suboptochiasmatic COA,
projecting medially and inferiorly, remains located over the diaphragm sellae and underneath the ICA. This type of COA is known also as
carotid cave aneurysm. (c) A suboptochiasmatic COA projecting inferiorly and posteriorly may reach the hypothalamus and upper brainstem,
thus causing corresponding endocrinological visual, and long tract symptoms and signs. (d) Supraoptochiasmatic COA, projecting posteromedially overlays the visual apparatus and ACA I and compresses the brain when it is large and/or giant. (e) Global COA (suboptochiasmatic) usually displaces the visual apparatus medially and upward by stretching the ipsilateral ON and the optic tract around its sac.
The ACAI also may be stretched and looping around the sac of the aneurysm. The PComA and the anterior choroidal artery may be firmly
adherent to the lateral wall of the aneurysm and nerve III might be stretched and displaced laterally. (f) A suboptochiasmatic COA is clipped
with fenestrated rect-angular Sugita clip. The dural ring is cut circumferentially around the ICA. The ophthalmic artery is visualized. The peripheral part of the aneurysm is resected and excluded and the pressure against the visual apparatus and pituitary stalk is not existing anymore.
Due to the circumferential cut ofthe dural ring and the dissection ofthe AL ofthe ICA from the lateral wall of the sphenoid sinus, the coursing
of the ICA from extradural to intradural space is preserved normal.
In Figs. a- f the completed epidural approach is presented: the orbit is unroofed on the anteroposterior aspect of the sphenoid wing, the
sphenoid wing and the ACP are resected and so are the superior, lateral and inferior walls (the optic strut) of the optic canal. The anteromedial
triangle is wide opened. The dural layer of the lateral wall of the CS is peeled from its anterior part of the lateral wall of the CS so that nerves III,
IV, VI, V2 are visualized. The CS has not been opened. The dura along the Sylvian fissure is cut and the Sylvian fissure is split in its entirety
along the MCA. The bifurcation of the ICA into the ACAI and the MCA, the anterior choroidal artery, the PComA, nerve III, the ON and
different aneurysm(s) are visualized in Figs la through Ie
92
V. V. Dolenc
Fig. 2. A left carotid angiogram, AP view (a) and lateral view (b), demonstrates a giant COA with a large thrombus in it. The large mass of the
lesion caused epileptic seizures whereas aneurysm-to-artery embolisms caused several TIAs and a moderate stroke. Cross-flow studies revealed
significant displacement of the ACAI in the supero-posterior direction and borderline filling of the ipsilateral MCA (c). The postoperative
angiogram, AP view, demonstrates that the ICA after resection of the giant COA and reconstruction of the artery is occluded, but the ipsilateral
ACAI and the MCA are in a good position and are much better filled (d) from the contralateral side than preoperatively (c). The most probable
reason for the postoperatve occlusion of the ICA was that the inner diameter of the ICA was too small since the wall of the aneurysm at its neck
was very thick
93
Carotid-Ophthalmic Aneurysms
The distal segment of the extradural ICA, representing the anterior loop (AL) of the ICA, is situated
infero-medial to the ACP and supero-lateral to the
lateral wall of the sphenoid sinus. After the of the
ACP, the AL of the ICA is exposed from the proximal
ring (PR) to the distal ring (DR) in the antero-medial
triangle [11]. The AL of the ICA is covered with a
dural sheath which makes the PR and distally the DR
around the ICA. The ICA then courses through the
DR into the intradural space where it gives off the
ophthalmic artery on its supero-medial side, underneath the ON. In the majority of cases the ophthalmic
artery originates approximately 1-2 mm distal to
the DR. The ophthalmic artery courses upward and
anteriorly, under the ON, into the optic canal. The
Dawson arteries originate on the inferomedial side of
the wall of the intrathecal ICA. They provide vascularization of the visual apparatus and the pituitary stalk
[6]. The PComA, and more distally the anterior choroidal artery, originates from the lateral side of the
ICA.
According to the definition, COAs are aneurysms of
the intrathecal ICA, arising from the segment between
the ophthalmic artery and the PComA. This definition,
however, only holds if the aneurysm is small (Fig. 1a).
In cases where it is a large aneurysm, the segment of
the ICA involved in the orifice of the aneurysm may
extend either more proximally, i.e. into the extradural
space, or more distally, i.e. beyond the origin of the
PComA, or in both directions. In cases where a large
part of the circumference of the I CA is involved in the
orifice of the aneurysm, the lesion fills most of the
suprasellar space and is classified as a global COA [25].
The surgical approach to COAs, as described initially [10] and re-described later [11], proved - in cases
of large and giant COAs - a rather demanding procedure and was not generally accepted; it was even classified as hazardous [31]. Additional laboratory studies
led to the transorbital, transclinoid and transsylvian
approach to COAs which was published 10 years after
the initial report [12].
The patient and the patient's head is positioned as
in cavernous sinus (CS) surgery. The other initial surgical steps, including the type of skin incision and osteomuscular flap used, as well as the unroofing of
the orbit and the resection of the sphenoid wing, also
follow established guidelines for CS surgery and are
published elsewhere [12]. After the resection of the
medial portion of the sphenoid wing and the roof of
the orbit on the posterior aspect of the superior orbital
fissure (SOF), the dural tent covering the neural structures coursing through the SOF from the CS to the
94
orbit, is dissected free on the antero-medial and posterior side. The dural duplicature is then cut, and a
cleavage line located so that the outer layer of the
lateral wall of the CS is peeled off cranial nerves III,
IV, and VI, and from the inner layer of the lateral wall.
This maneuver provides good access to the the inferolateral aspect of the ACP. Drilling of the ACP starts on
its infero-Iateral side and proceeds in posteromedial
direction. It is performed with a diamond drill and is
carried out in short bursts. After each drilling period
the walls of the hollowed ACP is checked. Continuous
irrigation of the tip of the drill is necessary in order to
avoid over-heating of the drill as this puts cranial
nerves II, III and IV in danger. Hollowing the ACP by
short periods of drilling thus also minimizes the possibility of mechanical injury to the ON, ICA, nerves III
and IV and the aneurysm itself. The optic strut should
be removed in the same manner, care being taken not
to open the sphenoid sinus which may result in a CSF
fistula. The optic canal should be opened on the lateral
and superior aspects. After the removal of the optic
strut the optic canal is also opened on its inferior
aspect and the ICA is exposed along ~ of its lateral
circumference. Additional dissection of the ICA at the
level of the AL from the bone on its medial side (i.e.
from the wall of the sphenoid sinus on medial side of
the artery) will enable placement of a temporary
proximal clip on the AL of the ICA in cases of rupture
of the aneurysm or in cases of difficult dissection and/
or resection of the aneurysm and reconstruction of the
ICA wall.
After the removal of the ACP, exposure of the ON
on the superior, lateral and inferior aspects and dissection of the AL of the ICA from the wall of the
sphenoid sinus, the dura is opened along the Sylvian
fissure. Retraction of the frontal or temporal lobes is
not allowed since it may cause premature rupture of a
large/giant COA. The Sylvian fissure is split from its
periphery along the entire length of the MCA so that
the ICA bifurcation is fully visualized. The next step is
dissection of the anterior choroidal artery, cranial
nerve III and the PComA. The DR is cut circumferentially around the ICA first when of the AL and
the intrathecal ICA proximal to the anterior choroidal
artery has been visualized. Venous blood oozing from
the intercavernous sinuses on the inferomedial side of
the ICA can be stopped by packing the intercavernous
sinuses with Surgicel. By holding the dura propria with
a stitch in the anteromedial direction and lifting the
ON the surgeon will be able to see the ophthalmic
V. V. Dolenc
Results
The postoperative results of the whole series of
COAs treated by the direct surgical approach are presented in Table 1. One hundred and twenty-one COAs
were clipped, whereas 22 COAs were treated by resection of the aneurysm and reconstruction the ICA wall
with sutures. Postoperative angiography was performed in all the patients except in two cases, who died
after surgery. In 137 cases postoperative angiography
showed patency of the ICA. In 4 cases the ICA was
occluded after surgery. In these 4 cases the COAs were
partially thrombosed and were resected, the thrombotic material being evacuated from the aneurysms
and the ICA wall being reconstructed with sutures. In
none of these 4 cases were neurological deficits or endocrinological disturbances present postoperatively.
The ipsilateral ICA after surgical exclusion of the
COA was patent in 2 patients with postoperative contralateral hemiparesis and in 2 patients with postoperative endocrinological disturbances. In 36 cases, visual
function remained unchanged after surgery, whereas
in 47 cases visual function improved. The overall results of the whole series were considered to be excellent
in 96 patients, very good in 36 patients, and good in
4 patients.
Carotid-Ophthalmic Aneurysms
Discussion
Anatomical studies of the parasellar area [9,11, 15,
18,26,27,33,35-37,40,41,45,47,51] have brought
new knowledge and stimulated further research of
normal anatomy and pathological conditions in the
region. Despite the benefits of such studies, controversy still remains regarding the definition and treatment of CO As [1, 2, 4,5,7,10,13,16,20,22-25,29,
34,38,39,43,48-51]. There is general agreement that
aneurysms of this kind originate in the medial half of
the wall of the intrathecal ICA. Controversy thus,
centres on the segment of the ICA from which COAs
emerge, the shortest being the segment of the ICA
between the ophthalmic artery proximally and the
PComA distally and the longest being the segment
from the ophthalmic artery proximally to the bifurcation of the ICA into the MCA and the ACA distally [7,
10, 13, 14, 16, 20, 22-27, 34, 43, 46, 49-51]. In the
available literature we were not able to find reports of
COAs located proximal to the origin of the ophthalmic
artery, i.e. on the segment of the intrathecal ICA from
the DR proximally to the origin of the ophthalmic artery distally. On the other hand, several authors claim
that COAs may extend beyond the intradural space
into the extradural space, i.e. proximal to the DR. The
description of COAs as being supraclinoid or paraclinoid [16,34,49] or terming them "carotid cave ICA
aneurysms" [24] does not offer any clarification of the
anatomical relationship of the aneurysms in this area.
It is generally accepted that the DR around the ICA
represents the site where the ICA pierces the dura and
enters the intradural space, and that the DR provides
the best anatomical landmark on the ICA, at the same
time representing the most proximal point of the intrathecal ICA, and for this reason it should be included
at least in the description if not in the definition of
COAs.
The DR forms a border between the two major
portions of the intracranial ICA, i.e. the extra- and
intra-dural segments [11]. It is very important to realize that the great majority of COAs are located intradurally and only exceptionally extends into the extradural space. In such cases the DR runs around the
aneurysm which is located in both the intradural and
the epidural compartments. In such instances it is also
very likely that the ophthalmic artery arises from the
aneurysm and not from the ICA. The preoperative
study of the exact size and location of the aneurysm
and of the point of origin of the ophthalmic artery
95
96
V. V. Dolenc
In cases of large/giant sub-optochiasmatic COAs adherent to the chiasm, pituitary stalk, optic truct and/or
the hypothalamus, the sac of the aneurysm should not
be peeled off the surrounding structures since this may
cause damage to the previously compressed structures.
These aneurysms should therefore be transsected and
emptied berfore the neck is clipped or the ICA wall
reconstructed with sutures, whereas the fundus firmly
attached to surrounding structures should be left in
place.
Once extremely demanding to be dealt with by the
direct surgical approach, COAs are - if the approach
described above is used - nowadays quite an easy task
for a surgeon who is familiar with the anatomy of the
central skull base and who is ready to spend more time
in carrying out the approach than in dissecting the
aneurysm itself. With this approach it is possible to
safely exclude the COA and at the same time both
preserve the patency of the ICA and avoid damage
to surrounding structures, thereby conserving the remaining function of the visual apparatus, and provide
the conditions for its improvement. When one uses this
approach as is described, any postoperative worsening
of the visual acuity should be avoided.
Contemporary treatment of COAs reflects the
microsurgical skills and also testifies interventional
neuroradiology, offering a good opportunity for
co-operation, not only in discussion, but in actual
performance.
