0148-396X/85/1603-0293$02.00/0
NEUROSURGERY
Copyright ¢ 1985 by the Congress of Neurological Surgeons

Vol. 16, No. 3. 1985
Printed in U.S.A.

Microsurgical Excision of Paraventricular Arteriovenous
Malformations

Hoi Sang U, M.D.

University of California Medical Center, San Diego, California

Periventricular arteriovenous malformations (AVMs) have often been deemed inoperable because of their location in
critical structures. Furthermore, the excision of large lesions may be complicated by the potential for serious brain
swelling and hemorrhage due to “autoregulation breakthrough.” Nonetheless, the unfavorable natural history of the
untreated disease in a symptomatic young patient has induced us to approach these lesions using staged microsurgical
excision combined with elective barbiturate coma for maximal cerebral protection. Between 1979 and 1983, six patients
(four female. aged 12 to 60 years, and 2 male, aged 14 and 29) who harbored large AVMs in the basal ganglia, thalamic,
and hypothalamic areas presented with subarachnoid hemorrhage (2 cases), progressive neural deficits (3 cases), and
intractable headache (1 case). Nineteen staged operations were performed for the complete excision of these lesions.
Among the first three patients, there was one death due to “autoregulation breakthrough” hemorrhage into the lateral
ventricle during the excision of a lesion approached through the sylvian fissure using standard anesthesia techniques.
This led to the adoption of the transventricular surgical approach and elective barbiturate coma to facilitate exposure
of the lesion and to protect the adjacent vital structures from potential ischemia. Three patients were treated in this
fashion uneventfully. Of the five successfully treated patients, two have returned to their preoperative status and one
has completely recovered from global hemispheric ischemia and hemiplegia. The hemiparesis in one patient worsened
as a result of postoperative hypertensive intraventricular hemorrhage, and one patient developed mild dysphasia and
hemiparesis. This experience suggests that this approach offers a valid therapeutic regimen for the treatment of this
disease. During the same period, three patients—one man (age 23) and two women (aged 29 and 22)—harboring four
intraventricular AVMs presented with intraventricular hemorrhage. After the acute effects of chemical ventriculitis and
hydrocephalus were overcome with cerebrospinal fluid diversion, all four lesions were excised microsurgically using the
transtemporal approach. One patient demonstrated significant and progressive improvement of her preoperative memory
deficit. The remaining two patients have both returned to their preoperative employment. Homonymous visual defects
in two patients were transient, and seizure activity developing after operation was easily controlled medically. This
experience confirms that intraventricular AVMs can be excised with minimal morbidity and should be treated
aggressively in the symptomatic young patient. (Neurosurgery 16:293-303, 1985)

Key words: Barbiturate coma, Basal ganglia. Intraventricular arteriovenous malformation, Microsurgical excision

Arteriovenous malformations (AVMs) located in function-
ally critical areas of the brain remain one of the most difficult
therapeutic challenges in neurosurgery. Operation for the
excision of lesions located in the motor or speech area carries
the risks of paralysis and/or aphasia (11, 34). Complications
in the excision of extensive paraventricular lesions may
threaten the basal nuclei and thus the very survival of the
patient. These latter AVMs have therefore frequently been
deemed inoperable (12). Yet, when the natural history of
these lesions is considered, the prognosis for a symptomatic
young patient is not favorable (4, 5, 8, 14, 17, 18, 22-25. 31,
32). Up to 50% of the symptomatic patients will die from or
be impaired by the AVM during their lifetime. With this in
mind, we have taken an aggressive approach to the treatment
of basal ganglia AVMs.

The surgical approach to AVMs located in paraventricular
regions poses certain characteristic problems (1-3. 6, 10, 12.
13, 21, 27. 28, 30. 33, 35). Because of their location, hemor-
rhage is often directed into the ventricular system (26). Local
parenchymal compressions may lead to focal neurological
deficits. More frequently. however. intraventricular hemato-
mas obstruct cerebrospinal fluid (CSF) circulation and pro-
duce chemical ventriculitis. CSF drainage is therefore neces-
sary. The periventricular location of these lesions also fre-
quently necessitates a transventricular approach for their sur-
gical excision (4). Cerebral retraction to ensure adequate
exposure may be severe. leading to troublesome postoperative
brain swelling. In addition. intraoperative hemorrhages must

293

be meticulously controlled to prevent any insidious intraven-
tricular bleeding. Last, manipulation of basal periventricular
nuclei can be associated with acute vasodilation (9, 20) and
resultant massive cerebral swelling or hemorrhage. Such oc-
currences carry a significant mortality rate. Immediate reduc-
tion of intracranial blood flow is imperative to ensure survival
and to prevent catastrophic neurological deficits (15, 16).

