:Acta .
.
Ncurochlrurglca

Acta Neurochir (Wien) (1995) 133:206-210

9 Springer-Verlag 1995
Printed in Austria

Frequent TIA in the Territory Fed by the Anastomosed STA After
Combined Therapeutic ICA Occlusion and Extracranial-Intracranial Bypass:
Case Report
S. Takeuchi 1, R. Tanaka 1, T. Koike 1, H. Abe 1, T. Sorimachi ~, Y. Yoneoka 1, and I. Odano 2
~Department of Neurosurgery, Brain Research Institute and 2Department of Radiology, School of Medicine, Niigata University, Niigata,
Japan

Summary
Frequent transient ischaemic attacks (TIAs) in the territory fed
by the anastomosed superficial temporal artery (STA) after combined therapeutic internal carotid artery (ICA) occlusion and extracraniaMntracranial bypass is described in a 52-year-oldwoman with
a giant aneurysm in the supraclinoid portion of the left ICA showing
impairment of visual acuity in the left eye and right upper quadrantanopia. After the balloon test occlusion of the left ICA which
was tolerated, the left STA-middle cerebral artery anastomosis was
performed and occlusion of the left ICA using detachable balloons
was carried out a day later. TIAs corresponding to the territory fed
by the anastomosed STA occurred nine times two to four days and
five times eight to nine days after the ICA occlusion without new
infarction on computed tomography (CT) scan. Single-photon emission computed tomography showed no hypoperfusion immediately
after the initial TIA. CT scan revealed thrombosis of half of the
aneurysm a day after the ICA occlusion. The patient developed the
same TIA as previously by compression of the left anastomosed STA
at the time of follow-up angiography which was carried out eight
days after the occlusion. Although heparin was continuously administered after the ICA occlusion for two days, the initial TIA
occurred during heparinization.
Anticoagulation seemed to be inadequate judging from activated
coagulation time and incomplete thrombosis of the aneurysm occurred during heparinization. It is likely that the TIAs are caused
by embolism via the STA, which is a rare ischaemic complication.
Keywords: Giant cerebral aneurysm; carotid artery occlusion;
extracraniaMntracranial bypass; cerebral embolism.

Introduction
A l t h o u g h the accepted m e t h o d of t r e a t m e n t for
giant carotid a n e u r y s m s is surgical clipping if it is feasible, u n c l i p p a b l e carotid a n e u r y s m s have recently been
treated by occlusion of the i n t e r n a l carotid artery (ICA)
with or w i t h o u t a n e x t r a c r a n i a l - i n t r a c r a n i a l (EC-IC)
bypass p r o c e d u r e 1' 3, 4, 6, 7, 9, 12. However, therapeutic

occlusion of the I C A carries some s u b s e q u e n t risk of
cerebral ischaemic complications in spite of E C - I C
bypass 3, 6, 7. Pathogenetic m e c h a n i s m s o f cerebral ischaemic events after therapeutic occlusion of the I C A
have been explained by h a e m o d y n a m i c or t h r o m b o embolic theory 2'8 10, b u t it is often difficult to determine
the true m e c h a n i s m of cerebral ischaemia in each case.
F u r t h e r m o r e , there has been n o report of a case whose
cerebral b l o o d flow was e x a m i n e d after the I C A occlusion d u r i n g ischaemic complications.
The p u r p o s e o f this paper is to report a case showing
frequent a n d t r a n s i e n t ischaemic events in the territory
fed by the a n a s t o m o s e d superficial t e m p o r a l artery
(STA) after c o m b i n e d E C - I C bypass a n d s u b s e q u e n t
therapeutic occlusion of the I C A using detachable balloons with cerebral h a e m o d y n a m i c study d u r i n g these
ischaemic events. The m e c h a n i s m s a n d p r e v e n t i o n of
the ischaemic events are discussed.

Case Report
A 52-year-old woman first noticed impairment of visual acuity
in the left eye affecting the nasal side of the left visual fieldin January,
1993. She presented herself to the Department of Ophthalmology at
Niigata University Hospital in April, and was transferred and admitted to the Department of Neurosurgery on May 14, 1993.
Examination
Visual acuity was 0.9 (corrected : 1.2) in the right eye and 0.2 in
the left which was unable to be corrected. There was right upper
quadrantanopia which was more severe in the left eye. Computed
tomography (CT) scan revealed an oval-shaped mass with homogeneous contrast enhancement in the left suprasellar region (Fig. 1).
Cerebral angiography demonstrated a giant aneurysm (31 x 27 •