References
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Carotid-Ophthalmic Aneurysms
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pp46 57
Correspondence: V. V. Dolenc, University Medical Centre,
Department of Neurosurgery, Ljubljana, Slovenia.
Summary
A series of 115 intracavernous internal carotid artery (lCA)
aneurysms have been treated by a direct surgical approach during
the past 15 years. Sixty-eight aneurysms were small. Of these 11 were
traumatic; nine caused by severe head injury and 2 by ICA injury
during transsphenoidal surgery. Twenty-six aneurysms were large
and 21 were giant.
Thirty-eight aneurysms were clipped, 46 were treated by resection
followed by ICA wall reconstruction with interrupted sutures, 16 by
excision and proximal/distal ICA end-to-end anastomosis and 15 by
resection/grafting. Postoperative angiography was performed in 107
cases and the ICA was found to be patent in 100 of these. Three patients died after surgery, two (with traumatic aneurysms) from associated brain injury and 1 from pulmonary embolism. Oculomotor
palsy was present in the immediate postoperative period in 104 patients. However, six months after surgery only 7 patients had residual
palsy.
The direct surgical approach to intracavernous ICA aneurysms
has constantly been changed and improved. The approach in its
original version [6] was mainly intradural, whereas its contemporary
version in most cases is extradural [10, II]. The latter approach provides complete exposure of the entire parasellar region, good proximal control of the ICA [13], and good access to the cavernous sinus
through the individual "corridors" between the cranial nerves [7]. In
the author's opinion the direct surgical approach provides better results than endovascular treatment with regard to patency of the ICA
[11].
Keywords: Aneurysm; cavernous sinus; internal carotid artery;
surgical technique.
Introduction
Surgical treatment of vascular lesions in the cavernous sinus (CS) has until recently been controversial. A
direct surgical approach to the CS was considered
hazardous notably because of lack of knowledge about
the topography of the region, the risk of venous
and arterial bleeding, and the inherent danger of the
approach. Even though some preliminary descriptions
of the region were available already in the 1940's [2,
27], more detailed anatomic studies have only emerged
during the last 30 years [6-11,19-22,28-31]. Follow-
100
V. V. Dolenc
Number
Aneurysm presentation
incidental
rupture
/.
paresis of
nerves III,
IV, VI
0/7
2/9
1/15
3/31
2/1
2/1
20
26
21
67
impaired
nerveV function
Small
Large
Giant
Total
68
26
21
115
27
9+2 3
/
/
/
/
27
14
stroke
4/2
Four-vessel angiography is mandatory in all patients with intracavernous ICA aneurysms in order to
identify incidental aneurysm. During the angiography
cross-flow via the anterior and posterior communicating arteries is investigated, a balloon occlusion test is
performed and venous out-flow studied. Apart from
the angiography, computed tomography (CT) and/or
magnetic resonance imaging (MRI) are also necessary
to demonstrate extension of the sphenoid sinus into the
anterior clinoid process (ACP), the presence of thrombus in the aneurysm or calcification of the wall of the
101
l .c
:t9n,~
Tnl ni.TC'
-OO~ . ' I~ AD I 0
d
'-J
lJ - (
Fig. I . Preoperative left carotid angiogram showing a large intracavemous ICA aneurysm - the antero-posterior view (a) and the lateral view
(b). The situation after resection of the aneurysm and reconstruction of the ICA with separate sutures in the anteroposterior view (c) and the
lateral view (d). The patient was right-handed and did not tolerate the balloon occlusion test. Endovascular exclusion of the aneurysm was attempted in three different centres and was not feasible due to the very broad neck of the aneurysm. The preoperative visual defect from the left
optic nerve completely disappeared during the first postoperative week. The postoperative paresis of nerves III and IV was also of short duration and one month after the operation the patient no longer had diplopia
102
through the skull base the ICA makes 4 loops [7]: the
posterior (PL), lateral (LL), medial (ML) and anterior
loops (AL). There are well defined anatomical points
which are of great importance for describing the configuration and the course of the ICA. The PL of the
ICA is located in the petrous bone and represents the
first tum of the ICA at the skull base, where its course
changes from vertical to a horizontal course towards
the foramen lacerum. From the LL, overlying the
foramen lacerum, the ICA passes in a supero-medial
direction towards the lateral aspect of the posterior
clinoid process (PCP). In its intracavernous part, on
the lateral aspect of the PCP, the ICA forms the ML
and courses anteriorly towards the ACP, where it
forms the AL which is situated on the inferomedial
side of the ACP. At the DR the ICA pierces the dura
and enters the intradural space.
True aneurysms are only found on the intracavernous segment, where the ML gives off two
branches: the meningohypophyseal and the inferolateral trunk. True aneurysms are not found in the
petrous segment since it is covered by bone. A false
aneurysm may, however, arise in the bone-covered
segments of the ICA. This is usually caused by a
fracture of the lateral wall of the sphenoid sinus that
lacerates the artery wall, most commonly of the AL.
The resulting false aneurysm projects into the sphenoid
sinus. Mycotic aneurysms are found on any segment of
the ICA.
The location, size and nature of an intracavernous
aneurysm dictate the extent of displacement and
stretching of cranial nerves III-VI. The corridors
between the individual nerves, i.e. the anteromedial,
paramedian and Parkinson's triangles [7], are very
important because different segments of the ICA, as
well as the aneurysm, are accessible through these triangular entry points. The distal part of the PL of the
intrapetrous ICA is covered with bone in about 80% of
cases, but it is easily accessible to the surgeon and after
being exposed it enables proximal control of the ICA
and/ or reconstruction of the artery by grafting.
Surgical Technique
The skin incision starts in front of the tragus and
continues close to the ear in an upward direction and
in a semicircular fashion. It ends 2-3 cm beyond the
midline and behind the hairline. The skin flap is reflected anteriorly until the orbital rim is exposed. The
temporal muscle is cut in the direction of the muscle
V. V. Dolenc
103
Table 2. Size of the lntracavernous ICA Aneurysms, Type of Aneurysm Exclusion. Postoperative Patency of the ICA and Outcome
Size and
Type of aneurysm exclusion leA
number of
patent
aneurysms leA reconstruction
clipping local direct graft
Small 68
Large 26
Giant 21
Total 115
32
4
2
38
30
10
6
46
6
4
6
16
8
7
15
Postop. nerve( s)
III, IV, VI
deficits after
one
week
59
63/63
24
20/24
21
17/20
100/107 104
6
months
2
2
3
7
Fig. 2. (a) MRI (coronal cut) showing a right CS lesion. (b) MRA showing right CS aneurysm. (c) Right carotid angiogram showing a large
intracavernous ICA aneurysm - preoperative anteroposterior view. (d) The lateral view ofthe right carotid angiogram shows the broad-necked
intracavernous ICA aneurysm originating from the horizontal segment ofthe intracavernous ICA. (e) Postoperative right carotid angiogramanteroposterior view. (f) Postoperative carotid angiogram, lateral view, showing narrowing of the intracavernous ICA. The arterial tree ofthe
right ICA is well visualized, hence the flow through the intracavernous ICA stenotic segment is sufficient (one month after surgery the patient
was symptom free - not even sUbjective diplopia)
105
The majority of small, intracavernous ICA aneurysms do not rupture, and may remain unchanged and
asymptomatic for many years. They rarely cause intrathecal hematoma or subarachnoid haemorrhage
(SAH) (14). If they rupture, they cause a CCF or, very
occasionally, a large false aneurysm which usually fills
the whole intracavernous space. Such CCFs and large
false intracavernous ICA aneurysms require an active
therapeutic approach. Small, incidentally found intracavernous ICA aneurysms should therefore be taken
seriously and - if possible - treated either by an endovascular or a direct surgical approach in a center where
sufficient experience has been accumulated from a
large number of comparable cases.
Traumatic (false) aneurysms, regardless of size, necessitate urgent treatment. Since false aneurysms are
located along the AL of the ICA and reconstruction of
the artery wall is necessary, surgical treatment is the
first choice. This applies especially to cases where endovascular treatment cannot preserve the patency of
the ICA and occlude the neck ofa false aneurysm (e.g.
in large false aneurysms projecting into the cavity of
the sphenoid sinus), the wall of the ICA should be
surgically reconstructed with separate sutures and/or
with a Sundt-Kees cuff clip. If the patient's medical
condition does not permit a direct surgical approach,
and provided the patient tolerates ICA occlusion, endovascular treatment should be considered.
As large/giant intracavernous ICA aneurysms
mostly manifest themselves with symptoms and signs
due to compression of the adjacent cranial nerves, it is
clear that a direct surgical approach is indicated to
remove the aneurysm mass. In elderly patients and
in those with medical problems the direct surgical
approach may not be appropriate and therefore endovascular treatment - either alone or in combination
with extracranial - intracranial (EC-IC) by-pass - is
the treatment of choice.
Even in patients that tolerate the balloon occlusion
test, occlusion of the ICA is not considered the treatment of choice, since postoperative neurological deficits may develop even if the patient has passed the test.
Such patients can, however, tolerate reconstruction of
the ICA after excision of the aneurysm, and hence re-
References
I. Berenstein A. Ransohoff J. Kupersmith M, Flamm E, Graeb D
(1984) Transvascular treatment of giant aneurysms of the cavernous carotid and vertebral arteries. Functional investigation
and embolization. Surg Neurol21: 3-12
2. Dandy WE, Follis RH Jr (1941) On the pathology of carotidcavernous aneurysms (pulsating exophthalmos). Am J Ophthalmol 24: 365
3. Debrun G, Lacour P, Caron JP, Hurth M, Comoy J, Keravel Y
(1978) Detachable balloon and calibrated-leak balloon technique in the treatment of cerebral vascular lesions. J Neurosurg
46:635-649
4. Debrun GM (1987) Embolization techniques in the treatment of
vascular lesions involving the cavernous sinus. In: Dolenc VV
(ed) The cavernous sinus: a multidisciplinary approach to vascular and tumorous lesions. Springer, Wien New York, pp 173181
5. Diaz FG, Ohaegbulam MD, Dujovny M, Ausman II (1988)
106
6.
7.
8.
9.
10.
II.
12.
13.
14.
15.
16.
17.
18.
19.
Summary
The purpose of this paper is to present the results, assessed by
an independent observer, of surgical treatment of 428 consecutive
patients harbouring aneurysms of the anterior circulation, together
with a review of relevant anatomy and operative strategy.
At follow-up (mean 5.6 years) 89.3% lived at home and were independent, 5.1% lived at home but needed some kind of assistance,
2.0% lived in institution, whereas information was unavailable in
3.6% ofliving patients. Two hundred and fifty-three patients (64.5%)
had unchanged employment status, 0.3% worked in sheltered environment, whereas 30.9% went out of work due to their subarachnoid
hemorrhage (SAH). Information about employment status was unavailable in 4.3%. For aneurysms of the internal carotid, anterior
communicating and middle cerebral artery, respectively, mortality
was 3.2, 3.9 and 5.6%, whereas 92.0, 88.1 and 89.0% of surviving
patients lived at home and were independent and 67.0, 63.6 and
63.0% had unchanged employment status.
Three-months mortality of all causes was 4.2%. In the postoperative period 53 (12.4%) patients developed clinical signs of vasospasms, 6 (1.4%) had cardiac infarction, 4 (0.9%) lung oedema, 4
(0.9%) deep vein thrombosis, and 7 patients (1.6%) infection. During
the follow-up period shunt-dependent hydrocephalus developed in
4.2% and 0.2% had a subsequent SAH from the same aneurysm.
Forty-three patients were on anticonvulsive therapy.
Keywords:
Cerebral
aneurysm;
subarachnoid
hemorrhage;
surgery.
Introduction
The term aneurysm was coined by Galen and first
used to describe an intracranial aneurysm by Wiseman
in 1669 [90]. Saccular aneurysms have a predilection
for the intracranial vessels and are found in 1-8% in
autopsy studies [8, 54, 87]. The major part of the 10
subarachnoid hemorrhages occurring per 100.000 citizens per year [66,69] is caused by aneurysms, of which
about 85% are located in the anterior circulation.