BASAL GANGLIA AVMs

Between 1979 and 1983. six patients harboring extensive
basal ganglia AVMs were treated by staged surgical excision.
The indications for operation were intracranial hemorrhage,
progressive neurological deficits. and intractable headache.
Each patient was evaluated with three-vessel angiography and
axial. coronal, and sagittal computed tomographic (CT) scan-
ning before each procedure and after the final operation.

Case 1

[This case has been reported previously (3) and is summa-
rized briefly. ]

A 30-year-old woman had a 12-year history of complex
partial seizures accompanied by focal seizures of the left arm.
Angiographic examination disclosed a right basal ganglia
AVM (Fig. 1. 4 and B). An episode of severe headache
suggestive of hemorrhage occurred 6 months before admis-
sion. The onset of progressive left-sided hemiparesis precipi-

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Neurosurgery, Vol. 16, No. 3

Fic. 1, Case |. Right internal carotid angiogram shows the lateral (4) and anteroposterior (AP) (B) projections of the AVM. The large
amount of arteriovenous (AV) shunting probably led to the formation of the large venous aneurysm and the paucity of opacification of the
cerebral vessels. C, postoperative angiogram shows complete AVM excision.

tated her admission in November 1979. Increasing lethargy,
nausea, vomiting, and left hemiplegia soon followed. A radi-
ographic work-up disclosed no interval enlargement of the
AVM or intracranial hemorrhage. Her symptoms were attrib-
uted to progressive vascular shunting.

The patient was immediately alert and oriented after the
first operation through the right sylvian fissure, during which
the lateral aspect of the AVM was isolated from the surround-
ing brain. Her sensorium returned to normal, but hemiplegia
persisted. After the second operation using the same approach
with complete excision (Fig. 1C), she became neurologically
intact with the aid of intense rehabilitation. Her seizures have
been adequately controlled with medication during the last
4', years.

Case 2

A 14-year-old boy presented with a history of 4 years of
severe, intractable pulsatile headache that was frequently as-
sociated with transient left homonymous hemianopia. The
incapacitating nature of the headache had necessitated mul-
tiple hospitalizations that significantly disrupted his daily life.
Increased frequency of these attacks led to angiographic ex-
amination that demonstrated a giant AVM involving most of
the right temporal, occipital, and parietal lobe, as well as the
basal ganglia (Fig. 2), The two distinct components of the
malformation were fed by the anterior and posterior circula-
tions, respectively.

Initial therapy included embolization with cyanoacrylic
glue, which occluded only a small portion of the malforma-
tion. The decision was therefore made to excise the lesion in
multiple stages. During the first procedure, multiple clusters
of abnormal vessels were excised in the anterior temporal
region. During the second stage, feeding arteries entering the
malformation from the incisura were occluded. Part of the
lesion was also isolated from the surrounding brain, Both
procedures were uneventful, During the third operation, how-
ever, progressive occlusion of feeder vessels led to vigorous
pulsation of the brain. This necessitated termination of the
procedure.

During the fourth stage of the excision, most of the malfor-
mation was excised, but a persistent left supraquadranopsia
developed. A final angiographic examination demonstrated
two small nests of AVM—one anteriorly in the midtemporal
region and one at the occipital pole fed by one large artery.
The anterior component was removed without difficulty dur-
ing a fifth procedure. However, approximately 30 minutes
after removal of the occipital lesion, the perioccipital cerebral
substance started to pulsate vigorously. This was soon fol-
lowed by acute swelling and multiple hemorrhages at sites

distant from the AVM bed. The brain herniated through the
craniotomy defect. Mannitol and the intravenous infusion of
thiopental were necessary for brain relaxation and closure of
the wound. An immediate postoperative CT scan demonstra-
ted an intraoccipital hematoma. No attempt was made to
evacuate the hematoma because the intracranial pressure
(ICP) was controlled adequately with medical treatment.

Barbiturate coma was maintained with pentobarbital for 7
days. Full neurological recovery with the exception of a left
homonymous visual field defect was attained after | month
despite an initial transient left hemiparesis. The patient de-
clined postoperative angiography. The AVM was presumed
to be totally removed because surgical inspection at the end
of the last operation did not disclose any abnormal vascula-
ture.

Now, 3 years later, the patient is performing well at school
and is able to drive and water-ski. He has had two seizures,
which were controlled medically.

Case 3

A 60-year-old woman presented with a 5-year history of
episodic left-sided paresthesia diagnosed angiographically as
being due to a right basal ganglia AVM (Fig. 3). Left hemi-
paresis commenced 10 years before this evaluation and be-
came progressive. It was the progressiveness of the weakness
that led to the decision for therapy. At the time, the patient
was leading an independent life requiring minimal assistance
in her daily chores. Two sessions of preoperative embolization
were attempted, and the second was complicated by a mild
ischemic attack leading to worsening of her focal deficit.

