IV

Chapter

Arteriovenous
Malformations
of the Brain

226

Arteriovenous Malformations of the Brain

In this chapter, we describe surgical
approaches to arteriovenous malformations
(AVMs) of the brain. The operative princi-
ples listed are applicable to all AVMs, re-
gardless of the AVM's location, size, or
configuration.

Guidelines to Surgery

of Arteriovenous Malformations

1. Classification of Arteriovenous
Malformations of the Brain

AVMs are classified by degree of sur-
gical difficulty and location. The schema of
Spetzler is used to classify lesions accord-
ing to surgical difficulty (grades I to V)
based on size, relation to important brain
structures, depth, location, and number of
venous channels. Classification by location
is based on a modification of Yasargil's rec-
ommendations, namely that AVM lesions
will be considered either convexity or deep;
each designation is arbitrarily subdivided
into supratentorial and infratentorial. Deep
malformations are those located in the
structures of the deep gray matter, white
matter pathways, and choroid plexus of the
ventricles. This classification of malforma-
tions by locale also considers arterial sup-
ply and venous drainage.

2. Understanding the Arteriovenous
Malformation

Angiography remains the standard for
AVM evaluation. A complete angiographic
evaluation includes a four-vessel study and
sequential evaluation of all phases includ-
ing arterial, capillary, and venous. This se-
quence gives a clear understanding of the
vascular dynamics of the malformation
such as rate of blood flow, steal of regional
flow, and patterns of collateral flow. The
angiogram should be analyzed for nidus
size and configuration and its relation to
normal arteries (en passage), as well as the
position, number, and size of feeding arte-
ries (especially deep feeders), and location.
The angiographic search entails exploration
not only for commonly found associated
aneurysms but also for more rarely found
additional AVMs.

Magnetic resonance imaging (MRI)
supplements information regarding the
presence of hemorrhage, relative chronol-
ogy of multiple hemorrhages, and status of
the regional parenchyma in terms of mass
effect, edema, or injury. This technique
also detects cryptic malformations undis-
covered by angiography.

3. Localization of the Arteriovenous
Malformation Within the Brain

MRI is a critical part of the radiologic
evaluation of AVMs. MRI details the mal-
formation's location in three-dimensional
relation to the regional brain and bony anat-
omy, thereby serving as a map to the surgi-
cal approach as well as an indicator for
potential complications. Localization of
speech dominance can be assessed with se-
lective Amytal injection studies.

4. Exploration of Options With a
Multidisciplinary Approach

An AVM can present as an incidental
finding or with symptoms of headache,
hemorrhage, or seizure. Treatment alterna-
tives considered offer a balance between
the natural history of the disease and the
expected outcome of the various treat-
ments specific for each patient, surgeon,
and center. Treatment options should
include observation, endovascular oblit-
erative techniques, and stereotactic radio-
surgery. A team approach to discuss treat-
ments will provide the best option or
combination of options for the patient.

5. Identification of Associated Aneurysms

The incidence of aneurysms associated
with AVMs varies greatly (2 to 50 percent).
These aneurysms occur in three locations:
proximal, on vessels of the circle of Willis;
pedicular, on vessels directly supplying the
malformation; or intranidal, on or in the
nidus of the malformation. Intranidal aneu-
rysms can be excised with the AVM. Un-
ruptured proximal and pedicular aneurysms
can regress after the AVM is eliminated or
persist, requiring delayed treatment. Proxi-
mal and pedicular aneurysms associated
with hemorrhage should be treated pre-
operatively by direct surgery or endovascu-
lar technique.

227

Guidelines to Surgery of Arteriovenous Malformations

6. Formulation of the Operative Plan (Phase I)

The operative plan should be precise
and contain preoperative considerations,
such as the use and timing of embolization
as an adjunct to surgical resection and
treatment with agents that prevent peri-
operative blood pressure fluctuations. The
intraoperative plan addresses surgical
tools, patient position, skin and bone flap
design, surgical corridors to deep malfor-
mations, and sequence of approach to feed-
ing and draining vessels. If epilepsy is a
presenting complaint, cortical mapping and
resection of epileptic foci may be required.
In certain cases, functional preservation
can be enhanced by use of electrophysio-
logic mapping or local anesthesia. Timing
of the surgical treatment is usually elective
except when a life-threatening hematoma is
present.