108
I. A. Langmoen et al.
o
I
2
3
~4
Total
Location of aneurysm
ACA
MCA
6
108
20
7
2
143
17
110
28
3
3
161
ICA
Total
11
86
24
2
34
304
72
12
6
428
124
2.
3.
143
124
161
428
33,4
29,0
37,6
100,0
ICA
ACA
MCA
Other**
Total
Asymptomatic aneurysm
lCA
ACA
12
10
4
2
27
MCA
5
7
10
1
23
other
total
3
1
24
20
21
I
66
4.
5.
109
into the sphenoparietal and cavernous sinus, occasionally to the superior petrosal sinus [104]. They
are in general in associated with the temporal lobe,
although smaller frontal veins cross the fissure to
join them. The fissure is therefore almost always
entered between the frontal lobe and the superficial
middle cerebral veins. The lateral part of the anterior fissure is often compressed. Consequently the
frontal and temporal lobes are often adherent in
this area. Also, the frontal lobe/orbital gyrus frequently indents the temporal lobe, or vice versa.
The correct plane of dissection in this part of the
fissure can be easier identified if working from the
inside to the outside. Slightly further distal, however, the cortex on the two sides of the fissure is less
compressed against each other and the Sylvian cistern is closer to the surface. By following a distal
arterial branch retrogradely by sharp dissection the
deep part of the Sylvian cistern is easily reached.
Dissection proceeds retrogradely along M2 and Ml
to the ICA bifurcation. Following this the outer
part of the anterior Sylvian fissure is opened from
the inside to the outside.
6. The following steps depend on the location, size
and projection of the aneurysm. We generally
puncture, and - if necessary - remove the aneurysm
dome, in order to verify occlusion and to facilitate
the final inspection of surrounding structures. It is
of special importance to assure that the clip(s) do
not interfere with the patency of parent vessels,
arterial branches, or major perforators. If in doubt,
this may be evaluated by intraoperative microvascular doppler sonography [2, 58, 59] or in some
centers intraoperative angiography [50, 51]. If
occlusion of the aneurysm is impossible without
parent artery occlusion, special techniques like
extracranial-intracranial bypass grafting [4, 44, 83,
85, 86] and clip reinforced wrapping [5] should be
considered.
()verallltes~ts
All patients included in the present material underwent microsurgical treatment. Twenty-five patients
had more than one aneurysm ligated during the operation for the symptomatic aneurysm and 17 patients had surgery twice. In one of these the symptomatic aneurysm was located at the superior cerebellar
artery. In the postoperative period 53 (12.4%) patients
Infection
Cardiac infarction
Lung oedema
Mortality (all causes within 3 months of surgery)
Clinical vasospasm
Symptomatic DVT*
Shunt dependent
Rebleeding
Seizures
Anticonvulsive medication
7
6
4
18
53
4
18
I
2
43
1,6
1,4
0,9
4,2
12,4
0,9
4,2
0,2
0,5
10,0
Independence
350
20
8
14
392*
89,3
5, 1
2,0
3,6
100,0
Employment
253
64,5
0,3
30,9
4,3
100,0
Mortality
121
17
392*
18
4,2
110
I. A. Langmoen et af.
Table 6. Frequencies (%) of Outcome (Glasgow Outcome Scale (GOS)) Related to Location of Aneurysm
GOS
ICA
MCA
AComA
Other ACA*
All aneurysms
2
3
4
5
Unknown**
Total
3,2
0,8
7,3
17,7
68,6
2,4
100
5,6
0
5,6
23
62, 7
3, I
100
3,9
0
4, 7
13,4
71, 7
6, 3
100
0
0
0
18,8
68,7
12,5
100
4,2
0,2
5,6
18,5
67, 3
4,2
100
111
increasing the necessity for temporal lobe retraction, the head is rotated 20 degrees towards the
contralateral side. The neck is extended to provide
gravitational retraction of the frontal lobe.
2. These aneurysms are treated through a conventional pterional craniotomy with radical sphenoid
wing removal. An orbitozygomaticopterional craniotomy with or without anterior clinoidectomy
facilitates proximal control and dissection from a
wider angle in large/complex aneurysms (see separate article by Lawton and Spetzler in this issue and
ref[18, 19, 108]).
3. Depending on the type of aneurysm different parts
of the basal cisterns are opened to deliver cerebrospinal fluid. When operating PComA, AChorA
or ICA bifurcation aneurysms, the initial approach
to the basal cisterns is made through the chiasmatic
cistern and the carotid cistern medial to the ICA.
When operating superior hypophyseal or ophtalmic
artery aneurysms, the inital opening is usually made
lateral to the ICA, into the carotid, crural and interpeduncular cisterns. This is followed by isolation
of the proximal ICA in order to secure proximal
control in the event of intraoperative rupture.
4. Some proximal ICA aneurysms may be treated
without opening the Sylvian fissure. ICA bifurcation aneurysms, however, require wide opening of
the fissure. PComA amd AChorA aneurysms may
be adherent to the temporal lobe, and ICA bifurcation aneurysms to the frontal lobe. Selective retraction of the appropriate lobe is therefore used in the
early stage of microsurgical dissection. When following MI to the ICA bifurcation it is important to
realize that one may meet the dome of the aneurysm
first. Depending on the location of the aneurysm,
the superior (PComA, AChorA) or inferior (ICA
bifurcation) wall of the MI is followed.
Results of Surgical Treatment of leA Aneurysms
diagnosed following SAH. Of these patients 86 suffered one SAH, whereas 24 suffered 2 bleedings, 2 patients 3 bleedings and 1 patient 4 bleedings prior to
surgery (Table 1).
Three months mortality of all causes was 3.2%. One
hundred and twelve patients were alive at follow-up.
Among these 75 (92.0%) lived at home and were independent, 5 (4.4%) lived at home but needed some kind
of assistance and 2 (1.8%) lived in institutions (Table
6). Seventy-five patients (67.0%) had unchanged employment status, 1 (0.9%) worked in sheltered environment, whereas 33 (29.4%) went out of work following their SAH. Information about employment
status was unavailable in 3 (2.7%) living patients.
Eight patients were dead in the follow-up period. This
was unrelated to surgery and had occurred after 2,3,5
(2 patients), 6 (2 patients), and 7 years. Grading according to the Glasgow Outcome Scale (GOS) is
shown in Table 6.
112
ACA close to the AComA [20, 64] and runs in a retrograde fashion along its mother vessel. Perlmutter
and Rhoton [68] found it to arise from A2 in 78%, Al/
A2 junction in 8% and A 1 in 14%. The diameter is on
average about 1 mm [27, 68], but varies considerably
(0.2-2.9 mm). It is almost always the largest branch
from AI/proximal A2, and may - if the Al is hypoplastic - be almost as large [lOS]. On its retrograde
course along Al it is most frequently situated on its
anterior side. Its mean length is 22 mm [46], and at
the ICA bifurcation it usually divides into several
branches (mean number 4.2) mainly turning into the
anterior perforated substance, but also into the frontal
lobe and the Sylvian fissure [20, 46, 68]. It is double in
5-20%, absent in 1-17%, and asymmetric in about
20% [20, 46, 68, 95, 107]. It supplies the anterior parts
of the caudate nucleus, putamen and internal capsule,
as well as a small part of the lateral globus pallidus
[20,64].
The anterior communicating artery (AComA) connects the two A I in the lamina terminalis cistern. It is
2.5 mm (range 0.1-7 mm) long. The diameter is up to
3.0 mm. If < 1.0 mm, which occurs in 16%, it is considered to be hypoplastic. It runs a single channel in
60% [68, 104], but variations are common, including
duplication, triplication, fenestration(s), and reticular
patterns [68, 104, 107], whereas true aplasia may not
occur.
The AComA gives rise to 1-4, or even more, perforating arteries [20, 74, 104] that terminate in the
suprachiasmatic area, dorsal chiasm, anterior perforated substance, and frontal lobe [74]. Dye perfusion
has indicated blood flow to the fornix, corpus callosum, anterior cingulum, and septal region [20]. They
most often emerge from the superior or posterior side,
often as a single vessel. If the two Al segments are of
unequal size, the site of origin is most commonly the
side of the larger Al [104]. In the case of a third or
single A2, these arteries may arise at or within the first
15 mm of its origin.
I. A. Langmoen et al.
2.
3.
4.
5.
113
%
92,0
4.4
1.8
1, 8
100,0
67,0
0,9
29,4
2, 7
100,0
3,2
Independence
103
5
2
2
112*
Employment
75
33
3
112*
Mortality
114
I. A. Langmoen et al.
115
116
I. A. Langmoen et at.
Independence
104
5
3
6
118*
88, I
4,2
2,6
5, I
100,0
Independence
130
9
3
4
146*
89,0
6,2
2, 1
2, 7
100,0
Employment
75
0
37
6
118*
63,6
0
31,3
5, 1
100,0
Employment
92
0
49
5
146*
63,0
0,0
33,6
3,4
100,0
Mortality
3,9
Mortality
5,6
Orbitofrontal artery
Prefrontal artery
Precentral artery
Central arteries
Anterior and posterior
parietal artery
Angular artery
Temporo-occipital
artery
Posterior temporal
artery
Middle temporal
artery
Incidence
Saccular aneurysms have a predilection for the
intracranial vessels which has been attributed to their
thin walls with less elastic tissue. They are distinctly
infrequent in children and adolescents, and often
associated with atherosclerosis. Prior to formation of
the aneurysm there is mural atrophy with fragmentation of the internal elastic membrane, attenuation of
medial muscle and thinning of the adventitia. These
observations are consistent with a degenerative rather
117
Timing of Surgery
In 1953 Norlen and Olivecrona published their results of delayed surgery [57]. These results compared
so favourably with earlier reports, which consisted
mainly of patients operated on in the acute phase, that
it changed the attitude of most neurosurgeons. With
the development of modern neuroanesthesia, improved surgical approaches and microsurgical techniques, however, it became possible to perform early
surgery with good results [35, 47]. Due to the high incidence of rebleeding and vasospasms, it was felt that
early surgery, which eliminated the aneurysm and
allowed more aggressive treatment of vasospasms,
would be beneficial. This hypothesis was tested in a
randomized study by Ohman and Heiskanen [62] who
found that 91.5% of patients operated early were independent at 3 months post-SAH compared to 80.0%
of the patients operated on more than 8 days postSAH, and further that management mortality was
twice as high among patients subject to delayed surgery. In a multicenter study performed between 1980
and 1983 by Kassell and coworkers it was found that
although 30% of patients admitted early would not
survive untit later surgery, the complications due to
early surgery more or less offset its advantage [37, 38].
Today it is generally agreed that most aneurysms
should be treated as early as possible.
Results of Surgery
In a series of 100 consecutive cases Post et al. [71]
observed an overall surgical mortality of 8.1 %. The
surgical mortality of patients in Grades 1,2 and 3 was
6.3%. At follow-up 60 patients had returned to their
activities, whereas activity limiting deficits were found
in 25.
Yasargil and Smith [107] reported a series of 678
anterior circulation aneurysms predominantly operated late. Postoperative results were good (returned to
normal occupation with no or minimal deficit) in 83%,
fair (returned to work in a more limited capacity because of neurological deficit) in 7%, poor (requiring
supportive care) in 4%. Operative mortality was 4%
and mortality of other causes 1.6%. Among ICA
aneurysms good results were obtained in 83%, fair in
7% poor in 4%, and operative mortality was 4.7%.
Among MCA aneurysms good results were seen in
74%, fair in 14% poor in 4.5%, and operative mortality
was 4.7%. Among ACA aneurysms good results were
118
obtained in 87%, fair in 4% poor in 4.5%, and operative mortality was 2.3%.
Sundt [90] reported a series of 1005 saccular aneurysms. Overall 73% of the patients were in normal employment without neurological deficits. Excellent
(normal employment without deficits) or good (neurological deficit with normal mentation and functional
employment) results were obtained in 94% of the patients in Botterell grade 0, 93% in grade 1, 84% in
grade 2,51% in grade 3 and 22% in grade 4. Among
ACA aneurysms, excellent results were seen in 73.6%,
ICA aneurysms 76.6% and MCA 70.7%.