Eight weeks later, the AVM was approached directly
through the right sylvian fissure without any initial attempt
at occluding the small lenticulostriate feeders. When the sur-
face of the AVM was reached, its lateral surface was isolated
from the surrounding brain through microsurgical dissection
in the gliotic brain-lesion interface. There was no worsening
of her neurological deficit postoperatively. The second stage
of the excision was carried out 2 weeks later. The same lateral
sylvian approach was followed without initial exposure of the
lateral ventricle. However, as the dissection progressed, the
brain pulsated somewhat more vigorously. Episodes of vas-
cular oozing and bleeding became difficult to control by
bipolar coagulation and were more frequent. One arterial
bleeder was packed at the mesial aspect of the dissection. No
further hemorrhage occurred during the ensuing 20 minutes,
when there was no surgical manipulation of the wound.
Suddenly, acute massive swelling of the entire frontal lobe
occurred, with significant herniation of the brain out of the
craniotomy defect. At some distance anterior to the operative

March 1985 EXCISION OF PARAVENTRICULAR AVMs 295

Fic. 2. Case 2. Right internal carotid angiogram demonstrates the temporal component of the AVM (A and B). Note multiple clusters of
abnormal vessels in the anterior temporal region. The large AV shunt made it difficult to opacify the entire extent of the malformation. C and
D, vertebral angiography shows the occipital component of the AVM, which extended to the midline and the occipital pole.

Fic. 3. Case 3. The basal AVM was fed mainly by the right internal carotid artery. The cloudlike clusters of abnormal vessels at the periphery
of the AVM were fragile and produced intermittent intraoperative hemorrhages.

296 U

site. explosive hemorrhages appeared in the cerebral substance
and some dissected through the cortex. Attempts to control
these hemorrhages led to opening of the ventricular system.
which was already filled with blood. This was due in part to
the previously packed bleeder, which had retracted into the
ventricle and was now actively bleeding. Attempts to control
the hemorrhage with microsurgical coagulation were futile
and direct pressure over the entire exposed brain was neces-
sary to achieve hemostasis. Barbiturate coma using intrave-
nous thiopental and pentobarbital was immediately instituted,
together with mannitol infusion. The arterial pressure was
reduced to approximately 65 mg Hg. The brain thereafter
relaxed sufficiently to permit wound closure. In spite of
postoperative barbiturate therapy, intracranial hypertension
was only marginally controlled and a severe adult respiratory
distress syndrome and coagulopathy soon overwhelmed the
patient, leading to her death 3 weeks postoperatively.

Comment

In view of these occurrences, our approach to these exten-
sive periventricular lesions was modified. First, bleeding ves-
sels are meticulously coagulated (4). Packing of hemorrhages
is reduced to a minimum to avoid retraction of the opened
and bleeding vessel into another region of the CSF space.
Second. all procedures are terminated when excessive pulsa-
tion of the surrounding brain or excessive oozing around the
operative site does not subside after an observation period of
30 to 40 minutes because these latter conditions have been
the prodrome to “autoregulation breakthrough” swelling or
hemorrhages. Third. all lesions are approached transven-
tricularly because this will allow the surgeon to monitor the
intraventricular space. The surgeon can also approach the
AVM through the ependymal surface, thus treating the AVM
as a “superfical” lesion. Last, barbiturate coma and hypother-
mia (30°C) are instituted electively at the start of each opera-
tion to reduce cerebral metabolism and thus cerebral blood
flow (15, 16). Barbiturate coma is induced by the intravenous
infusion of thiopental over | hour with the infusion adjusted
thereafter to maintain an isoelectric electroencephalogram.
Intravascular volume is maintained and cardiovascular func-
tion is monitored with a Swan-Ganz catheter. Hypothermia
is achieved using topical cooling (water blanket). Thiopental
infusion is terminated at the end of any uneventful operation.
Such procedures afford brain relaxation for adequate surgical
exposure. In addition, reduction of brain metabolism and
blood flow may also afford some degree of protection against
acute vascular engorgement as a result of vasomotor paralysis
or “autoregulation breakthrough” (19, 29. 34). At the termi-
nation of each procedure. the ICP is monitored with a sub-
dural monitor until the patient awakens from coma.

Case 4

A 40-year-old, right-handed woman had had severe intract-
able vascular headaches for 5 years when an angiogram dis-
closed a large AVM in the left basal ganglia that extended to
the hypothalamus. Because of its location, the lesion was
deemed inoperable. However. as a result of progressive head-
ache and the commencement of intermittent but progressive
difficulty with vision, speech, and handwriting, the patient
was referred for evaluation.