S. Takeuchi etal.: Frequent TIA in the Territory Fed by the Anastomosed STA

207

Fig. 1. Computed tomography scan after contrast infusion showing an oval-shaped and homogeneously well enhancing mass in the left
suprasellar cistern. The image is presented as viewed from below
Fig. 2. Lateral projections of the left internal carotid angiogram, early arterial phase (left) and late arterial phase (right), showing a giant
aneurysm arising from a supraclinoid portion of the internal carotid artery and the delayed filling of the middle and anterior cerebral arteries

23 mm) in the supraclinoid portion of the left ICA and delayed filling
of the middle and anterior cerebral arteries (Fig. 2). Cross-filling of
the left hemisphere via the anterior communicating artery was good
in spite of a narrow horizontal segment of the left anterior cerebral
artery, but that via the posterior communicating artery was poor.
The test occlusion of the left ICA by balloon on May 19 was clinically
tolerated for one hour and ten minutes. The electroencephalogram
was unchanged during the occlusion. Single-photon emission computed tomography using 99mTc-hexamethylpropyleneamine oxime
(99mTc-HMPAO SPECT) images during the test occlusion showed
no asymmetric perfusion in either hemispheres in spite of a little
reduction in perfusion in the both frontal regions.

A left STA-middle cerebral artery (angular artery) anastomosis
was uneventfully performed on May 25. Controlled therapeutic ICA

occlusion was carried out on the morning of the May 26. The actual
balloon-catheter procedure was performed with the patient awake,
under local anaesthesia using femoral artery catheterization under
full anticoagulation with heparin. A goldvalve balloon GVB 9 (Laboratoire Nycomed Ingenor S.A., France) attached to a co-axial
catheter was placed through the introducer catheter and the first one
was located in the cavernous portion of the left ICA. The balloon
was inflated with contrast material to effect arterial occlusion and
was detached. Two further similar balloons inflated with contrast
material were detached at a more proximal site. A fourth one was
inflated with 2-hydroxyethylmethacrylate (HEMA) 14 and detached
in the cervical portion of the ICA. The patient showed no new
neurological deficits during the procedure, Since the left STA contributed to the parietal branches of the middle cerebral artery via
the patent bypass after occlusion of the ICA (Fig. 3), the left hemisphere was fed by both the right ICA and the anastomosed STA.

Fig. 3. Left external carotid angiograms, anteroposterior (left) and
lateral (right) views, demonstrating good filling of the middle cerebral
arteries in the parietal region through the anastomosed superficial
temporal artery

Fig. 4. Computed tomography scan before (left) and after (right)
contrast infusion indicating thrombosis in the posterior half of the
aneurysm

Operation and Balloon Occlusion

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S. Takeuchi etal.: Frequent TIA in the Territory Fed by the Anastomosed STA

Fig. 5. Single-photon emission computed tomography using 99 m Tc-hexamethylpropyleneamineoxime 2 days after occlusion of the left internal
carotid aneurysm showing no hypoperfusion in the left hemisphere and a little hyperperfusion in the left parietal region. The images are
presented as viewed from below as computed tomography scans

The aneurysm was not filled after the ICA occlusion. The patient
was subsequently anticoagulated by continuous intravenous infusion
of heparin (750-500 IU/hour). The activated coagulation time5 before and during the heparinization was 130 seconds and 140 to 170
seconds, respectively.

Post-ICA Occlusion Course
Postcontrast CT scan on May 27 revealed thrombosis of one
half of the aneurysm (Fig. 4). The patient developed numbness of
the fifth finger of the right hand without weakness for a few minutes
at 10 a.m. on May 28 (2 days after the ICA occlusion). 99rnTCHMPAO SPECT images immediately after the initial transient ischaemic attack (TIA) showed slight hyperperfusion in the left parietal
region and no hypoperfused area in the left hemisphere (Fig. 5).
However, the patient subsequently developed numbness of the Ist
and 2nd fingers of the right hand for a few minutes at 12 p.m.,
numbness of the same fingers as previously and slight dysarthria for
ten minutes at 2:50 p.m., and slight dysphasia and numbness of the
2nd to 5th fingers of the right hand for a few minutes at 7:25 p.m.
on the same day. Administration of heparin was stopped at 3 p.m.,
because incomplete thrombosis in the aneurysm and the proximal
segment of the occluded ICA was suspected to be one of causative
factors of these TIAs. Concentrated red blood cells separated from
400 ml of whole blood were transfused to improve anaemia on May
28. There was numbness of the 1st to 4th fingers of the right hand
for a few minutes at 9:25 a.m., numbness of all fingers of the right
hand and slight dysphasia for a few minutes at 6:05 p.m., slight
dysphasia for a few minutes at 8 p.m. on May 29, and numbness of
the 2nd to 5th fingers of the right hand for a few minutes at 12:10
p.m. on May 30. The patient developed dysphasia, finger agnosia,
right and left disorientation, acaleulia, apraxia from 2:30 p.m. to 7
p.m. on May 30. Emergency CT scan at 6:30 p.m. showed complete
thrombosis of the aneurysm and no lesion of the brain parenchyma.
There was no evidence of propagation of thrombus into the distal
ICA. The patient was free of TIAs from May 31 to June 2 while
the systemic blood pressure was relatively high compared with from