In the International Cooperative Study on the
Timing of Aneurysm Surgery by Kassell et al. [38] it
was found that alert patients had a mortality rate of
10-12% when undergoing surgery prior to day 11
compared with 3-5% when surgery was performed
after day 10. Patients drowsy on admission had a 2125% mortality rate when operated on up to day 11 and
7-10% with surgery thereafter. The postoperative risk
following early surgery was equivalent to the risk of
rebleeding and vasospasm in patients waiting for delayed surgery. Good recovery was observed in 69.6%
of patients with ICA, 67.5% with MCA and 67.0%
with ACA aneurysm, whereas mortality was 12.6%,
13.0% and 16.8% respectively.
Hernesniemi et al. [31] reported a series of 1007 patients where 55% were operated on during the first
three days and 77% during the first week. Surgical
mortality at 30 days was 9%. Ninety percent of the
patients presenting in Hunt and Hess grades I-II, 68%
in grade III and 30% in grade IV- V had an independent life at follow-up. In line with the results of the
present series they found poorer management results
for MCA aneurysms compared to ICA and ACA
aneurysms.
Deruty et al. [17] followed a group of 73 patients
that had undergone either early or late surgery.
Ninety-seven per cent of the patients were available for
follow-up. The overall immediate outcome was good
or fair in 85%, poor in 4%, and death in 11%. Among
63 patients alive and available for long term follow-up,
57% had returned to their previous activities, 16% had
returned to a reduced level of activity, and 27% were
unemployed.
Siiveland et al. [82] reviewed outcome of surgery in a
prospective study where all patients with verified
aneurysmal SAH admitted between June 1, 1989 and
May 31, 1990, were enrolled. The study covered 6.93
of Sweden's 8.59 million inhabitants (81%). Among
I. A. Langmoen et al.
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119
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Correspondance: Professor Iver A. Langmoen, M.D., Ph.D., Department of Neurosurgery, Karolinska Hospital, S- 171 76 Sweden.
Summary
Ninety-eight patients with aneurysms of the posterior circulation
were admitted to our department from 1993 to 1997. Sixty of them
underwent microsurgical treatment, mostly in the acute stage of
subarachnoid hemorrhage. Peri- and intraoperative management
were carried out according to a structured treatment strategy. Special aspects of surgical technique included extradural selective anterior clinoidectomy for basilar head aneurysms, lateral SUboccipital
craniotomy and partial condylectomy without laminectomy for
aneurysms of the vertebral artery or posterior inferior cerebellar
artery, and a trans-Sylvian approach, as used in selective amygdalohippocampectomy, for aneurysms of the posterior cerebral artery. A
careful angiographic evaluation of the aneurysms in relation to the
neighboring important arteries and bony structures was essential for
optimal surgical planning. Forty-nine patients (82%) made a good
recovery by 3 months after surgery. The mortality was 7%.
Keywords: Posterior circulation aneurysms; basilar head aneurysm; acute stage; extradural selective anterior clinoidectomy.
Introduction
Posterior circulation aneurysms remain a therapeutic challenge despite improvements in microsurgical
technique [7, 35, 40] and advances in endovascular
therapy. Promising early results have been obtained
with the latter method: about 50% of posterior circulation aneurysms can be completely occluded initially,
although coil compaction may often occur afterwards,
resulting in incomplete occlusion. [19, 22, 26] In this
paper, we report our technical strategies and the results
obtained in 60 consecutive operative cases performed
during the last 5 years (1993-1997), in accordance
with our principle that ruptured aneurysms, particu-
larly, in the acute stage should be occluded microsurgically with clipping of the neck [44]. Our structured perioperative treatment strategy for ruptured
aneurysms in the acute stage has been reported previously [24, 42, 44] and is summarized in Table 1. In
this paper, we discuss the application of this strategy to
aneurysms of the posterior circulation.
Strategies and Surgical Methods
Basilar Head Aneurysms
Angiographic and anatomical considerations. The
preoperative angiographic examination yields important information about the aneurysm: its size, shape,
and orientation, the width of its neck, the vertical and
anteroposterior distance of the neck from the posterior
clinoid process, and the distance of the neck from the
midline. Further important angiographic data include
the diameter of the posterior communicating artery
(PcomA), the distance of the internal carotid bifurcation from the midline (seen in an anteroposterior view)
and from the anterior clinoid process (lateral view), the
course of the posterior cerebral artery (PCA), the
presence of concomitant aneurysms, etc. These data
may be confirmed and extended by means of threedimensional angiographic CT (3D CT).
The location of the aneurysm in relation to the posterior clinoid process is of cardinal importance. A
plain lateral angiographic view demonstrating the
124
Y. Yonekawa et al.
Trannygomati<:... __ _
Pterional,
--=
Transpetrosal
Transcondylar
bony structures, in addition to subtraction angiography, is indispensable for proper evaluation (Fig. 1).
The aneurysm neck is located above the posterior clinoid process in approximately 60% of basilar head
aneurysms [13]. The optimal distance of the aneurysm
neck above the posterior clinoid process for the pterional approach has been reported to be between 0.5
to 1 cm [37]. This approach may still be used for
aneurysm necks situated up to 1.5 cm above the
posterior clinoid process, as long as the operative field
is widened in a manner discussed below. Aneurysms
located above this level can be managed with other
approaches, including the transzygomatic subtemporal approach, the orbitozygomatic temporopolar
approach, or special approaches through the third
ventricle [11, 14,31]. On the other hand, an aneurysm
neck more than 2- 3 mm below the posterior clinoid
process can be can be reached if the operative
approach is widened by a posterior clinoidectomy.
Aneurysm necks beneath this level require the use of
the subtemporal-transtentorial approach.
125
]
neck [11], the length and size of the PcomA - as it may
need to be mobilized and transected to gain a wider
operative field, and the thalamoperforating arteries although difficult to see on the angiogram preoperative
detection will make them easier to identify and preserve intraoperatively.
Our routine surgical strategy for basilar tip aneurysms and basilar artery-superior cerebellar artery (BASCA) aneurysms in the acute stage is as follows:
1. Conventional pterional craniotomy, usually from
the right side.
2. Extradural selective anterior clinoidectomy [45].
3. Opening of the membrane of Liliequist and the
lamina terminalis.
4. Posterior clinoidectomy (when necessary).
5. Transection of the PcomA (when necessary).
6. Temporary clipping of the BA trunk. Mannitol
(20 g) is given routinely in advance, and a bolus of
thiopental (500 mg) if the duration of temporary
occlusion exceeds 15 minutes.
7. Dissection of the aneurysm, identification of the
thalamoperforating artery, and isolation of the
aneurysm with a rubber dam [34].
10
;f
10
if
Dx H(mm' )
200
20
20
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OCT RCA
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'--------l
OCT
RCA
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'------'
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RCA
126
Y. Yonekawaetal.
Fig. 4. Selective extradural anterior clinoidectomy. After a conventional pterional craniotomy and drilling away of the lateral part of
the sphenoid ridge, the anterior clinoid process can be removed en
bloc by drilling away of the lateral cranial bony wall of the superior
orbital fissure and that of the roof of the optic canal and optic strut.
(a) This enables the access to the clinoid space (b)
If the PcomA must be divided it should be transected at its junction with the PCA. Perforating arteries
arising from the posterior communicating artery
should be preserved as far as possible, even if the artery
is hypoplastic. Compromise of its tuberothalamic
branch can result in a small infarct and mild hemiparesis [3, 27]. With our standard technique, there is
no need to sever the anterior temporal venous drainage
into the sphenoparietal sinus, or to sacrifice a well
developed temporopolar artery, as is done in the temporopolar approach or extended lateral approach [l, 4,
30]. These approaches remain very useful, however,
for special and difficult types of aneurysms.
Case J RT. This 49-year-old man suffered a subarachnoid hemorrhage (SAH) on February 19, 1995.
He was transferred to our clinic in good clinical condition about two months later.
Angiography (April 20): An aneurysm with a diameter of approximately I cm was found at the basilar
head (Fig. 5). The neck was located 0.5 cm above the
posterior clinoid process. The left PCA was filled from
ICA.
Operative procedure and findings (Fig. 6): A conventional right pterional craniotomy was followed by
an extradural selective anterior clinoidectomy which
provided a wider operative field for the retrocarotid
approach to the aneurysm. A partial posterior clinoidectomy was performed to expose a site for temporary
clipping of the BA trunk. The PcomA was transected
at its junction with the PCA. After temporary clipping
of the BA trunk for 3 minutes, the aneurysm was isolated with a rubber dam from the thalamoperforators
arising from the PI segments on both sides, and occluded with two permanent clips.
Postoperative course and follow-up angiography:
The patient woke up after surgery with an unexpected
left hemiparesis and a CT scan revealed a small tuberothalamic infarct (Fig. 7). The hemiparesis subsided
within a few days. Follow-up angiography on April 28
127
~~~~~~~------------~--M :
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. Os
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Fig. 5. Case I: RT, 49year-old man. (a) AP view. (b) Lateral view.
Note the height of the aneurysm neck (5 mm) above the posterior
clinoid process
128
Y. Y onekawa et af.
Fig. 8. Case 2: RB, 65-year-old man. (a) AP view. The right PCA was opacified by carotid angiography. (b) Lateral view. (c) 3D-CT angiography reveals that the aneurysm neck is at the level of the posterior clinoid process
129
The postoperative course was uneventful until the follow-up angiography on Sept. 17, which showed complete occlusion of the aneurysm and preservation of
important neighboring vessels (Fig. 10). Just after the
angiography, a severe visual disturbance developed,
almost to the point of finger detection only. This disturbance subsided day by day with conservative therapy with dexamethsone and heparin. By the date of
discharge (Sept. 23) Goldmann perimetry revealed
approximately the same visual field defect that the
patient had preoperatively.
Comment. This is a typical case in which the neck
could be clipped through the optic carotid triangle
after posterior clinoidectomy. Wide-necked aneurysms
130
Y. Y onekawa et al.
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Fig. II. Case 3: FL, 28-year-old woman. The CT scan shows extensive SAH and hydrocephalus with dilatation of the temporal horn
posterosuperiorly, and the PCA was somewhat Yshaped in the AP view. The aneurysm neck was
located approximately I cm above the posterior clinoid process.
Operative procedure and findings: (Fig. 13) The
patient was operated upon on the day of admission,
immediately after angiography. A conventional right
pterional craniotomy with selective extradural anterior
clinoidectomy was performed. Opening of the lamina
terminalis and the membrane of Liliequist, with removal of an extensive subarachnoid clot, enabled dissection of the aneurysm. Transection of PcomA was
necessary. A considerable part of the aneurysm dome
was hidden behind the right PI, as could be expected
from the angiographic finding of a Y-shaped PCA.
After dissection of an important thalamoper-forator
originating from the left PI, the basilar trunk was
temporarily clipped for 13 minutes, and the aneurysm
was occluded with a curved Yasargil clip inserted behind the right PI. A small piece of muscle was applied
to a small remnant of the aneurysm neck and fixed in
place with Aron Alpha (Sankyo Co. Ltd. Tokyo).
The head of the permanent clip touched the oculomotor nerve.
Postoperative course and follow-up angiography:
the course was uneventful except for an oculomotor
nerve palsy, and the patient was discharged on July 22.
The oculomotor palsy subsided completely by the time
of outpatient follow-up 3 months after surgery. Fol-
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Fig. 13. Artist's view of the operative procedure and findings: Note
transection of the posterior communicating artery. Because of
the Y-shaped PI and the posteriorly directed aneurysm, it was necessary to insert an aneurysm clip from behind the PI and the basilar
artery. A piece of muscle was applied to the small residual aneurysm
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Fig. 14. Postoperative angiography. (a) AP view and (b) lateral view
showing a complete clipping of the aneurysm neck
132
y. Y onekawa et al.
condylectomy, is the procedure of choice for such lesions, as well as for midline aneurysms at the junction
of the vertebral arteries. The lateral suboccipital
approach was reported on by Drake [7] and Heros [10]
but had been in use much earlier, as Yasargil had performed such procedures micro surgically as early as the
late 1960's. The prevailing method before that time
was the extensive midline posterior fossa craniotomy
approach described by Kempe [12].