The admission neurological examination was normal. A
repeat angiogram disclosed a left internal carotid aneurysm
in addition to the deep basal AVM (Fig. 4, 4 to C). The
aneurysm was clipped. Seven months later. the AVM was
approached through the sylvian fissure and insular cortex.

Neurosurgery, Vol. 16, No. 3

The lateral aspect of the lesion was isolated. A transient
receptive aphasia lasted 2 weeks postoperatively.

Stage 2 excision of the AVM was undertaken through the
same approach but under elective deep barbiturate coma.
After the lateral third of the AVM was isolated from the
surrounding brain, acute swelling occurred in the presence of
an initially relaxed brain and a mean arterial blood pressure
of 70 mm Hg. With the administration of a small dose of
mannitol, the brain became much more relaxed within |
minute. The procedure was immediately terminated. No sig-
nificant intracranial hypertension was encountered postoper-
atively. Barbiturate coma was maintained for | week. After
emergence from induced coma, the patient demonstrated a
moderate expressive aphasia and hemiparesis, which im-
proved significantly over the following months. When she
presented for the third stage of the AVM excision 9 months
later, only a very mild anomia and hemiparesis was detectable.

A transventricular approach through the left midfrontal
gyrus was performed with the patient under barbiturate coma
during the third stage operation. Attention was directed to-
ward isolating the mesial half of the AVM located in the
hypothalamus and the anterior perforate substance. At the
end of the procedure, the lateral left hypothalamus was re-
moved and the carotid bifurcation was visualized. There were
transient episodes of diabetes insipidus postoperatively, which
responded to fluid replacement and vasopressin treatment.

The fourth stage and the final excision of the AVM was
undertaken |! months after the third stage. At this time, the
patient was able to carry on a meaningful conversation despite
a mild dysphasia. The right hemiparesis was barely detectable.
Under barbiturate coma, the previous left frontal transventri-
cular exposure was reopened and the remaining AVM in the
lateral basal ganglia and internal capsule was removed. This
was confirmed by a postoperative angiogram (Fig. 4, D and
E). The patient awoke from coma 4 days later and is making
satisfactory progress in recovering from a transient worsening
of her speech impairment and hemiparesis. The patient cur-
rently converses with hesitancy in short sentences. Despite
the hemiparesis, she is able to ambulate without assistance
outside her home.

Case 5

The patient, a 29-year-old man, suffered an intracerebral
hemorrhage in December 1979 as a result of a deep-seated
AYM in the right hemisphere. Operation for evacuation of
the hematoma and ligation of a large feeding artery was
complicated by rebleeding and subsequent wound infection
and cerebritis. He was left with a residual left homonymous
hemianopia and left hemiparesis. Focal seizures were con-
trolled medically. Two years after the initial hemorrhage, the
patient was referred for surgical therapy.

A preoperative angiogram disclosed an AVM involving the
dorsal and posterior right thalamus, mainly supplied by the
thalamoperforators and the choroidal arteries (Fig. 5, A to D).
Under barbiturate coma, a right transfrontal approach to the
ventricular system was made. This allowed adequate access
from the foramen of Monro to the trigone. The lesion was
mainly subependymal with occasional vascular loops protrud-
ing into the floor of the body of the lateral ventricle. The
superior half of the AVM was isolated through dissection in
the perilesion gliotic plane. One bleeding vessel bordering the
internal capsule had to be followed into this structure for
coagulative control. The patient awoke from the operation
with worsening of the left hemiparesis, which did not recover
to his preoperative status despite intense rehabilitation.

March 1985

EXCISION OF PARAVENTRICULAR AVMs 297

Fig. 4. Case 4. The AVM was fed by the left internal carotid artery (lateral (4) and AP (B) views) with the mesial aspect approaching the
midline hypothalamus. The contribution from the posterior circulation (C) was minor, but these tortuous vessels were fragile and produced
some incessant hemorrhage. They were eliminated during the third operative stage (D). The postoperative angiogram (£) confirmed total excision

of the lesion.

Seven months later, the patient returned for the final re-
moval of the AVM (Fig. 5£), This was accomplished with the
same anesthetic and operative approach. The immediate post-
operative course, however, was complicated by transient sys-
temic hypertension as the patient was awakening from the
barbiturate coma. This led to intraventricular hemorrhage.
Despite immediate evacuation of the hematoma, recovery
was markedly delayed. Communicating hydrocephalus had
to be treated with CSF shunting. His mentation returned to
normal after 2 months, but he still had significant difficulty
with ambulation | year postoperatively.

