0148-396X/87/2 106-08 39$02.00/0
NEUROSURGERY
Copyright € 1987 by the Congress of Neurological Surgeons

Vol. 21, No. 6, 1987
Printed in U.S.A.

Higher Cortical Disorders: An Unusual Presentation of an
Arteriovenous Malformation

J.J. v. Overbeeke, M.D., N. J. Bosma, M.D., A. F. M. M. Verdonck, M.D., and A. C. vy. Huffelen, M.D.

Department of Neurosurgery (JJO, NJB), Department of Neuropsychology (AFMMV), and Department of Clinical Neurophysiology (ACH),
University Hospital, Utrecht, The Netherlands

The authors present a patient with a large arteriovenous malformation in the temperoparietooccipital region of the
dominant hemisphere that caused seizures, a homonymous hemianopia, and broad neuropsychological disturbances
probably caused by a cerebral steal syndrome. There was no history of hemorrhage. Surgical resection resulted in
marked improvement of neuropsychological function and disappearance of the hemianopia. The authors discuss the
pre- and postoperative neuropsychological findings, the pathogenesis of the steal phenomenon, and the indications
concerning the resection of this large and deep-seated arteriovenous malformation in a functionally important region
of the left hemisphere. They state that surgical resection is the method of choice. (Neurosurgery 21:839-842, 1987)

Key words: Cerebral steal phenomenon, Intracranial arteriovenous malformation, Neuropsychological deficit, Resection

The interest in surgical management of arteriovenous mal-
formations (AVMs) has increased because of more frequent
and earlier detection, improvement in microsurgical vascular
operative techniques and anesthesiological techniques, and
understanding of the anatomy and hemodynamics of AVMs.
AVMs commonly present with intracranial hemorrhage, sei-
zures, vascular headache such as migraine, and progressive
heart failure in some cases. Far less attention has been given
to the presentation of progressive or fluctuating neuropsycho-
logical deficits as a result of a “cerebral steal” phenomenon.

We present an unusual case of neuropsychological deterio-
ration caused by a large temporoparietooccipital AVM situ-
ated laterally close to the border of the left ventricular trigone.
In addition to the risk of bleeding, the neuropsychological
disturbances indicated the necessity for surgical resection.

CASE REPORT

A right-handed, 16-year-old girl suffered from progressive
headache. One year after the onset of the headache, she had
a partial seizure with complex symptoms characterized by
loss of spatial orientation and consciousness. Later, a gener-
alized tonic-clonic seizure was noted.

Physical examination revealed no neurological deficit.
Some weeks afier the tonic-clonic seizure, the patient com-
plained of disturbances in writing, reading, calculating, and
spatial orientation.

On admission, she was found to have a complete right-
sided hemianopia, with no other neurological deficit. Electro-
encephalography (EEG) indicated functional disturbances in
both superficial and deep layers of the left temporal-occipital
region, with slight epileptiform characteristics. There was
asymmetry of the background activity in the posterior tem-
poral and occipital regions. The « rhythm at the left side was
much slower than that at the right side. Moreover, there was
an excess of irregular slow activity with a diminution of fast
activity at the left side. The photic driving reactions were also
asymmetrical. Sporadically, there were some sharp waves in
the left posterior temporal region. The computed tomographic
(CT) scan showed a tortuous enhancement close to the left
trigonum (Fig. 1).

The cerebral angiogram showed an AVM supplied by

839

branches of the left posterior cerebral artery draining into the
left transverse sinus (Figs. 2 and 3).

Neuropsychological investigation (Table 1) showed several
remarkable disturbances: there was an indication of deterio-
ration of intellectual cognitive functions, especially of the
performance tasks of the WISC-R, but also of verbal tasks.
She had a very short attention span. There were also some
indications of a disturbance of short term memory and of
retention of visual information. There were severe problems
in visual perception. Spatial perception and organization were
insufficient, and visual analysis and synthesis were severely
disturbed, probably because of the hemianopia. There was a
pathological narrowing of the range of the visual field and a
simultaneous agnosia; only small parts or details of objects,
figures, words, and numbers were perceived, and this only in
the left part of the visual field. There was a total alexia and
she even did not recognize normal symbols, words, or her
own writing: she could not read musical notes, although she
had played music for several years. Although her mental
arithmetic function was normal, she did not recognize math-
ematical and chemical formulas and constructions on paper.
Indications of constructive apraxia were also present. The
whole complex of neuropsychological disturbances was a clear
indication of a functional disturbance of the parietooccipital
region of the left hemisphere. There was dysfunctioning of
the left occipitotemporal region especially.

At operation (N.J.B.), a temporoparietooccipital craniot-
omy was performed. When the dura mater was exposed, the
intracranial tension was found to be too high. With the aid of
hypotensive anesthesiological techniques, the intracranial
pressure was lowered. After incision of the dura mater, a large
red draining cerebral vein was visible on the temporal lobe,
close to the sigmoid sinus. First, the left posterior cerebral
artery was exposed by means of a subtemporal approach. Two
feeding arteries coming from the posterior cerebral artery
were clipped. This procedure did not diminish the volume of
the draining veins.