Our routine approach to the VA-PICA aneurysms is
as follows:
1. Lateral (retroauricular retromastoid) suboccipital
craniotomy in the sitting position.
2. Dissection of the extracranial VA at its horizontal
segment between the occipital bone and the atlas.
There is no need to perform even a partial resection
of the posterior arch of C 1.
3. Partial occipital condylectomy (Fig. 16) (eventually
by drilling away of the jugular tubercle).
4. Dural opening and dissection of the aneurysm
5. Temporary clipping of the proximal VA and clipping of the aneurysm neck.
Fig. 15. Distances of aneurysm from bony structures. (A) From the
midline. (B) From the most lateral part of the foramen magnum. (C)
From the clivus. These distances are related to operative accessibility
and postoperative complications involving the lower cranial nerves
(see text)
133
Fig. 17. Case 4: TK, 56-year-old woman. (a) AP view. Note that the
aneurysm is near the midline. (b) Lateral view showing origin of the
PICA from the aneurysm neck
134
of the sellar floor) can be managed through a conventional subtemporal approach combined with transection of the tentorium. Aneurysms at lower levels
should be managed through either an anterior transpetrosal approach or a lateral suboccipital approach,
with or without transection of the sigmoid sinus, and
with or without condylectomy [4, 33].
The orientation of the aneurysm is an important
factor in the ease or difficulty of access [9]. Laterally
pointing aneurysms are the most difficult, as these
must be approached from the aneurysm dome. The
dissection of posteriorly directed aneurysms is made
difficult by the need to dissect out the nearby perforating arteries. When the anterior inferior cerebellar
artery (AICA) and superior cerebellar artery (SCA)
are hypoplastic, great care should be taken to preserve
the circumferential branches of the BA, as these are the
main source of the blood supply to the brain stem [18,
Y. Yonekawa et al.
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Fig. 19. Case 5: BJ, 59-year-old man. (a) AP view. (b) Lateral view
showing a posteriorly directed basilar trunk aneurysm at the level of
the upper third of the clivus
136
Y. Yonekawa et al.
Fig. 21. Postoperative CT scan indicating an extensive pontine infarction in spite of apparent preservation of the perforating arteries
from the basilar trunk
Fig. 22. Case 6: LP, 39-year-old female. (a) AP view. (b) Lateral
view showing a bilobed fusiform aneurysm at the junction of the
right P2 and P3 segments
137
138
Y. Yonekawa et al.
Table 2. Posterior Circulation Aneurysms Surgically Treated (1993-1997) - 60 Consecutively Operated Patients - Results (3 Months)
GR
Basilar head
ruptured
unruptured
Basilar-SCA
ruptured
unruptured
Basilar trunk
ruptured
unruptured
PCA-PI
ruptured
unruptured
PCA-P2-P3
ruptured
unruptured
VA-PICA
ruptured
VA-BA dissection
ruptured
Total
MD
SD
VS
20
16
4
7(I:l,II4 @,III2)
1*
1 (II)
I
3
2
I (II)
2*
I (III)
I
17
2 (I, III)*
60
49 (82%)
I (III) @
3
I (III)
2 (III, IV) ++
17
1 (III .) +
1 (IV) @
1 (IV) +
1 (IV) @
I (IV)
3
I (IV)*
2 (3%)
2 (3%)
3 (5%)
4 (7%)
SCA Superior cerebellar artery; PCA posterior cerebral artery; VA vertebral artery; PICA posterior inferior cerebellar artery; BA basilar artery;
GR good recovery (Glasgow outcome scale); MD mildly disabled; SD severely disabled; VS vegetative state; D death; I-IV grading after
WFNS world federation of neurological surgeons; * coating; + proximal ligation or trapping; symptomatic vasospasm; @ hydrocephalus.
sufficiency, as mentioned above in Case 5. Six unfavorable results (SD, VS, D) in grade IV resulted in one
case from a combination of vasospasm and technical
insufficiency, and in five cases from direct injury of the
initial bleeding. Symptomatic vasospasm occurred in
7 cases (13.7%) and communicating hydrocephalus
necessitating a ventriculoperitoneal shunt in 10 cases
(19.6%).
Discussion
Improvements in microsurgical technique, the development of skull base surgery, and advances in the
understanding of the microsurgical anatomy of the
vertebrobasilar arterial territory have made it possible
to treat ruptured aneurysms of the posterior circulation in the acute stage, as has been done earlier with
aneurysms of the anterior circulation.
We consider surgery in the acute stage of SAH to be
necessary, as the mortality during the first 48 hours
after an aneurysmal rupture in the posterior circulation has been reported to be significantly higher than
that after an aneurysmal rupture in the anterior circulation [9, 16, 32]. Several authors have recently reported favorable results for the acute surgical management of ruptured aneurysms in the posterior
139
circulation, comparable to those obtained with aneurysms in the anterior circulation. Lang and Galbraith,
in 1993 [15], reported a series of 121 patients with
posterior circulation aneurysms, of whom 97 presented
with SAH; the overall management mortality was
30%, and the operative mortality was l3%, comparable to results obtained with anterior circulation aneurysms. The larger series of Peerless et al. included 206
patients [25] who underwent early surgery, including
cases of basilar head aneurysms managed through a
subtemporal approach; 82% of patients made a good
or excellent recovery, and 9.7% died. In the 146 cases
of Nukui et al. [23] 76% made a good recovery and
12% died. These authors stressed that the results were
better in patients less than 65 years old, and aggressive surgical treatment in the acute stage in patients
over 65 years old with an impairment of consciousness
due to hydrocephalus. Our results agree with those
reports. The figures we obtained in this series for the
frequency of complicating symptomatic vasospasm,
and for the frequency of hydrocephalus, were l3.7%
and 19.6%, respectively. These are to be compared
with the 17.5% and 9% that we reported previously
[42] in our series of 150 consecutive cases of ruptured
aneurysms.
It should be emphasized that deliberate planning of
the operative procedure, based on a careful evaluation
of the angiographic findings in relation to neighboring
bony structures, is mandatory for successful surgical
management of posterior circulation aneurysms. Furthermore, it should be pointed out that results as good
as those presented may be obtainable only in a limited
number of institutions that treat many SAH patients,
as these aneurysms are rather infrequent, and trained
hands and the associated infrastructure are prerequisites for the success of surgical management.
The role of endovascular treatment in the management of aneurysms, and particularly of ruptured
aneurysms in the acute stage, seems highly promising
but still remains to be established [19, 22, 26]. We
consider this form of treatment to have a largely auxiliary role in current management.
Acknowledgments
This work could not have been accomplished without the good
cooperation of the department of neurora-diology (Prof. A. Valavanis), University Hospital, Zurich.
The authors are indebted also to Ms Frick, Mrs Schurter and
Mr. Stillhard for their assistance.
Reference
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infratentorial supracerebellar approach: technical note and summary ofresults. Kitakanto Med J (SI): 15-22
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Correpsondence: Prof. Y. Yonekawa, Department of Neurosurgery, University Hospital, CH-8091 Zurich, Switzerland.
Summary
Untreated giant intracranial aneurysms have a dismal natural
history as a result of hemorrhage, cerebral compression, and throm
boembolism. The poor prognosis of patients with giant aneurysms
therefore warrants aggressive treatment. A surgical approach is
chosen to maximize the operative exposure of the aneurysm and de
pends mainly on the aneurysm's location. Once exposed, vascular
control of the aneurysm is required not only to manage an intra
operative rupture, but also to collapse the aneurysm, to increase
working space, and to improve visualization of the anatomy. Hypo
thermic circulatory arrest may be indicated in select patients with
complex posterior circulation aneurysms. Direct clipping of giant
aneurysms, with meticulous preservation of parent and branch ar
teries, is the preferred method of occlusion. Unclippable aneurysms
require alternative techniques (e.g., trapping, parent artery occlu
sion, excision, and aneurysmorrhaphy) that compromise parent ar
teries and may require revascularization to restore adequate cerebral
blood flow. Giant aneurysms are complex lesions that demand thor
ough surgical planning, individualized strategies, and a multi
disciplinary effort in specialized neurovascular centers.
Keywords: Giant aneurysm; hypothermic circulatory arrest;
revascularization; subarachnoid hemorrhage.
Introduction
Although giant aneurysms are rare lesions, their inherent anatomical complexity and the technical difficulty of their surgical treatment make them a common
topic of analysis. What makes giant aneurysms so
challenging are the preoperative and intraoperative
decisions required to devise the best strategy for safe
management. Sound decisions depend on familiarity
with the spectrum of treatment options, mastery of the
techniques required in surgery, and experience. Therefore, this review presents the critical elements of the
surgical strategies for giant intracranial aneurysms,
derived from an experience with more than 250 surgical patients.
142
Diagnostic Evaluation
Patients who presented with SAH were managed using the same
principles and protocols that have been established for other patients
with SAH [4]. Blood pressure was controlled carefully to minimize
the risk of rupture. Ventriculostomy with cerebrospinal fluid drainage was used to treat patients with Hunt and Hess grades IV and V,
and measurements of intracranial pressure (ICP) were used to guide
surgical decisions [5]. ICP elevations were managed aggressively
with conventional methods. Surgery was performed within 24 hours
of presentation in suitable patients.
Surgical Treatment
Results
Patient Outcome
The surgical mortality of this series was 7%. Many
of these patients presented with poor Hunt-Hess
grades after SAH. The treatment-associated neurological morbidity rate was 11 %.
Pre- and postoperative neurological function was
evaluated using Glasgow Outcome Scale (GOS) scores
[21]. At late follow-up, 85% had an excellent or
good outcome. Specifically, 66% had an excellent outcome (GOS 1), 18% had moderate disabilities (GOS
2), 7% had severe disabilities (GOS 3), and 2% were
vegetative. The mean length of follow-up was 2.2
years.
As expected, outcome for patients who presented
with SAH correlated with Hunt-Hess grade. As a
group, the SAH patients did worse than patients
with other presentations (i.e., compressive symptoms,
thromboembolic symptoms, and incidental aneurysms). Outcomes tended to be better in patients with
giant aneurysms in the anterior circulation. Eightynine percent of these patients had excellent or good
outcomes compared to 74% of the patients with posterior circulation aneurysms. The technique of aneurysm obliteration did not correlate with outcome.
Discussion
Rationale for Surgical Treatment of Giant Aneurysms
The natural history of untreated giant intracranial
aneurysms is dismal, due to a high risk of hemorrhage,
143
progressive neurological deficits from cerebral compression, and distal thromboembolism causing stroke
and death [23, 33, 34, 37, 38]. The mortality rate of
untreated giant aneurysms reported by Peerless et al.
was 68% after 2 years and 85% after 5 years [37]. All
survivors had marked neurological dysfunction. Michel [34] reported a 100% mortality rate at 2 years in
untreated patients. Seventy-five percent of Kodama
and Suzuki's [23] untreated patients died of SAH during their hospitalization. Therefore, the poor prognosis
of untreated giant aneurysms warrants aggressive
treatment.
In contrast to the natural history of giant aneurysms, surgical outcomes in large patient series have
been excellent to good, ranging from 61% to 86%.
Surgical mortality rates have ranged from 5% to 22%
(Table 1). When these surgical results are compared
with the poor outcome associated with the natural
history of untreated giant aneurysms, it is apparent
that an aggressive surgical posture is appropriate.
The objective of treatment is to eliminate the risk of
neurological impairment resulting from hemorrhage,
cerebral compression, or thromboembolism. Surgical
strategies are therefore designed to exclude the aneurysm completely from the circulation, to maintain
adequate cerebral blood flow, and to decompress vital
neural structures [29].
Elements of Surgical Strategies for Giant Aneurysms
Surgical approach: anterior circulation giant aneurysms. Selection of the approach that provides the
widest exposure and most direct access to the aneurysm is the first and most important surgical decision,
and aneurysm location is the primary factor that influences this decision.
F or anterior circulation giant aneurysms, selection
of approach amounts to deciding whether an orbitozygomatic osteotomy will enhance the routine pterional exposure enough to justify its use [1, 9, 39, 40].
