OPERATIVE NUANCES

SUPRATENTORIAL ARTERIOVENOUS MALFORMATIONS

Richard E. Clatterbuck, ARTERIOVENOUS MALFORMATIONS ARE a heterogeneous group of intra-axial central
M.D., Ph.D. nervous system vascular lesions consisting of tangles of abnormal arteriovenous connec-

Downloaded from https://academic.oup.com/ons/article/57/suppl_1/164/2562669 by Universität Heidelberg user on 18 November 2020

Division of Neurological Surgery, tions without intervening capillary beds. The heterogeneity of arteriovenous malformations
Barrow Neurological Institute,
St. Joseph’s Hospital and
is described by the Spetzler-Martin grading scale, a scale that also forms the basis for
Medical Center, Phoenix, Arizona, clinical decision making. The microsurgical treatment of appropriately selected supraten-
and Johns Hopkins University, torial arteriovenous malformations is based on the tenets of circumferential isolation and
Baltimore, Maryland
transection of arterial feeders, preservation of vessels en passant and surrounding func-
tional neural tissue, and skeletonization and transection of venous drainage.
Frank P.K. Hsu, M.D.,
Ph.D. KEY WORDS: Arteriovenous malformation, Microsurgery, Supratentorial
Division of Neurological Surgery,
Barrow Neurological Institute, Neurosurgery 57[ONS Suppl 1]:ONS-164–ONS-167, 2005 DOI: 10.1227/01.NEU.0000164454.70131.3A
St. Joseph’s Hospital and
Medical Center, Phoenix, Arizona,
and Loma Linda University

Medical Center,
Loma Linda, California
Robert F. Spetzler, M.D.
Division of Neurological Surgery,
Barrow Neurological Institute,
St. Joseph’s Hospital and
Medical Center, Phoenix, Arizona
Reprint requests:
Robert F. Spetzler, M.D.,
c/o Neuroscience Publications,
Barrow Neurological Institute,
350 West Thomas Road,
Phoenix, AZ 85013-4496.
Email: neuropub@chw.edu
Received, December 15, 2003.
Accepted, January 21, 2005.
A
rteriovenous malformations (AVMs) are
complex intra-axial central nervous system
vascular lesions consisting of tangles of ab-
normal arteriovenous connections without inter-
vening capillary beds. Multiple methods are at the
disposal of neurosurgeons for the treatment of
these lesions and usually include one palliative
method (i.e., endovascular embolization) and two
curative methods (i.e., stereotactic radiosurgery
and microsurgical resection). Optimizing patient
outcome requires careful patient selection and in-
dividualized treatment. Patient selection is based
on multiple variables, including age, medical sta-
tus, and a grading scale that predicts the outcome
of surgical intervention (1, 3). After appropriate
patients have been selected for surgical interven-
tion, preoperative preparation (including adjunc-
tive embolization when needed), neuroanesthesia
with adequate cerebral protection, and careful mi-
crosurgical resection form the cornerstones of care.
Essential surgical principles include circumferen-
tial isolation and transection of arterial feeders,
preservation of vessels en passant and surrounding
neural tissue, skeletonization of venous drainage,
and finally, transection of venous drainage. This
discussion is based on the surgical decision mak-
ing and technique of the senior author (RFS).
surgical practice for the treatment of AVMs is
predicated on the Spetzler-Martin grading
scale and our evolving understanding of its
treatment implications (1–3). AVMs are
graded I through V based on their size, loca-
tion, and pattern of venous drainage (3), with
Grade I lesions being small with superficial
drainage and in noneloquent brain locations
and Grade V lesions being large with deep
drainage and in an eloquent location. Al-
though treatment needs to be individualized
for each patient, Grade I and II lesions typi-
cally are best treated with microsurgical resec-
tion, whereas Grade IV and V lesions should
be followed up conservatively unless the pa-
tient experiences repeated hemorrhages lead-
ing to progressive and devastating neurolog-
ical consequences (1). Grade III lesions are a
more heterogeneous group and require the
most care in selecting microsurgery or radio-
surgery as the treatment option. In general,
endovascular treatment (embolization) is used
as an adjunct to definitive treatment or for
palliation of large lesions symptomatic of vas-
cular steal syndrome. Occasionally, endovas-
cular treatment can be curative.

PATIENT SELECTION AND THE
SPETZLER-MARTIN
GRADING SCALE
As with any surgical procedure, careful pa-
tient selection is crucial to ensuring optimal
treatment outcomes. Evidence-based neuro-
PREOPERATIVE
CONSIDERATIONS
The preoperative evaluation of the patient
with an AVM includes four-vessel cerebral
angiography and magnetic resonance imaging
(MRI). The angiography is necessary to under-
stand the angioarchitecture of the lesion, in-