7. Execution of the Plan (Phase II)

A well-formulated plan must be com-
municated to and understood by the entire
multidisciplinary team, including surgeons,
assistants, nurses, anesthetists, and often
neuroradiologists and electrophysiologists.

In patients with AVMs, the goal of
treatment is total removal of the malforma-
tion and preservation of neurologic func-
tion. High-quality intraoperative angiogra-
phy ensures that the goal of single-stage
AVM extirpation is achieved.

8. Surgical Tools

The primary tools for AVM resection
are nonadhering bipolar forceps and a dis-
secting microscope. Color-absorptive laser
energy is a useful adjunct to obliterate small
perforating vessels and shrink the overall
mass of the malformation. Ablative laser
energy is useful to cut vessels in deep loca-
tions in which scissors are difficult to ma-
nipulate. Temporary and permanent micro-
clips are useful to occlude large feeding
vessels and for test occlusion of vessels of
passage and draining veins.

9. Surgical Technique

Patient Positioning The patient is positioned
to improve venous drainage, enhance the
surgeon's trajectory and access to the le-
sion, facilitate retraction of the malforma-
tion, and provide access to the cranium and
proximal vessels for intraoperative angio-
graphy.

Exposure Brain relaxation is achieved by
the appropriate positioning of the patient's
head, use of osmotic agents, aspiration of
cerebrospinal fluid, and hypotension.

Guidelines regarding craniotomy flaps
are (1) the flap should expose the entire
AVM and normal brain on all sides; (2) the
origin of the venous drainage should be ex-
posed; (3) exposure of sinuses is generally
unnecessary and may be hazardous; and (4)
care must be exercised when elevating the
dura to avoid injuring the bridging arteries,
veins, and venous sinuses.

Dissection The AVM is circumferentially
dissected with the aid of a freely mobile
microscope. The plane between normal
brain and nidus is maintained by multiple
opposing retractors. Vessels, other than
vessels of passage, crossing this plane are
occluded with the aid of bipolar current or
color-absorptive laser energy. Metallic
clips are seldom needed to obliterate the
vessels of the AVM. The AVM vessels are
sectioned with scissors or focused laser
energy.

10. Assessment of Complete Removal

Inspection The entire bed of the malforma-
tion should be inspected for any evidence
of persistent red veins, which suggest the
presence of shunting due to residual malfor-
mation. There is no acceptable strategy for
partial resection of the AVM because of the
high incidence of postoperative hemor-
rhage in this circumstance.

Hypotension is continued throughout
the dissection phase, at least until intra-
operative angiography has proved that the
AVM is completely excised. Precise in-
spection of all bleeding points is mandatory
because these vessels may have lost vascu-
lar autoregulation (i.e., ability to contract)
and must be thoroughly obliterated by seal-
ing their collagen walls. Application of a
small pledget of Gelfoam soaked with
thrombin under a gently applied retractor
can eliminate troublesome bleeding from
capillaries and arterioles. It is important to
control all bleeding sites in the ventricular
cavities and to evacuate all of the hema-
toma.

228

Arteriovenous Malformations of the Brain

Intraoperative angiography Angiography with
digital subtraction in two planes is essential
to document complete removal of all mal-
formations prior to closure of the skull.
Placement of metallic markers near sus-
picious vessels facilitates the discovery of
hidden malformations when performing
angiography.

11. Postoperative Care (Phase III)

All patients are managed in the neuro-
science intensive care unit. Complications
in the postoperative period can often be
anticipated and are therefore preventable.
The primary cause of postoperative hemor-
rhage (i.e., residual malformation) has been
essentially eliminated by use of intraopera-
tive angiography and single-stage AVM
removal. In the immediate postoperative
period, regional cerebrovascular autoreg-
ulation may not protect parenchyma sur-
rounding large AVMs from reperfusion
injury. We therefore maintain systemic
hypotension for at least 72 hours post-
operatively (mean arterial pressure 60 to
70 mmHg). If indicated, intracranial pres-
sure is monitored and controlled with os-
motic agents, steroids, and diversion of
cerebrospinal fluid.