The pterional craniotomy is the standard approach for
these aneurysms and requires extensive drilling of 1.
the lesser wing of the sphenoid bone medial to the superior orbital fissure, 2. the bony ridges of the orbital roof, 3. the inner table of the inferior frontal bone
over the superior orbital rim, and 4. the squamosal
portion of the temporal bone inferiorly to the floor
of the middle fossa. The removal of bone around
the pterion flattens this corridor and creates space
under the frontal and temporal lobes and Sylvian
Author/reference
Sundt [49]
Peerless et al. [37]
Hosobuchi [17]
Ausman et al. [3]
Kodama and Suzuki [23]
Symon and Vajda [50]
Yasargil [52]
Heros [14]
Lawton and Spetzler [30]
Total patients
315
305
82
62
49
36
30
28
171
Outcome
excellent/
good
fair/ dead
poor
80%
67%
84%
84%
61%
86%
67%
82%
87%
6%
22%
9%
11%
16%
6%
23%
7%
8%
15%
11%
7%
5%
22%
8%
10%
5%
5%
144
rior circulation. If the basilar artery is divided conceptually into fifths [26], then the posterior circulation can
be considered as three distinct zones: an upper basilar
zone (upper two-fifths of the basilar artery), a midbasilar zone (middle fifth of the basilar artery), and
a lower vertebrobasilar zone (lower two-fifths of the
basilar artery and the intradural segment of the vertebral arteries). Giant aneurysms located in the upper
basilar zone may be accessed through the orbitozygomatic approach; those located in the midbasilar zone
may be accessed through a transpetrosal approach;
and those located in the lower vertebrobasilar zone
may be accessed through a far-lateral approach (Fig.
la) [26]. Giant aneurysms that straddle different zones
may require one of the combination approaches (Fig.
145
d
Fig. 2. (a)The extended orbitozygomatic approach uses a pterional craniotomy and removes the orbitozygomatic unit as a single piece. Osteotomies are made across the root of zygoma, across the malar eminence to the inferior orbital fissure, through the orbital roof lateral to the
supraorbital nerve, across the posterior orbit and pterion, and down to the inferior orbital fissure. (b) The view of the mid basilar artery is obstructed by the anterior and posterior clinoid processes and dorsum sella. (c) Drilling away these bony obstacles creates a window in the upper
clivus through which the mid basilar artery can be visualized. (d) Additional inferior exposure of the basilar artery enables the aneurysmal neck
to be dissected and defined, working along the axis of artery. With permission from Barrow Neurological Institute
146
~~""""""""'~#-=Transcochlear
Translabyrinthlne
Retrolabyrinth.ne
tentorium is divided to connect the supra- and infratentorial compartments. Extensive exposure of the
medial petrous and clival regions and associated neurovascular structures is obtained with minimal brain
retraction.
Vascular control of giant aneurysms. Once the surgical approach has been performed and the dura opened,
the next concern is vascular control of the aneurysm.
Vascular control is a basic tenet of aneurysm surgery
because it enables the surgeon to manage an intraoperative rupture. The fact that only a third of giant
aneurysms present with subarachnoid hemorrhage
may appear to lessen the importance of vascular control of these aneurysms, but it is equally important for
other reasons. The aneurysmal mass necessitates
maneuvers that decompress it and reduce it. This size
reduction, whether by collapsing the aneurysm or debulking it, enables visualization of the parent arteries
and aneurysm neck, which is essential to the repair.
Vascular control in the anterior circulation is usually easy to obtain; temporary clips can be placed
proximal and distal to the aneurysm to eliminate blood
flow through the parent artery. Several locations can
be difficult, however, including the clinoidal and ophthalmic segments ofICA. There are several options for
proximal control. I. The cervical ICA can be exposed
through a separate neck incision with temporary arterial ligation. 2. The petrous ICA can be exposed
through Glasscock's triangle on the middle fossa floor.
The artery can then be occluded temporarily with clips
or with temporary extraluminal balloon compression
with a Fogarty catheter inserted in the carotid canal
between the bone and the artery. 3. The clinoidal
segment of the ICA can be exposed and temporarily
occluded with a clip after the anterior clinoid process
has been removed. The final option is endovascular
balloon occlusion of the cavernous ICA with a catheter threaded into position through a femoral arterial
puncture.
Each of these four options has distinct advantages
and disadvantages. Proximal control via the cervical
ICA requires a visible incision of the neck, but it is the
quickest and easiest method. Drilling Glasscock's triangle is elegant because there are no external signs of
this exposure, but the procedure can be time-consuming. Anterior clinoidectomy is easier to perform, but
often the giant aneurysm obscures access to this region
and incising the medial portion of the distal dural ring
can be difficult. Endovascular balloon occlusion is easy
for neuro-interventionalists to perform and enables
147
148
149
Fig. 4. (a) A dolichoectatic aneurysm involving the intradural vertebral artery is shown compressing the brain stem and cranial nerves. (b) This
compressive mass is eliminated by opening the aneurysm and (c) removing thrombus with an ultrasonic aspirator. (d) The thrombectomy
proceeds until the lumen of the aneurysm is encountered. (e) Bleeding is controlled with Surgicel, and (f) the aneurysm walls are brought together with clips to reconstruct the parent-artery lumen. Note that the thrombectomy eliminates mass effect and generates the redundant vessel
wall for reconstructing the artery. With permission from Barrow Neurological Institute
150
151
Fig. 5. (a) Some giant midbasilar artery aneurysms are too difficult to reconstruct with clips, and treatment is limited to parent-vessel occlusion.
(b) Blood flow to the distal basilar artery territory is augmented with a superficial temporal artery-to-superior cerebellar artery bypass in an
initial surgical stage. (c) The proximal or distal basilar artery is then clip-occluded during a second surgical stage. (d) Reduction of flow through
the aneurysm promotes thrombosis of its lumen, which enables thrombectomy to be performed during a third surgical stage. The dashed line
designates the extent of the thrombectomy. Note that treatment relieves mass effect on the brain stem and preserves distal cerebral blood flow.
With permission from Barrow Neurological Institute
152
Fig. 6. (a) This giant middle cerebral artery aneurysm is amenable to resection with primary reanastomosis. (b) Proximal and distal control of
the aneurysm is obtained with temporary clips and the aneurysm is resected. The ends of the artery are mobilized by cutting their arachnoid
adhesions. (c) The artery is reanastomosed to reconstitute flow to Sylvian vessels. With permission from Barrow Neurological Institute
153
Supraclinoid
.
"
v
\
ICAv.,~__
Ophth A.
Saph .
Vein
Graft
Ophth A.
STA
Fig. 7. Surgical approaches to revascularization of the anterior circulation. Overview showing the anterior circulation and common locations
for aneurysms. (a) The internal carotid artery ( ICA ) aneurysm at the skull base is trapped and revascularized with a cervical-to-petrous carotid
bypass with saphenous vein graft. (b) The cavernous ICA aneurysm is trapped and revascularized with a petrous-to-supraclinoid (C3-C5) carotid bypass with a saphenous vein graft or, alternatively, with a cervical-to-supraclinoid carotid bypass. (c) The supraclinoid ICA is trapped
and revascularized with a superficial temporal artery to middle cerebral artery (STA-MCA) bypass or, alternatively, with an STA-MCA bypass with a saphenous vein interposition graft. (d) The MCA aneurysm is trapped and revascularized with a double-barrel STA-MCA bypass
or, alternatively, with an anterior temporal artery-to-MCA in situ bypass. (e) The anterior cerebral artery (ACA) aneurysm is trapped and
revascularized with A2-A2 in situ bypass. ECA External carotid artery; saph saphenous; supraclin. a supraclinoid artery; ophth. a ophthalmic
artery; PCoA posterior communicating artery; Ant. Temp. A anterior temporal artery; ree. a recurrent artery of Heubner, and A CoA anterior
communicating artery. With permission from Barrow Neurological Institute
154
./
-.-~
--
Fig. 8. Surgical approaches to revascularization of the posterior circulation. Overview showing the posterior circulation and common locations
for aneurysms. (a) The midbasilar artery is occluded proximally or distally to the aneurysm and revascularized with an superficial temporal
artery-to-posterior cerebral artery (STA-PCA) bypass or superficial temporal artery-to-superior cerebellar artery (STA-SCA ) bypass. (b) The
vertebral artery aneurysm is trapped (clips on proximal vertebral artery and at origin of posterior inferior cerebral artery ( PICA ) , and endovascular coils distally in vertebral artery) and revascularized with a PICA-PICA in situ bypass. Alternatively, an occipital artery-to-PICA bypass is shown. SCA Superior cerebellar artery; AICA anterior inferior cerebellar artery; vert. a vertebral artery. With permission from Barrow
Neurological Institute
mally in the neck and distally along the petrous carotid can be revascularized with a cervical-to-petrous
carotid bypass, remaining entirely extraduraL Intracavernous aneurysms can be trapped and bypassed
with a (C5) petrous-to-supraclinoid (C3) carotid bypass. The proximal clip is placed on the petrous carotid
artery, and the distal clip is placed on the ICA proximal to the ophthalmic artery to preserve the collateral
blood flow from the external carotid system. If the
petrous ICA is friable or difficult to anastomose, a
cervical-to-supraclinoid ICA saphenous-vein bypass is
another option.
Revascularization of the supraclinoid ICA and
MCA territory is achieved with a superficial temporal
artery (STA)-MCA bypass. A saphenous-vein interposition graft increases the caliber of the bypass vessel
and delivers blood flow deeper within the Sylvian
fissure. Alternatively, a "double-barrel" STA-MCA
155
culation is accomplished with a bypass from the occipital artery to the PICA. In addition, the PICA vessels
run in the posterior midline in proximity to each other,
enabling a side-to-side PICA-to-PICA anastomosis to
be performed. These lower vertebrobasilar bypasses
enable the sacrifice of one vertebral artery as part of
a proximal aneurysm occlusion. The PICA origin
ipsilateral to the aneurysm is clipped proximally to
prevent retrograde filling of the aneurysm from the
bypass. It is possible to anastomose the occipital artery
to the anterior inferior cerebellar artery, but this
bypass is technically difficult.
15.
16.
17.
18.
19.
20.
References
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
156
46.
47.
48.
49.
50.
51.
52.
53.
Correspondence: Robert F. Spetzler, M.D., Neuroscience Publications, Barrow Neurological Institute, 350 W. Thomas Road,
Phoenix, AZ 85013-4496.
Summary
The introduction of the operating microscope, the principle of
early surgery, specialized intensive care units, the calcium antagonist
nimodipine, the sophisticated pre- and postoperative management
and an aggressive antiischemic pharmacological management have
substantially reduced morbidity and mortality after aneurysmal
subarachnoid hemorrhage (SAH). In spite of this progress, many
patients after rupture and surgical repair of an intracranial aneurysm
exhibit substantial cognitive deficits and emotional problems although their neurological outcome was rated as good according to
the Glasgow Outcome Scale (GOS = I). Therefore, a comprehensive
neuropsychological examination is called for in order to evaluate the
factual functional outcome after SAH. Neither focal brain damage
associated with aneurysm location nor surgery but the hemorrhage
itself and related events can be regarded as the most important causal
factors for the late result after SAH. In contrast to the mild permanent effects of aneurysm surgery, the initial bleeding itself seems to
have substantial lasting adverse neurobehavioral effects after. In
concordance with other authors our own data stress the strong predictive power of the bleeding pattern such as the presence of intraventricular and/or intracerebral blood on the functional outcome
after aneurysmal SAH.
Keywords: Aneurysm rupture; subarachnoid hemorrhage; early
surgery; cognitive deficits; quality oflife.