28th to 30th, and assumed a sitting posture on June 2. Since the
patient developed numbness of all fingers of the right hand for a
few minutes at 1:30 a.m. and 5:30 a.m., and slight dysphasia for a
few minutes at 7 a.m. on June 3, however, cerebral angiography was
carried out from 3 p.m. to 4:20 p.m. on the same day. The parietal
region of the left hemisphere was fed by the STA via the patent
anastomosis, and the stump of the left ICA showed smooth tapering
occlusion. The left hemisphere was fed by both the left STA and the
right 1CA. No aneurysm was filled in any angiograms. The filling
condition of the vessels shown in the 4-vessel study was the same as
that after the left ICA occlusion on May 26. When the left anastomosed STA was compressed by finger to make sure of the cause
of the TIAs, the patient developed slight dysarthria and dysphasia
30 seconds after the compression and then numbness of the 1st to
3rd fingers of the right hand one minute later. These signs gradually
disappeared after release of the compression. Concentrated red blood
cells separated from 400 mI of whole blood were transfused to improve anaemia, and 30 mg of aspirin therapy daily was started on
June 3. However, the patient developed numbness of all fingers of
the right hand and slight dysphasia for a few minutes at 12:45 p.m.,
and numbness of the 1st to 3rd fingers of the fight hand, dysphasia,
right and left disorientation, alexia from 5 p.m. to 5:30 p.m. on June
4. Then the patient was free of TIA and was transferred to another
hospital to be treated for mild liver dysfunction on June 16.
Although TIAs occurred during normotension, the systemic
blood pressure was relatively high during period free of TIAs. The
visual field defect and visual acuity in both eyes were aggravated
postoperatively, but improved soon. Visual acuity was 1.0 (corrected: 1.5) in the right eye and 0.3 (corrected:0.4) in the left 3
months later, and was 0.9 (corrected : 1,2) in the both eyes one year
later. Right upper quadrantanopia was the same 3 months later as
pre-operatively, and disappeared one year later. CT scan 5 months
later revealed a completely thrombosed aneurysm which was reduced
in volume. No abnormal lesion in the brain was detected.
The patient developed numbness of the 3rd and 4th fingers of
the right hand for an hour on January 3, 1994, in spite of the
administration of 30rag of aspirin and 100 mg of ticlopidine daily,

S. Takeuchi etal.: Frequent TIA in the Territory Fed by the Anastomosed STA
but had no more TIAs subsequently.99mTc-HMPAOSPECTimages
on January 11 showed no significant reduction in left hemispheric
perfusion in spite of slight symmetricalreduction in perfusion in the
both frontal regions. The patient showed no further symptoms or
signs when compression of the left STA for a few minutes was
undertaken.
Discussion

Mechanisms of Ischaemic Complications
The possible mechanisms involved in the ischaemic
cerebral complications after therapeutic carotid occlusion include inadequate flow in the hemisphere corresponding to the side of the carotid occlusion, the
development of throml~o-embolism or the both. Heros
reported twelve cases of probable embolic complications occurring during or after therapeutic occlusion
of the ICA by EC-IC bypass 7. In all twelve but two
cases, the complication occurred either during gradual
occlusion or within 48 hours of complete occlusion,
and it was felt that the complication occurred as a result
of propagation of the clot in the ICA or dislodgement
of an embolus from the distal tail of this clot or, less
likely, from the aneurysm itself. In none of the patients,
however, did the embolus travel through the bypass
graft itself. In our case, all the TIAs seemed to correspond to ischaemia in the territory fed by the anastomosed STA, and 99mTc-HMPAO SPECT study
immediately after the initial TIA showed no hypoperfusion in the hemisphere ipsilateral to the occluded
ICA. Moreover the patient developed the same TIA
as previously when compression of the anastomosed
STA was undertaken. It seems that emboli originated
from the stump of the proximal ICA migrated to the
vessels in the left parietal and the surrounding regions
via the anastomosed STA and caused transient ischaemia. Embolism via the anastomosed STA appears
to be rare. If a series of the TIAs was secondary to
emboli from the partially thrombosed aneurysm or emboli arising from the residual stump of the intracranial
carotid artery, the symptoms of the TIAs should be
more variable and correspond to the area other than
the territory fed by the anastomosed STA. Therefore
this assumption seems to be incompatible with the fact
that the TIAs occurred in the territory fed by the anastomosed STA. Although anaemia and dynamic
changes of the systemic blood pressure were present,
an idea of transient hypoperfusion only in the territory
of the anastomosed STA looked improbable. Furthermore TIA 7 months later should be an embolic episode
via the STA judging from the symptoms and signs and
the SPECT images at that time. Nishioka described

209

that 89% and 95% of all ischaemic complications occurred within four and seven days after the carotid
occlusion, respectively 1~ Moreover Landolt reported
that most of the transient complications occurred
within the first six hours after occlusion of the vessel 8.
Frequent and transient ischaemic events in our case,
which occurred nine times during 2-4 days, five times
during 8-9 days after the ICA occlusion and once 7
months later, might be rare.