Case 6

A subarachnoid hemorrhage led to the diagnosis of a right
basal ganglia AVM in a 12-year-old girl. The lesion involved
the dorsal and posterior aspect of the thalamus, with a portion
extending around the trigone into the temporal horn (Fig. 6,
A to D). Two subsequent hemorrhages left her with a severe
left hemiparesis. Her mentation was, however, bright and she
performed well at school. Despite her hemiparesis. she was
physically active. Embolization with partial occlusion of the
lesion was performed before referral to our center. When she
presented for operation 4 years after the initial hemorrhage,
her examination disclosed a left homonymous hemianopia
and a severe left hemiparesis.

Under barbiturate coma. a right frontal transventricular
approach was taken for isolation of the anterior portion of

the AVM. The lenticulostriate feeders entering from the in-
ferior aspect of the AVM were easily identified with reflection
of the isolated portion of the AVM. These were coagulated
and divided. Three weeks later, a second stage operation was
undertaken through an inferior temporal transventricular ap-
proach for isolation of the portion of the AVM in the temporal
horn. The AVM was completely excised through the frontal
transventricular approach in two additional stages spaced 2
and 1 month apart, respectively (Fig. 6F).

At discharge, the patient's neurological status was essen-
tially the same as when she first presented for operation.
Currently, she is active and attending school 1' years after
total AVM removal.

INTRAVENTRICULAR AVMs

Between 1979 and 1983, four AVMs located in the trigone
of the dominant hemisphere were excised from three patients.

Case 7

A 23-year-old man had an intraventricular hemorrhage 2
years before operation. A 2.5- x 2.5- x 2.5-em AVM in the
left ventricular trigone was fed by both anterior and posterior
choroidal arteries. as well as the middle cerebral artery (Fig.
7, 4 to C). His neurological function remained normal despite
a second intraventricular hemorrhage.

Surgical excision was undertaken through a middle tem-

Fic. 5, Case 5. The AVM was supplied by both the right internal carotid (lateral (A) and AP (B) views) and the posterior cerebral (lateral (C)
and Towne (D) views) arteries. It occupied the dorsoposterior thalamus, but also presented in the temporal horn. Postoperative angiography (£)
demonstrated total excision.

Fic. 6, Case 6. The AVM was similar to the one in Case 5, being supplied by both the right internal carotid (lateral (4) and AP (B) views)
and the posterior cerebral (lateral (C) and Towne (D) views) arteries. Postoperative angiography (E) demonstrated total excision.

298

March 1985

a

Fic. 7. Case 7. The dominant trigonal AVM was supplied by both the left inte

EXCISION OF PARAVENTRICULAR AVMs 299

al carotid (lateral (4) and AP (B) views) and the posterior

cerebral (lateral view (C)) arteries. The lesion filled the entire atrium. Complete excision was demonstrated by postoperative angiograms (D).

poral gyrus approach to the trigone. The lesion occupied and
distended the entire ventricular atrium. Abnormal vessels
were encountered before any release of CSF to indicate entry
into the ventricular system. Total excision was accomplished
after shrinkage of the lesion through coagulation of surface
vessels (Fig. 7D). Even though the lesion was closely applied
to the choroid plexus, it seemed to have originated from
ependymal vessels.

A small homonymous right temporal visual field defect
resolved after | year. The patient has remained neurologically
intact without any memory deficits over the past 3 years.
These were rare seizures, which have been controlled medi-
cally.

Case 8

Multiple seizures over a 2-year period led to the diagnosis
of a left intraventricular AVM in a 29-year-old woman. A
subsequent intraventricular hemorrhage forced the decision

to attempt definitive surgical treatment. Because of a domi-
nant supply to the malformation from the posterior cerebral
artery. which originated from the internal carotid artery (Fig.
8. 4 and B), an attempt at embolization was unsuccessful.
No neurological deficit was present preoperatively.

The ventricular atrium was approached through the inferior
temporal gyrus. Even though the majority of the lesion resided
in the CSF space. a tongue of it extended through the white
matter to the inferior occipital cortex. A complete removal
was achieved and confirmed angiographically (Fig. 8C).

The patient regained her preoperative status without any
change in her memory function. Her seizure activity has been
controlled medically for the past 2’ years.

Case 9

A 22-year-old woman suffered intraventricular hemor-
rhage. which rendered her stuporous and aphasic. This appar-
ently resulted from a small AVM located in the left ventricular

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Neurosurgery, Vol. 16, No. 3

Fic. 8. Case 8. This AVM was supplied by the posterior cerebral artery, which originated from the left internal carotid artery (lateral (A) and
AP (B) views). A small component of the lesion presented at the inferior occipital cortex. Complete excision was achieved (C).