Introduction
Since the last 25 years the progress made in the
neurosurgical management of aneurysmal subarachnoid hemorrhage (SAH) has been associated with a
substantial reduction of morbidity and mortality. The
introduction of the operating microscope, the concept
of early surgery, specialized intensive care units, the
calcium antagonist nimodipine and a sophisticated
pre- and postoperative management including hypervolemia, hemoclilution and induced hypertension
(triple-H therapy) have increased the survival of the
catastrophic event SAH [20, 28, 29, 58, 59]. In the
meantime, 50-60% of the patients affected by the rupture of one or more intracranial aneurysms can be re-
158
B. O. Hiitter et al.
No.
o;()
Initial SAH
Surgical complications
Vasospasm
Medical complications
Unknown
18
6
4
4
4.6%
1.5%
1%
1%
0.3%
Post-operative mortality
33
8.4%
159
robehavioral morbidity after aneurysmal SAH, reaching from prevention of the deleterious event SAH to
improved recognition of warning bleeding, a reduction
of the encephalopathy resulting from the bleeding and
related events to improved rehabilitation and psychosocial counselling.
After cerebral computed tomography (CT) was introduced, SAH is diagnosed more readily and with
greater reliability. Moreover, the amount of blood and
its anatomical distribution can be determined accurately. Several clinical studies have addressed the relationship between the extent of the hemorrhage, as
assessed by means of CT scans, and the outcome,
incidence of vasospasm, and occurrence of chronic
hydrocephalus in patients with SAH. Various methods
have been used to estimate the quantity of extravasated blood following aneurysm rupture using CT.
Some authors measured the density at a single point in
the subarachnoid space in Hounsfield units [95].
Others evaluated the thickness oflayers of blood in the
basal cisterns [25, 26, 32]. While some scoring systems
quantify solely the amount of cisternal blood [32, 38],
others also consider the presence of cerebral hematomas and/or intraventricular hemorrhage [25]. Until
now, the CT score introduced by Fisher et al. in 1980
[25] is by far the most commonly applied instrument to
grade the severity of SAH based on morphological
criteria and has proved to be a valid prognostic indicator [2, 3, 25, 28, 36]. On the other hand, this grading
scale (as many others with a limited number of categories) is inadequate to reflect the variability concerning anatomical distribution as well as quantity of
intracranial blood following SAH [114]. A more sophisticated method for assessing the severity of SAH,
according to which the amounts of blood in 10 basal
cisterns and fissures are graded separately, has been
proposed by Hijdra et at. [38].
We recently performed an analysis of 251 patients
with SAH to investigate the relationship between the
initial CT findings and the clinical course which
yielded a significant correlation between the amount of
cisternal blood as determined by the grading system of
Hijdra et al. [38] and the clinical grade according to
Hunt & Hess (Spearman correlation coefficient r =
0.35; p < 0.001). A likely explanation might be that
the extravasation of a greater volume of blood is asso-
Intraventricular Hemorrhage
160
B. O. Hutter et al.
Table 2. System for Grading Amount of Intraventricular Blood According to Le Raux et al. [64 ]
Score*
Description
2
3
4
161
162
study of patients with severe and prolonged vasospasm, we found that patients who had been treated by
means of aggressive catecholamin-induced hypertension at the onset of dopplersongraphically defined
vasospasm (as compared to a historical control group)
exhibited an insignificant trend (p = 0.065) for a better
neurological result at discharge (GOS) and a significantly better self-rated quality of life in the areas
mobility (p <0.05) and free-time activities (p < 0.05).
The partner-rated overall quality of life in these
patients was significantly better (p = 0.012) than in the
conventionally treated patient group [61]. The above
mentioned pathophysiological considerations, empirical evidence from clinical studies and our positive experiences confirm our opinion that the role of vasospasm as a leading factor for a poor outcome after
aneurysmal SAH is overestimated. State-of-the-art
early surgery, postoperative medical management
based on TCD guided hypertension combined with
nimodipine prevention provides a promising concept
to further reduce the number of patients afflicted by
this complication.
Neurological Results in Poor-Grade Patients
(Hunt&Hess Grades IV or V)
Various clinical studies in poor-grade patients have
clearly demonstrated that re-bleeding and vasospasm
are the leading and most serious complications of
aneurysmal SAH [7, 19,29]. However, the attitude of
early treatment of the ruptured aneurysm is still controversial, although conservative treatment in poorgrade patients exerts a significant unfavorable influence on morbidity and mortality. Several authors
found a mortality rate of nearly 100% in their nonsurgical group, and concluded that half of these patients would, in retrospect, have profited from surgery,
because they died of vasospasm and re-bleeding [7, 99).
An often mentioned argument against early surgery in
poor-grade patients is the expectation of difficult surgical conditions in the acute stage of a severe SAH
with the awareness of possible fatal results, and a
marked rate of severely disabled patients [99, 107].
In our department, we follow the policy of early
surgery also in selected poor grade patients with
aneurysmal SAH. This aggressive surgical policy is, in
our opinion, warranted by the results of an 8-year
consecutive series of 76 prospectively evaluated poorgrade patients, who have been operated upon early
(within 72 hours) in our department. The indication
B. O. Hiitter et al.
Good
Fair
Poor
Dead
Grade IV
(n= 44)
n
10
10
17
7
Grade V
(n = 32)
n
23
23
39
16
4
8
8
12
13
25
25
38
Good
Fair
Poor
Dead
Grade IV
(n= 44)
n
16
13
6
9
Grade V
(n = 32)
n
36
30
14
20
8
4
8
12
25
13
25
38
surgical and medical management policy in poorgrade patients after aneurysmal SAH. In our series, ten
(13%) patients showed an immediate postoperative
deterioration and in a further 5 (6.5%), recovery was
markedly impaired, resulting in a permanent disability
in two and lethal outcome in three. In half of the patients with immediate postoperative deterioration, the
worsening of the clinical state was transient and resolved during the hospitalisation period. Immediate
postoperative deterioration was related to surgical
problems such as massive hemorrhage (1%) due to a
prematurely ruptured aneurysm, prolonged temporary
clipping (3%), major vessel occlusion (4%) and the
closure of small perforating vessels or local compression by spatula (5%). Sixteen (21%) patients presented
delayed postoperative deteriorations due to infection
(1%), rebleeding (3%), vasospasm (3%), edema (7%)
and hydrocephalus (7%). Especially in poor grade patients, the timing of surgery after aneurysmal SAH
must be decided in every individual case anew. Delayed surgery is favoured in the hope that the patient
will recover to a better clinical condition with a decreased postoperative mortality. However, if the patient dies from rebleeding or vasospasm during the
waiting period, the reproach will remain, because we
have lost this patient due to inactive treatment. The
risk of rebleeding is highest around the fourth to the
tenth day, with an additional peak within the first 24
hours after the initial SAH [19, 29, 67]. Most grade IV
and V patients have a great amount of subarachnoid
blood. Consequently, patients in Hunt&Hess grades
IV or V frequently will develop severe or even fatal
complications and should therefore be treated by early
surgery [83, 99, 107]. Furthermore, the prevention of
delayed neurological deficits by aggressive treatment
of vasospasm is only safe with a sufficiently clipped
aneurysm. In our series, only one patient showed a
postoperative deterioration and finally died due to
symptomatic vasospasm. Another problem that may
be improved by early surgery because of the possibility
to remove blood clots from the subarachnoid cisterns
and ventricles and to open the lamina terminalis is the
impairment of CSF, especially in poor-grade patients
with an increased risk for consecutive hydrocephalus.
In addition to the overall mortality rate, there is a
further aspect, the frequency of postoperatively permanently severely disabled patients. Totally, 18% of
our patients remained in a poor condition, seriously
handicapped with all medical, psychological, ethical
and financial problems of long lasting nursing and in-
163
164
B. O. Hutter et al.
Table 5. Frequency of Cognitive Deficits in Neurologically Intact Patients in the Chronic State After SAH in whom Comparable Tests were
Employed
Cognitive function tested
Sonesson et al. ,
1985 (N = 40)
Concentration
Figural short-term memory
Verbal long-term memory
Aphasia
Perceptual speed and accuracy
130/0-25%
53%
30%
Ogden etal.,
1993 (N = 66) #
not comparable
7%-13%
53%
21%
10%
28/0-62%
47%
18%
7%
44%-76%
not examined
40%-45%
# 58 patients had a good (GOS = J) and 6 patients a fair (GOS = II) neurological result while 2 patients were dependent.
(GOS = I) in the chronic state after SAH when comparable neuropsychological tests have been employed.
The general conclusion that can be drawn from this
comparison is that impairments of short-term memory
and cognitive speed seem to be the most frequent longterm sequelae of SAH and that short-term memory
tends to be more often defective than long-term memory [62]. This pattern of neuropsychological impairments seems quite similar to the mental late sequelae of
mild to fair head injury [109]. On the other hand, the
discrepancies in the reported frequencies of substantially impaired patients can mainly be attributed to
differences between the tests employed and the criteria
used for defining a single cognitive deficit. In the study
by Hutter and Gilsbach [41] multivariate analyses
proved significant harmful effects of the severity of the
bleeding as rated according the the CT grading system
of Fisher [25] on information processing and wordfinding capacity. This could be interpreted as an indication for the detrimental effect of the subarachnoid
blood on the brain, especially on frontobasal structures. Older patients at the time of SAH were at follow-up significantly more disturbed in concentration,
short-term memory and information processing capacity [41]. Similar results have also been reported by
Bomstein et al. [11]. Neither the grade of vasospasm,
even if severe, the neurological grade on admission
(Hunt&Hess), the interval between SAH and investigation nor the gender of the patients had any significant influence on neuropsychological test performance
at follow-up [11].
The cognitive functional level of patients after SAH
and the classification of their outcome as good (GOS =
I) may diverge completely with regard to the neuropsychological and psychosocial late result. This apparent discrepancy challenges the neurological status
of SAH patients as the gold standard for the evaluation of disease sequelae and treatment outcome [41].
Therefore, a comprehensive neuropsychological examination is called for in order to evaluate the factual
outcome after SAH.
The Profile of Neuropsychological Impairments After
SAH
Beyond methodological differences, most neuropsychological studies converge in the finding that SAH
patients are particularly impaired in functions of
memory, attention, concentration and cognitive speed
and flexibility [8, 11, 18,62,68,97, 104, 105, 110, 117].
According to the studies of Hutter and coworkers [41,
43] the neuropsychological impairments in SAH patients were most prominent in the complex choice reaction time task and figural short-term memory. These
findings are in accordance with data of other research
groups [11, 68, 87, 97, 104, 105, 110, 117]. In a retrospective study 58 patients after SAH were examined
neuropsychologically one to five years after the acute
event [43]. There were 38 (65%) early (within 72 hours)
operated patients and 20 (35%) patients with spontaneous SAH of unknown origin. The neurological outcome rated according to the GOS at 6-month followup was good (GOS = I) in 48 (83%) and fair (GOS =
II) in 10 (17%) patients. Most deficits (46%) emerged
in figural short-term memory and in different parameters of a complex choice reaction time task reaching
from 31 ~65% of significantly disturbed patients. Verbal long-term memory was impaired in 28% of the
patients. The Token test revealed an aphasic language
disturbance in six (10%) patients after SAH. Only 9
(15%) patients presented with no single cognitive deficit. On the other hand, the mean scores of all neuropsychological tests were with one exception in the
normal range [43]. Vilkki et al. [117] reported similar
results in a sample of 83 SAH patients. The authors
found that deficits in memory functions and cognitive
165
Table 6. Cognitive Functions Tested, Neuropsychological Tests Used and Frequency of Cognitive Deficits in the Acute and Chronic Stage After
Early Aneurysm Surgery in Patients whose Neurological Result had been Rated as Good (GOS = /) at the 6-Month Follow-up
Cognitive function
Neuropsychological test
Speed of concentration
Accuracy of concentration
Error-reduced concentration
Aphasia screening
Verbal long-term memory
Figural short-term memory
3
11
3
9
15
20
3
2
4
3
6
16
11%
39%
11%
32%
54%
71%
10%
7%
13%
10%
21%
53%
Deficits in functions of attention were not comparable because of different tests used
# A cognitive deficit was defined as a test performance two standard deviations or more below the population mean according to the test
norms; the Benton and the Token test have individual cutt-offvalues.