Because of the high intracerebral pressure, the temporal
lobe could not be mobilized further. Therefore, other feeding
arteries could not be found under the temporal lobe.

A transtemporal approach along the draining vein to the
malformation was chosen. The malformation was found very

840 OVERBEEKE et al.

Fic. 1. CT scan with contrast enhancement showing a large left
parietal-occipital AVM.

Fic. 2. Venous phase of the left internal carotid angiogram show-
ing a large AVM draining into the left transverse sinus.

close to the left posterior portion of the lateral ventricle. First,
the feeding arteries were identified and clipped. When the
malformation was completely loose from the surrounding
brain tissue, the draining veins were coagulated, and the
malformation was removed as a whole. There were no signs
of previous bleeding from the anomaly.

On the Ist day after the operation, the hemianopia had
disappeared. EEG during the postoperative period showed an
asymmetry similar to that found before operation.

The neuropsychological investigation (Table 1) was re-
peated 3 weeks after the operation. There was improvement
in almost all functions, but cognitive functions were still less
than the estimated premorbid level and visual analysis and
synthesis were still weak; furthermore, information-processing
was slower than normal. Visual memory and reproduction of
visual information had improved, but were still not normal.
Concentration and attention span were better than before the
operation, but not yet normal. The simultaneous agnosia had
disappeared. There were no more signs of alexia and construc-
tive apraxia. Spatial perception and organization had im-
proved considerably. There were still disorders in interpreta-
tion, however: the understanding and use of written mathe-

Neurosurgery, Vol. 21, No. 6

Fic. 3. Left vertebral angiogram showing feeding branches from
the posterior cerebral artery to the AVM.

matical and chemical formulas and constructions was practi-
cally impossible.

Three months after the second neuropsychological investi-
gation, the patient had no more problems with visual percep-
tion, reading and writing, memory, and recognition of objects
and symbols. Dyscalculia and alexia had disappeared almost
totally, and spatial perception and orientation were normal.

One year after the operation, neuropsychological investi-
gation was repeated once more. Intellectual-cognitive func-
tions had improved, but the patient still showed somewhat
more difficulty in performance tasks (visuoconstructive tasks)
than in verbal tasks. All other functions were normal, except
attention span and pace of work. She was given counseling
for her school problems because of depression and emotional
problems that she developed after the operation. She still
receives psychological therapy. Antiepileptic treatment was
given, and the seizures did not recur.

DISCUSSION

The concept that an AVM can interfere with circulation in
the surrounding brain tissue has been discussed by several
authors (3, 5, 6, 16, 17, 23). Terms such as “parasite of the
circulation” and “thirsty lesion” have been used (5, 6). The
excessive shunt flow through the AVM causing a state of
permanent insufficient perfusion of viable tissue has been
termed “cerebral steal” (6). Nornes and Grip described the
hemodynamic aspects of cerebral AVMs (16, 17), stating that
the pressure drop in the feeding artery of an AVM is propor-
tional to the resistance of this vessel and the flow through the
AVM. A long feeding artery has a comparatively high resist-
ance due to friction. The shunt flow through the AVM is not
considered influenced by autoregulation. Therefore. the flow
is extremely pressure-dependent and can be high in a large
AVM. The flow through an AVM may range from | to 3

December 1987

TABLE
Neuropsychological Tests*

AVM CAUSING NEUROPSYCHOLOGICAL DISORDERS 841

1

Test At school Preoperative 3 wk postop 15 wk postop 10 mo postop
I. WAIS (subtests)
Digit Span 12 1 11 1 12
Arithmetic 10 10 10 10
Similarities 12 12 he 12
Block Design 10 10 11 12
Object Assembly 12 10 10 9 15
Digit Symbol 12 0 8 10 10
2; Bourdon- Wiersma (Dutch paper 1 2 3 3
and pencil attention-concen-
tration test)
3. Benton Visual Retention Test 1 2 2 4
4. 15 Words Auditive Verbal Mem- 1 5 4
ory Test
5; Hooper Visual Organization Test 2 3 3 3
6. Ayres Figure Ground Visual Per- 2 4 4
ception test
ws Grassi Block test 5] 4 4 4
8. Bender Visuo-Motor Gestalt test 2 3 3 3
9: Vigilance Task, Reaction Time 1 ps 2, 3
(continuous performance task)
10. Halstead-Reitan
Trailmaking 2 3 3 3
Tactual Performance 2 3 3 3
Finger Tapping 2 1 3 3
Lt. Motor Performance Task
Steadiness 3 4 4 4
Tapping 3 1 3 3
Trace Tracking 2 3 3 3
Pegboard 3 3 4 4

“ The neuropsychological tests were administered in the order listed. Scoring: much below average = |, below average = 2, average = 3, above

average = 4, much above average = 5.

litres of blood per minute, sometimes causing a serious load
on the heart (6). Thus, the greater the shunt through the AVM
and the larger the caliber of the feeding arteries, the greater
the pressure drop in the feeding arteries. The perfusion pres-
sure through the nutrient vessels of the surrounding brain
tissue is dependent on the arterial pressure minus the venous
pressure. In the case of a large AVM, such as in our patient,
the peripheral tissue perfusion is decreased because of a great
pressure drop in the feeding artery and an increased venous
pressure. Evidence of an increased venous pressure is obtained
from observations of dilated arteriolized veins produced by
the transmission of arterial pressure directly into the veins.