Necessity of Bypass
In our case, the balloon test occlusion of the left
ICA was clinically tolerated and the electroencephalogram was unchanged. Furthermore 99mTc-HMPAO
SPECT images during the occlusion showed no asymmetric perfusion in the both hemispheres. Although the
permanent ICA occlusion without EC-IC bypass might
be safe, the STA-middle cerebral artery anastomosis
was performed before the occlusion because of lack of
hypotensive haemodynamic stress during the balloon
test occlusion, a possibility of late haemodynamic ischaemic complications, significant long-term haemodynamic reserve in the brain, and the danger of contralateral aneurysm formation.

Types of Occlusion of the ICA
There were two ways to occlude the carotid artery:
abrupt and gradual occlusion. According to Nishioka ~~ the incidence of ischaemic neurological deficits after carotid occlusion was found to be higher
when the occlusion was carried out abruptly than when
the artery was gradually occluded with a clamp, but
careful consideration of the variables of the interval
from last subarachnoid haemorrhage tended to negate
the differences. On the other hand, Landolt described
that the quick type of occlusion of the artery resulted
in a lesser complication rate than the slow type 8. When
the patient tolerates the balloon test occlusion, abrupt
occlusion may be safer than gradual occlusion because
the gradual occlusion bears the risk of development of
thrombus formation at the clamping site before completion of the occlusion.

Prevention of" Haemodynamic Ischaemic Complications
In an attempt to minimize the haemodynamic complications, various tests of cerebral perfusion have been
used. These include: Matas test, angiography before
and after carotid compression, measurement of the
stump pressure during the ICA occlusion 12' 13, cerebral

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S. Takeuchi etal.: Frequent TIA in the Territory Fed by the Anastomosed STA

blood flow measurements by a xenon-133 technique
before and after temporary ICA occlusion under general anaesthesia6, and the ICA balloon test occlusion
under local anaesthesia with SPECT study ll, with cerebral blood flow study by xenon CT ~3 or without cerebral haemodynamic study ~' 4. Although the cerebral
haemodynamic study during the test occlusion of the
ICA is useful, the study after permanent occlusion is
also important for managing of the postocclusion
course and prediction of haemodynamic complications.

Prevention of Thrombo-Embolic Ischaemic Complications
Patients who tolerate acute ICA occlusion may still
be vulnerable to propagating thrombosis or thromboembolism in the hours, days or even longer after the
occlusion. To prevent these complications, full anticoagulation with heparin followed by antiplatelet therapy I or administration of antiplatelet agents with lowdose heparin therapy4 have been proposed after occlusion of the ICA, especially balloon occlusion. Although
heparin was continuously administered after the ICA
occlusion in our case, anticoagulation seemed to be
imperfect judging from activated coagulation time during heparinization5 and incomplete thrombosis of the
aneurysm on CT scan. Thus an initial TIA is thought
to have occurred during inadequate anticoagulation.
Although full anticoagulation may be the best way to
prevent the thrombo-embolic complications after ICA
occlusion, there is a risk of postoperative intracranial
haemorrhage if it is done soon after the bypass surgery.
It is still unclear how long full anticoagulation is necessary. Furthermore anticoagulation delays thrombosis
of the aneurysm, which was seen in our case, and the
incomplete thrombosis of the aneurysm is possibly the
cause of embolic complications. No anticoagulation
may be an option of management after the ICA occlusion.
To reduce the cerebral ischaemic complication rate
after therapeutic occlusion of the ICA, some devices
are necessary. The ICA test occlusion with study of
cerebral haemodynamics is useful for predicting subsequent cerebral hypoperfusion. Furthermore the cerebral haemodynamic study after permanent occlusion
of the ICA is also important for predicting haemodynamic ischaemic complications. It seems that further
study concerning thrombus formation in the aneurysm
and the occluded site is needful to determine whether

or not anticoagulation and/or antiplatelet therapies are
useful and how long they are necessary.
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Correspondence: Shigekazu Takeuchi, M.D., Department of
Neurosurgery, Brain Research Institute, Niigata University, Asahimachi 1-757, Niigata 951, Japan.