166
B. O. Hutter et al.
Table 7. Neuropsychological Impairments in Patients After SAH of Unknown Origin and After Aneurysm Rupture
Authors
No. 1
Clinical
condition (H&H)2
GOS
(interval) 3
Non-aneurysmal
SAH
Aneurysmal
SAH
Spallone
eta!., 1986
56
I-IV
I-II
2.6-15
50% headache
50% mental alowing
not examined
Eskesen
et al., 1984
42
I-IV
I-II
0.6-5
44% headache
41 % mental slowing
29% reduced mental capacity
15% aphasia
not examined
Sones son
et al., 1989
20
I-III
Ogden
eta!., 1990
Hutter
etal.,1994
20
0.3-7
I-IV
5
I-III
I-II
1-5
108, 117]. Several studies have shown that these emotional problems and subjective complaints are also
frequent when the neurological and/or cognitive impairment is relatively slight [11, 43, 75, 86, 104, 108,
117]. Ljunggren et al. [68] reported that 25% of their
SAH patients with a good neurological outcome complained in clinical interviews of emotional problems.
Bornstein et al. [II] found frequent emotional disturbances in SAH patients using a clinical interview
and the Minnesota Multiphasic Personality Inventory
(MMPI). In a further study Vilkki and coworkers
[117] described personality disturbances and emotional problems in 32% of their patients after SAH using standardized personality tests. Stegen and Freckmann [108] found in a collective of 87 SAH patients
with an almost good neurological recovery changes in
mood in 51 %, depression in 36% and changes in social
behavior in 98%. Ropper and Zervas [93] investigated
a series of 112 consecutive cases after aneurysmal SAH
with a good neurological recovery and saw in 25%
substantial emotional disturbances. In a study exploring the emotional adjustment of 58 patients one to five
years after SAH, emotional lability was significantly
increased in 48%, motivation was significantly reduced
in 41 % and life-satisfaction in 37% [43]. Of the 58 SAH
patients studied, 17 (30%) were identified as depres-
167
168
B. O. Hutter et al.
Journal
Year of
publication
Richardson
Hutter & Gilsbach
DeLuca
Odgen et al.
Hutter & Gilsbach
Satzger et al.
Tidswell et al.
Hutter & Gilsbach
Hutter
1989
1992
1992
1993
1995
1995
1995
1996
in press
studies the patients after AcoA aneurysm rupture presented apart of their confabulatory memory syndrome
with additional deficits in neuropsychological tests
measuring frontal functions [6, 56]. The authors assumed, that the frontal lesions do not necessarily have
to be so extensive, that they can be recognized on CT
scans [6, 56]. In a single-case study of Vilkki [116], all
five patients with an operated AcoA aneurysm had a
postoperative Korsakoff syndrome. In three of them, a
postoperative CT scan showed frontal defects.
However, most of these studies are flawed by several
factors: 1. many have been performed before the introduction of the operating microscope; 2. many
studies are only casuistic and not based on consecutively treated patients - therefore, the cases presented may be selected and in fact not typical for AcoA
patients; 3. nearly all studies lack an adequate control
group in order to demonstrate typical neuropsychological sequelae of rupture and surgical repair of
AcoA aneurysms. An adequate control group
should be composed of patients with ruptured aneurysms of other locations and of patients after spontaneous non-traumatic SAH of unknown origin in order
to control for the effects of the bleeding itself. An increasing number of studies performed during the last
10 years have been unable to find more memory disturbances or more severe neuropsychological impairments in AcoA patients. Table 8 gives an overview of
those publications where the AcoA patients did not
differ from patients with aneurysms at other locations
in terms of neuropsychological impairment including
memory.
Richardson [91] found no statistically significant
differences in the postoperative impairment in a verbal
recall task in patients with different aneurysm loca-
donment of trapping procedures of the aneurysmbearing vessel and the principle of early surgical repair
[27-29,40, 59]. Neuroanatomical studies have shown
that there is a supply of structures near the anterior
wall of the III. ventricle by perforating arteries, which
originate from the AcoA [16, 90]. They supply the
anterior hypothalamus, septum pellucidum, anterior
parts of the cingulate gyrus, sections of the fornices
and the anterior parts of the corpus callosum [70]. Recently, neuroanatomical evidence was provided that
the perforators stemming from the AcoA primarily
supply the basal nucleus of Meynert [50]. This structure can be supposed to be of critical importance for
memory processing [48]. These findings prove a neuroanatomical basis for the neuropsychological deficits
in AcoA patients described in earlier studies. The use
of the operating microscope and of modern
aneurysm clips help the neurosurgeon to prevent
damage to the small perforators originating from the
AcoA and, therefore, to minimize the patient's risk for
a postoperative Korsakoff-syndrome [27, 40]. Evidence for the relevance of different surgical techniques
in aneurysm surgery for the neuropsychological outcome in patients with ruptured AcoA aneurysms
was presented first by Gade [27]. The author found a
close relationship between intraoperative trapping of
the AcoA and postoperative memory disturbances.
If trapping of the aneurysm was performed, 9 (81 %) of
11 patients showed a postoperative amnestic syndrome. Of the 37 patients, where the neck of the
AcoA aneurysm was operated by ligation, only 6
[16%] cases presented with an postoperative amnesia
[27].
Early and Late Effects of Surgical Procedures and
Events in Aneurysm Surgery
169
46, 71, 97]. The only relevant finding is that the careful
clipping of AcoA aneurysms sparing the perforating
arteries originating from the AcoA and the Al segment seems to prevent massive memory disturbances
and/or psycho organic syndromes [27, 40]. Regarding
the overall effect of early aneurysm surgery, indirect
evidence supports the assumption of only marginal
additional adverse effects of aneurysm surgery because
in several studies patients after spontaneous nontraumtic SAH of unknown origin showed comparable
deficits to patients after aneurysmal SAH [42, 86, 105].
However, a direct attempt to explore possible neuropsychological effects of aneurysm surgery on cognition has rarely been performed. Maurice-Williams et
al. [71] examined 27 patients after aneurysmal SAH in
a prospective study with one preoperative and two
follow-up examinations on the day before discharge
and one year later. All patients were operated upon
late without any surgical complications. At the time of
postoperative assessment, 11 (41 %) patients performed
substantially worse as compared to their preoperative
level and one presented with a newly developed aphasia. Persistent deficits were explained by prolonged
intraoperative ischemia, prolonged fixed retraction of
the dominant hemisphere and inadvertent occlusion of
the right choriodeal artery [71]. The authors could not
find any relationship between cognitive postoperative
performance and the degree of induced hypotension
and intraoperative aneurysm rupture [71]. In a study
by Hutter and Gilsbach, a series of 28 patients was
examined neuropsychologically one to 13 days (median 5 days) after early (within 72 hours) aneurysm
surgery [46]. Plegias, other severe neurological impairments, fluent aphasia or acute psychosis were exclusion criteria. The neurological outcome of all patients
at 6-month follow-up was good (GOS = I). Induced
hypotension was never employed during surgery. Four
years after surgery the patients were examined in a
follow-up study for their quality oflife by means of the
Aachen Life Quality Questionnaire (ALQI) [45, 47].
No substantial effect of premature aneurysm rupture
or surgical approach (left versus right pterional), neither on the acute neuropsychological performance nor
on the later quality of life could be revealed. Temporary clipping of vessels was used in 18 (64%) operations. The mean occlusion time of one vessel was 2.8
minutes with a range between two and 13 minutes. If
temporary clipping was employed, the patients performed significantly worse in the concentration and
alertness task as compared to those patients in whom
170
B. O. Hutter et af.
171
patients suffer from persistent neurobehavioral impairments after aneurysm rupture. Even a good neurological result (GOS = I) does not exclude substantial
mental impairments. Therefore, we suggest a comprehensive neuropsychological assessment after SAH in
order to obtain information about the factual functionallevel of the patients. Adverse neuropsychological effects of aneurysm surgery remain relatively weak,
if performed by a skilled neurosurgeon using modern
microneurosurgical techniques. In contrast to the
weak permanent effects of aneurysm surgery, the severity of the bleeding, its anatomical pattern and the
initial neurological state have the main prognostic
impact for the neurological and neurobehavioral
functional late outcome after aneurysmal SAH.
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174
106.
107.
108.
109.
110.
111.
112.
Author Index
Aaslid, R. 47
Curcic, M. 123
Dolenc, V. V. 89,99
Ekseth, K. 107
Enblad, P. 73
Gilsbach, J. M. 157
Kaku, Y. 123
Kiss, M. 123
Kreitschmann-Andennahr, I. 157
Langmoen, 1. A. I, 107
Lawton, M. T. 141
Le Roux, P. D. 7
Lindegaard, K.-F. 59
Loch Macdonald, R. 27
Lundar, T. I
Mayfrank, L. 157
Rohde, V. 157
Roth, P. 123
Spetzger, U. 157
Spetzler, R. F. 141
Steiger, H.-J. 81
Stoodley, M. 27
Taub, E. 123
van Loon, J. J. L. 81
Hauglie-Hanssen, E. 107
Hiitter, B. O. 157
Nomes, H. 107
Weir, B. 27
Winn, H. R. 7
Imhof, H. G. 123
Persson, L. 73
Yonekawa, Y. 123
Index of Keywords
Hemodynamics 47
Hemoglobin 27
Humans 59
Hypothermic circulatory arrest 141
Revascularization 141
Review article 59
Carotid-ophthalmic aneurysm 89
Cavernous sinus 99
Cerebral aneurysm 1,59,81,107
Cerebral arteriovenous malformations
Cerebral pathophysiology I
Cerebral vasospasm 59
Cerebrovascular spasm 47
Clinical 59
Clinical grade 7
Cognitive deficits 157
Computed tomography 81
Nitric oxide 27
Ophthalmic artery 89
Posterior circulation aneurysms 123
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Intracranial Pressure
and Neuromonitoring in Brain Injury
Proceedings of the Tenth inlernationallCP Symposium,
Williamsburg, Virginia, May 25-29, 1997
Haruc(I,"er DM 320.- . !IS 2240,lIeducro price for subsc ribers 1<) "Acta Neuroch;ru rgi~a": DM 288.-. OS 20 16.-
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intens ive care as well as the c urrent stale of knowledge in neurochemical and oxygen monItoring of the injured brain. Recent advances In molecular mechanis ms of injury and the pathophYSiology of ischemia and trauma are also included.
Contents
Manageme nt of ICP and CPP
I CP Measurement Techni(IUeS
Neuromonitoring in Inte ns ive Care
Traumatic Brain Inju ry
Brain Oxyge n Monitoring
Molecular Mechanisms of Injury
Cerebral Blood Flow and Metabolism
Micro<lialysis in Brain Injury
Near Infra-He(j Spectroscopy
Biophysical Modeling of ICP
Pathophys iology of ICP
. T... ,. II 3.l-IJ."-"-<_."'""',.h
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Brain Edema X
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Acta Neurologica Belgica
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AnaeSlhesia and Inle nshe Care
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Volume 23
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SpaceOccupying Lesions of the Sensori-Motor Hegion (U. Ebel ing, H.-J. Reulen)
Technical Standards
The Surgery of Ca"emomas Both Supra-Tentorial a nd Infra-Te ntorial (J.P. Uoulteville)
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Hearing Preservation in Acoustic Tumour Surgery (t.! . Samii. C. Matthies)
~ Springer\\
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Volullle 25
Edited by f. Cohadon (Ed itor-in-Chid), V. V. Dolenc, 1. Lobo Antunes, H. Nomes,
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1999. XI V. 241 Seitell.
/\d vances
Treatment of diseases of the central nervous system using encapsulated cells
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Chronic Deep Brain Stimulation for Move ment Disorders
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Hecent Advances in the Treatment of Central Ne rvous System Genn Cell Tumors
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The Septal Hegion and Memory (D. Y. von Cramon, U. !'I1iiller)
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(J.M. Derlon)
Use of Surgical Wands in Ne urosurgery (I.. Zamorano, F. C. Vinas, Z. Jiang, F. C. Diaz)
Technical Standards
The Endovascular Treatment of Brain /\ rteriovenous Mulfonnations
(f\ . Valavanis, ~1. C. Yasargil)
The lnterventionul Neu roradiological Treatment of Intrac ranial Aneut)'sms (C. Guglielmi)
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