Fic. 9. Case 9. The small AVM (solid arrowheads) was demonstrated in the left internal carotid (lateral (4) and AP (B) views) and left
posterior cerebral (lateral view (C)) angiograms. A less distinct cluster (open arrowheads) was not evident and had to be excised in a second

operation.

trigone (Fig. 9). The patient’s sensorium rapidly improved
with the placement of a ventriculoperitoneal shunt for ob-
structive hydrocephalus, but her speech and orientation re-
mained impaired. Eighteen days after her initial hemorrhage,
a left temporal craniotomy was performed for excision of the
AVM.

The left trigone was approached through ai incision in the
inferior temporal gyrus. After the removal of a liquified
hematoma, a small cluster of abnormal vessels was removed
from the posterolateral thalamic ependyma. Inspection of the
remaining trigonal ependymal surface disclosed no other ab-
normality. A postoperative angiogram, however, revealed a
residual cluster in the inferior trigone. A repeat craniotomy
through the previous transcortical approach was therefore
undertaken. The AVM was | cm in diameter and was located
subependymally at the junction of the inferior trigone and
temporal horn. A total removal was achieved and verified
angiographically.

The patient demonstrated a transient right visual field
defect postoperatively. Her major disability was short term
memory loss and partial aphasia. Over the past year, these
defects have improved significantly with intense rehabilita-

tion. She has been able to care for herself and conduct a
meaningful conversation. Rare absence spells have been con-
trolled medically. The patient currently is contemplating re-
turning to school.

DISCUSSION

AVMs in the paraventricular region are uncommon (1, 4,
7, 10, 17, 18, 24, 25, 36). Their treatment represents a
formidable therapeutic undertaking. Even though the excision
of small lesions in the basal nuclei or ventricles has been
reported (1, 2, 6, 10, 12, 21, 27, 28, 33, 35), extensive lesions
are generally declared inoperable because of their relative
inaccessibility and involvement with functionally critical
areas. This report details a systemic approach to the micro-
surgical treatment of some extensive central AVMs. Six le-
sions involving the basal nuclei were treated with 19 staged
operations. Three patients are back to their preoperative
occupations. with one of these having fully recovered from a
complete hemiplegia. One woman developed a mild speech
deficit and hemiparesis postoperatively, and the mild hemi-
paresis in the 29-year-old man worsened markedly after the

March 1985

EXCISION OF PARAVENTRICULAR AVMs

301

excision of a thalamic lesion as a result of postoperative
intraventricular hemorrhage. This led to severe disability in
ambulation. The only mortality occurred in the oldest patient
(60 years old), who succumbed to uncontrolled acute intra-
cerebral swelling and hemorrhage. During the same period,
four AVMs were removed from the trigone in the dominant
hemisphere of three patients. Although two patients had
transient homonymous quadrantanopia, only one still has the
preoperative memory deficit, which is clearing with rehabili-
tation. These results suggest that microsurgical excision offers
a valid therapeutic approach to extensive central AVMs.

Central AVMs pose specific therapeutic problems as a result
of their paraventricular location, which predisposes them to
hemorrhage within the ventricular system. Intraventricular
hemorrhage is also a common presentation of intraventricular
AVMs, and recurrent hemorrhage is more frequent in these
lesions (26). The hemorrhagic episode most often leads to
compromise in sensorium. This may be a result of acute
obstructive hydrocephalus or chemical ventriculitis. Because
these symptoms are usually subacute, immediate operative
evacuation of the intraventricular clot is seldom necessary.
Cerebrospinal fluid drainage for the relief of increased ICP
and elimination of the lytic products of the hematoma suffices
in most cases for clinical improvement. This temporizing
measure permits the acute effects on the surrounding brain
to subside. It also allows time for a detailed angiographic
study of the vascular anatomy before surgical excision.

Extensive lesions were excised in multiple stages to allow
graded redistribution of cerebral blood flow. In these in-
stances, a complete angiographic and CT evaluation was
undertaken before each procedure because different surgical
exposures may have to be adapted to approach different
aspects of an extensive lesion. Accurate delineation of the
relationship of the feeding arteries and draining veins to the
ventricular system and basal structures (visualized by CT
scanning) is critical because this permits the surgeon to use
the most direct transventricular or subarachnoid approach to
the feeding vessels while protecting the integrity of the veins.
In addition, large venous channels or aneurysmal dilatations
are frequently reflections of the degree of arteriovenous shunt-
ing. The presence of large channels would thus alert the
surgeon to the possibility of “autoregulation breakthrough”
hemorrhages should an extensive excision be planned. Such
venous channels, however, seldom present significant techni-
cal challenges intraoperatively because they collapse and
thrombose after elimination of the arteriovenous shunts.
The location of AVMs in the basal nuclei usually renders
them relatively inaccessible. Their periventricular presenta-
tion, however, can be turned to the surgeon's advantage if he
adapts the transventricular approach. Once the ventricular
system is entered, many of these AVMs can be seen to present
through the ependyma or to be directly subependymal. In
such situations, they can be handled in like fashion as super-
ficial cortical lesions. Dissection planes can be developed in
the perilesion gliotic plane (4). Coagulation of surface vessels
will shrink the lesion, thus further developing the dissection
plane and reducing the need for extensive brain retraction to
provide exposure. The transventricular approach also affords
the surgeon adequate monitoring of the intraventricular con-
tent so that any packed bleeder would not be overlooked
should it retract and bleed into other portions of the intraven-
tricular system. This may have been the situation in Case 3.
where the sylvian approach was taken. Conceivably. the intra-
ventricular hemorrhage could have been dealt with sooner if
the transventricular approach had been pursued.