The permanent state of insufficient tissue perfusion may
cause several disturbances related to the location of the AVM.
Among these, real neuropsychological disturbances are less
commonly described. Several cases of intellectual changes
resulting from an AVM have been reported. There is a sparsity
of reported cases of documented neuropsychological deficit,
however. Most authors only report the possibility of or present
some examples of decreased intellectual function caused by
an AVM (2, 3, 11, 14, 25). The earlier literature reported
psychiatric disorders caused by AVMs. Tonnis reported per-
sonality changes in 9.5% of the patients with AVMs (22).
Hamilton Paterson found “dementional” disorders in 8% (8),
and Kelly found such disorders in 9.5% of patients with
supratentorial AVMs (10). Almost all authors refer to the
effects of the steal phenomenon as the cause of these disturb-
ances. In most cases, other deficits have been described, such
as seizures and neurological deficit.

The decision of whether to operate on a large AVM that

has not bled and is situated in functionally important regions
requires one to weigh natural risks against surgical risks (1, 2,
9, 11-13, 20, 24-26). The yearly rate of initial hemorrhage is
between 2% and 3%, with a considerable mortality and mor-
bidity of 10 to 30%. The accumulated risk of bleeding at 20
years is 37% (7, 12). The natural incidence of spontaneous
disappearance of intracranial AVMs is estimated at 2 to 5%.
This phenomenon is primarily caused by acute thrombosis,
with a time interval from diagnosis to disappearance of 7
months to 21 years (19). Although a large AVM is less likely
to bleed (12, 18), Drake frequently found blood around large
AVMs during excision (4). It is possible that symptoms as-
cribed to the steal phenomenon are really those of repeated
minor bleeding.

We do not agree with Ianesk that conservative treatment is
the appropriate management of an AVM that has not bled
(9). Apart from the considerable risk of bleeding in the case
of a young patient with an AVM there are other indications
for operation, such as disabling neurological and neuropsy-
chological disturbances.

Because of careful microdissection techniques, the use of
embolization as a preliminary step, hypotensive anesthesio-
logical techniques. and the peroperative avoidance of abrupt
hemodynamic changes by gradual occlusion of the feeders.
the surgical risk has been decreased considerably (2, 4. 11, 12.
15, 18, 20, 21, 25). The surgical mortality and morbidity has
ranged from 2% (20) to 11% (4) in many series (1. 2, 11. 13.
18, 21, 25, 26). The statistical variance depends on the pre-
operative condition of the patient, the location and size of the
anomaly, and the operative procedure.

842

OVERBEEKE et al.

To evaluate the pre- and postoperative state of patients

with AVMs in the temporoparietal region of the dominant
hemisphere, we used neuropsychological tests. We suggest the
following as the most useful: WAIS, Benton Visual Retention
Test. 15-Words Auditive Verbal Memory Test. Motor Per-
formance Task, Bender Visuo-Motor Gestalt Test, Grassi
Block Test, Reaction Time Test (continuous performance-
vigilance task), and some subtests of the Halstead-Reitan
Neuropsychological Battery (Trail Making, Tactual Perform-
ance, Finger Tapping, and Aphasia Screening Test).

To prevent hemorrhage and progressive ischemic damage

of the brain tissue adjacent to the AVM, we decided that
surgical removal of this anomaly was the method of choice.

Received for publication, October 21, 1986; accepted, June 23,

1987.

Reprint requests: J. J. v. Overbeeke, Department of Neurosurgery,

University Hospital, Catharijnesingel 101, 3511 6V Utrecht, The
Netherlands.

Nv

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COMMENT

The authors present a patient with a left temporoparietooc-
cipital arteriovenous malformation. The clinical presentation
consisted of a right homonymous hemianopsia, seizures, and
a severe left temporal parietal cognitive deficit. The arterio-
venous malformation had never bled. The importance of this
report lies in its recognition of and emphasis on the severe
disruption of the normal cortical functions occurring in the
temporoparietooccipital junction on the left side due to an
apparent steal phenomenon. The authors document the re-
versal of these cognitive deficits after removal of the arterio-
venous malformation. The authors’ conclusion, which is
clearly supported by this case report, is that the potential
reversible effects of the steal phenomenon due to arteriove-
nous malformation should be considered when decisions re-
garding the treatment of arteriovenous malformations are
being made.

Charles J. Hodge, Jr.
Syracuse, New York