Supratentorial Convexity
Arteriovenous Malformations

General The arterial blood supply or venous drain-
Considerations age of convexity arteriovenous malforma-
tions (AVMs) presents on the brain's
surface. These lesions may be discovered
as incidental findings or present with head-
ache, seizure, or intracerebral hemorrhage.

Excision of convexity malformations is as-
sociated with a relatively low morbidity de-
spite variable size, multiple arterial supply,
and occasional deep venous drainage. The
depth of these malformations frequently ex-
tends to the ventricular surface. The major
blood supply arises from the convexity, and
perforating arteries are a minor source of
vascular contribution. Preoperative emboli-
zation can eliminate most of the convexity
blood supply and reduce flow through the
malformation. Postoperative hemorrhage
and cerebral edema are rare complications
except in grade V lesions.

229

Supratentorial Convexity Arteriovenous Malformations: Frontal

Frontal Arteriovenous Malformations

I
I

Special Frontal arteriovenous malformations
Considerations (AVMs) derive blood supply from branches
of the anterior and middle cerebral arteries.
Venous drainage terminates in the sagittal
sinus and basal veins of the sphenoparietal
sinuses. The malformation depicted in this
procedure is located anterior to the central
sulcus and is supplied by anterior and mid-
dle cerebral artery branches. The malfor-
mation terminates at the ependyma of the
lateral ventricle. Preoperative embolization
has been rejected because several branches
of the M₂-M₃ middle cerebral artery (MCA)
pass near the malformation and proceed to
supply normal brain (vessels of passage).

Wide exposure of this convexity malforma-
tion provides visualization of the lesion,
vascular supply, and venous drainage. The
location of this frontodorsal lesion above
the sylvian fissure does not require dissec-
tion of arteries within the sylvian fissure.

Arteriovenous Malformations of the Brain

Approach A frontoparietal craniotomy is performed
with the patient in the supine position. The
thorax is elevated 15 degrees to improve
venous drainage. The ipsilateral shoulder is
elevated on a gelatin pad. The head is ro-

tated until the sagittal suture is parallel with
the floor and is maintained in a radiolucent
head-fixation device for intraoperative an-
giography.

Feeding vessel from
callosal marginal artery

Major

draining

vein

4.2

4.2 Coronal view of the mal-
formation shown in this procedure depicts
the arterial supply by a callosal marginal
arterial branch and deep feeders originating
from M₂ branches of the MCA. Venous
drainage terminates in the vein of Labbe.

Supratentorial Convexity Arteriovenous Malformations: Frontal 231

Draining
vein

I
I

1

4.4

4.3 The dural flap is re-
flected superiorly. Care is taken to avoid
injuring surface and bridging veins. Mean
arterial pressure is maintained at 70 mmHg
and osmotic diuretics are administered to
reduce intracranial pressure. Dissection of
the pia-arachnoid membrane adjacent to
the malformation establishes the appropri-
ate plane of dissection.

4.4 Self-retaining retractors
develop and maintain the plane of dissec-
tion between the surface of the malforma-
tion and the normal brain. Vessels
stretched between the malformation and
the brain are coagulated and sectioned. The
plane is evenly developed around the AVM
circumference, progressively dissecting but
avoiding penetrating too deeply in any one
location.

232

Arteriovenous Malformations of the Brain

4.5 Additional retractors main-
tain adequate visualization of the plane
of dissection. Feeding arteries are sac-
rificed while adequate venous drainage is
preserved. Deep arteries penetrating the
bed of resection are coagulated and incised.

4.6 As feeding vessels are
sacrificed, the mass of the malformation
and pulsations diminish. It is then appropri-
ate to begin sacrificing secondary draining
veins while preserving the primary venous
drainage.

4.7 An artery of passage is
identified and preserved. After sacrificing
remaining feeding arteries and draining
veins, the surgeon elevates the malforma-
tion from its bed and coagulates and sec-
tions its primary draining vein. The mal-
formation bed is inspected for residual
malformation and sites of potential hemor-
rhage. Intraoperative angiography docu-
ments complete excision of the AVM prior
to dural closure.

r

Supratentorial Convexity Arteriovenous Malformations: Frontal 233

4.6

Draining
vein

Artery of
passage

Ependyma

Perforating
arteries

4.7

Closure Closure is performed using standard pterio-
nal eraniotomy techniques (see Chapter I).

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