Acute vasodilatation has been observed with manipulation
in the basal area (9. 20). This may be responsible for some

instances of acute brain swelling. Acute brain swelling or
hemorrhage is also sometimes encountered during the elimi-
nation of extensive high flow AVMs (19, 29, 34, 36). This is
presumed to result from engorgement of the maximally di-
lated, chronically ischemic perilesion cerebral vessels, which
have lost autoregulation. When the physical integrity of such
vessels is disrupted, uncontrolled catastrophic hemorrhages
may ensue. The outcome of such occurrences has been uni-
formly dismal. One method of treatment is by induced hy-
potension to reduce regional blood flow through the use of
agents such as sodium nitroprusside. Under such treatment
conditions, the cerebral metabolism, however, remains unal-
tered in the face of reduced blood flow. On the other hand,
agents that reduce both blood flow and cerebral metabolism
theoretically would afford additional protection against is-
chemia. Barbiturates possess such properties and have been
used to control intracranial hypertension as a result of head
trauma. These agents have also been used successfully to
control acute brain swelling during the surgical treatment of
extensive AVMs (15, 16). In the latter situation, the patients
commonly suffered devastating neurological deficits, probably
as a result of damage sustained during the period (20 to 30
minutes) required to achieve brain relaxation. We reasoned
that if barbiturate coma were induced before the event, not
only would the brain be sufficiently relaxed to facilitate sur-
gical exposure, cerebral blood flow would also be reduced to
allow ischemic vessels to accomodate any acute blood redis-
tribution. With this in mind, we used induced barbiturate
coma for extensive basal AVMs. This was done with the full
awareness that it would frequently be 4 to 7 days before the
patient would emerge from induced coma. Our experience
with Case 4, where acute swelling was successfully treated
within | to 2 minutes with mild resultant clinical deficit, tends
to support our contention. With continued experience, we are
now able to titrate the barbiturate dose to achieve a much
earlier wake-up time (24 to 36 hours). Staged operations with
resultant limited but progressive redistribution of blood flow
would potentially facilitate the circulation accommodation
process as well (29. 33, 34. 36).

The need for multiple stages is suggested by the significant
degree of arteriovenous shunting on the preoperative angio-
grams. It is difficult to determine the number of stages re-
quired at the beginning because the outcome of each stage
cannot be foreseen. Excessive pulsation of the surrounding
cerebral substance or unexplained oozing at sites distant from
the operative field frequently indicate impending “autoregu-
lation breakthrough” swelling and hemorrhage. Thus, each
stage would proceed until such occurrences and be termi-
nated: otherwise, as extensive a resection as possible will be
carried out. Should the operation be uneventful, we have
seldom encountered significant postoperative problems if the
patient's cardiovascular status is well controlled. The hemor-
rhagic episode in Case 5 was a result of a hypertensive event
due to the lack of patient sedation. This occurred early in our
experience with elective barbiturate anesthesia. No such com-
plication has since occurred.

Operations for the excision of intraventricular AVMs are
similar to those for basal lesions because the transventricular
approach is necessary. The surgical approach to the lateral
and 3rd ventricular system is either transcortical or transcal-
losal (4. 10). The transfrontal approach not only allows access
to the frontal horn and 3rd ventricle. but will also provide
ample exposure to the trigone (4). Trigonal lesions can also
be excised through incisions in the superior parietal or mid-
temporal gyri or the splenium of the corpus callosum. One
possible limitation of the transcallosal approach is in the
lateral exposure of extensive lesions, as in Cases 7 and 8.

302 U

Exposure is nonetheless generally adequate through these
“silent” areas without causing significant neurological defects.
Visual deficits have been transient in our experience with the
temporal approach. Any involvement of structures such as
the limbic or thalamic systems. however, may lead to signifi-
cant impairment of memory and language functions. It is
therefore essential that the approach taken avoid retraction
or dissection within these vital structures.

In conclusion, our experience with this series of extensive
basal AVMs suggests that microsurgical excision coupled with
cerebral protection using elective barbiturate coma offers a
valid therapeutic regimen in the treatment of this devastating
disease. In addition, our experience supports the contention
that intraventricular AVMs can be excised with little morbid-
ity. Their tendency to rebleed is an argument for an aggressive
approach to their treatment.

ACKNOWLEDGMENTS

The author thanks Drs. M. Todd, J. Drummond, L. F.
Marshall, and J. Alksne for continuous support and encour-
agement; the operating room personnel for technical assis-
tance; and the neurosurgical house staff and the nursing staff,
especially in the intensive care unit, for their devoted care of
these critically ill patients. I also thank D. Rosati and B.
Siaumau for excellent secretarial assistance.

Received for publication, March 3, 1984: accepted, October 19,
1984,

Reprint requests: Hoi Sang U, M.D., University of California
Medical Center, 225 Dickinson Street. San Diego, California 92103.

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March 1985

COMMENTS

The author of this article dealing with deep and intraven-
tricular arteriovenous malformations records a number of
instances of technical triumph with lesions that most people
would consider inoperable. One might question the surgical
indications of some of the larger lesions, especially the 60-
year-old patient who had not had previous hemorrhage. This
happened to be the one mortality, and many neurosurgeons
would not have operated on this patient, considering the
clinical history and the complexity of the lesion. With some
of the other large, deep lesions, the surgical results were less
than satisfactory, again raising the question of judgment in
terms of the operability of these lesions. The use of up to four
staged operations to remove some of the more complex lesions
is interesting. In my experience, staging may be of benefit.
On the other hand, it may lead to unpredictable disasters
because portions of the AVM are isolated during the staging
procedures and may explode postoperatively. In the cases
with more complex lesions, a great deal of difficulty was
experienced with brain swelling, venous congestion, and un-
expected hemorrhages during operation and postoperatively.
This probably bears witness to the partial removal during the
initial operative stages and the massiveness of some of these
lesions. Also of interest was that the author found no benefit
from preoperative embolization. On the contrary, we have
found embolization to be quite useful in reducing malfor-
mations, especially the deep ones, making them more acces-
sible to surgical excision, often in a single operative interven-
tion. Also, the use of CT scans in further analyzing the size
and relationship of these deep malformations is not stressed
by Dr. U. We have found that CT scanning is extremely useful
in guiding the operative approach and in anticipating the
relationship of these malformations to the deep structures.

Ventricular malformations represent some of the more
difficult ones to treat and, as noted by the author, are some
of the most dangerous AVMs. The exposed venous coils are
treacherous areas where hemorrhage may occur during oper-
ative intervention.

Often, the arterial supply to these lesions is obscure to the
surgeon working down a deep passageway. The various routes
to the ventricle deserve an elaborate discussion because the
choice of a route may determine whether the operation is
successful or disastrous. Interestingly, some of the patients

EXCISION OF PARAVENTRICULAR AVMs 303
reported here had malformations located in the region of the
left trigone. We have encountered a number of patients similar
to these who presented with hemorrhage, with the resultant
primary neurological deficit of recent memory impairment.
Similar impairment existed postoperatively. In one of the
cases, the author mentioned that recent memory impairment
was a problem, but cleared. The other cases were not detailed
in terms of memory impairment. The presence of this neu-
rological deficit suggested to us that cerebral dominance is
important in terms of the deep paratrigonal structures often
relating to memory such as the fornix, caudate, and corpus
callosum and its connections. The author must be compli-
mented on his tenacity and persistance in removing some of
the more complex and larger lesions.

Bennett M. Stein, M.D.
New York, New York

The author reports nine cases of unusual AVMs. Six were
very extensive paraventricular lesions mainly involving the
basal ganglia region and beyond. Three were intraventricular
lesions. This report is the first, to my knowledge, of surgical
treatment of such extensive lesions in the depth of the brain.
The author is to be congratulated for his excellent work and
for sharing his experiences with the medical community. This
report illustrates that such so-called inoperable lesions can, in
fact, be totally removed with acceptable mortality and mor-
bidity. It is obvious that much preoperative planning is needed
to determine the surgical approach and the use of hypoten-
sion, hypothermia, and barbiturate coma in certain cases.
Likewise, intraoperative judgment is critical in deciding when
to terminate the procedure to allow the brain to accommodate
to a drastically changed cerebral blood flow pattern before
another trial of dissection and excision is attempted. In the
author's first six cases, he performed 19 procedures, an aver-
age of about 3 procedures per case.

The author deserves credit for his courageous and persistent
approach in managing such extensive AVMs in the depth of
the brain.

Shelley N. Chou, M.D.
Minneapolis, Minnesota