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cluding the feeding arteries, draining veins, and their juxta-
position. MRI further clarifies the anatomic location of the
AVM, including the anatomy and location of surrounding gyri
and sulci, or subcortical structures in the case of deep-seated
lesions. Computed tomography and MRI angiography have
not proven as useful in the operative planning for the resec-
tion of AVMs as they have for the treatment of cerebral
aneurysms. Similarly, functional MRI, although potentially
useful for the resection of some eloquent AVMs, has not found
widespread usefulness in preoperative planning.
Preoperative embolization of AVMs is a valuable adjunct in
the surgical treatment of selected lesions. Preoperative embo-
lization of deep or dominant feeding arteries often signifi-
cantly alters blood flow in an AVM, simplifying its resection
and improving the safety of surgery. When used in this fash-
ion, however, the embolization should be performed within a
few days of the planned surgical procedure because emboli-
zation does not always alter the hemodynamics of AVMs in a
predictable fashion and may increase the risk of hemorrhage.
It is vital for the interventional surgeon and microsurgeon to
recognize the goal of embolization, which is to embolize the
vessels most distal from the surgical exposure. Good emboli-
zation of these feeding vessels and good glue penetration of
the nidus greatly facilitate resection.
NEUROANESTHESIA AND
CEREBRAL PROTECTION
Mild hypothermia and barbiturate-induced electroencepha-
lographic burst suppression are important elements in the
neuroanesthetic plan for patients undergoing microsurgical
resection of an AVM. Mild hypothermia (33–35°C) provides
modest cerebral protection and is commonly used for many
intracranial procedures. Thiopental is the barbiturate we use
for titration of burst suppression. This agent not only de-
creases the cerebral metabolic rate, providing cerebral protec-
tion during surgery, but it also decreases cerebral blood vol-
ume, thereby decreasing intracranial volume and decreasing
the need for brain retraction. Consequently, collateral injury to
the surrounding brain can be minimized. The additional brain
protection provided by mild hypothermia is very useful when
temporary clipping of feeding vessels is required.
Mild hypotension also can be used during surgery. Modest
lowering of systolic blood pressure can increase the compli-
ance of the AVM nidus and can be of obvious benefit in
minimizing procedure-related blood loss. Careful control of
blood pressure after surgery also helps prevent hemorrhagic
complications caused by normal perfusion pressure break-
through (4).
MICROSURGICAL RESECTION
(see video at web site)
The skin incision and craniotomy used to approach any
AVM needs to be tailored for each patient. However, several
important themes are common to the approach of any AVM.
NEUROSURGERY
SUPRATENTORIAL ARTERIOVENOUS MALFORMATIONS
Neuronavigation based on an MRI dataset can be very
helpful in planning the approach. The ability to project the
boundaries of the AVM onto the surface of the head allows the
surgeon to plan the incision and craniotomy with considerable
precision. As a result, smaller, less invasive incisions can be
used. In the case of AVMs, the desire to minimize incisions
and craniotomies must be tempered by the need for adequate
exposure. This balance includes adequate exposure of the
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feeding pedicles, associated draining veins, and surrounding
sulci and gyri to allow maximum visualization and control of
the nidus.
We favor the use of fishhook retraction systems (Fig. 1).
When applied properly, they supply superior exposure with a
much lower profile than self-retaining retractors. This advan-
tage can decrease the working depth significantly, thereby
improving the maximum angle of exposure and allowing
easier resection of the AVM.
Isolation and Transection of Arterial Feeders
After the brain is exposed, the arachnoid overlying the
AVM (or the sulcus to be used in approaching a deep lesion)
is opened using meticulous microsurgical technique. The anat-
omy of the feeding arteries should be well understood based
on careful preoperative evaluation of the patient’s angiogram.
Vessels identified as arterial feeders from initial observation
and traced definitively to the nidus of the AVM can be clipped
temporarily (Fig. 2). If it is clear that the artery enters the AVM
and is not a vessel en passant, it can be coagulated and cut.
Small clips ranging from 0.5 to 4 mm can be used if coagulat-
ing the vessel is inadequate. If a vessel is suspected of being en
passant, it can be followed, and all branches going to the AVM
are coagulated and cut. Such vessels may pass deep into a
sulcus only to bypass the nidus (Fig. 3). All suspected arterial
feeders must be followed until they are clearly seen entering
the AVM. Feeding arteries should be transected as near to the
nidus as possible to allow any surrounding parenchyma sup-
plied by the vessel en route to the nidus to continue receiving
blood.
FIGURE 1. Intraoperative photographs showing the fishhook retraction
system. Using fishhooks to retract the edges of the wound provides several
advantages. The extremely low profile of the retraction system allows
unparalleled access to the surgical field and dramatically increases the
angle over which the field can be approached. As shown, the surgeon’s
hands (A) and instruments (B) can use space that otherwise would be
occupied by a self-retaining retractor. The circumferential retraction possi-
ble with such a system maximizes exposure.
VOLUME 57 | OPERATIVE NEUROSURGERY 1 | JULY 2005 | ONS-165
CLATTERBUCK ET AL.
FIGURE 2. Intraoperative photographs demonstrating transection of arte-
rial feeders. A, the arterial loop (arrows) appears to enter the AVM. B,
however, further dissection reveals another loop of this vessel traveling
deep into the sulcus before looping back up to enter the nidus. The vessel
must be followed until it enters the AVM. Bipolar coagulation is then
applied (C), and the vessel is transected (D).-
FIGURE 3. Intraoperative photographs demonstrating preservation of ves-
sels en passant. A, a small vessel (arrow) covered by arachnoid appears
to enter the superficial aspect of the AVM. B, the same surgical field after
arachnoid and sulcal dissection. The vessel that appeared to enter the
AVM on initial inspection can now be seen to pass into the depth of the
sulcus (arrows) and to bypass the AVM without supplying blood to the
lesion.-
When the AVM is located in a relatively noneloquent re-
gion, the individual loops of the AVM at the edge can be
followed and dissected free. This maneuver keeps the AVM
soft and pliable because it does not interrupt venous outflow.
In eloquent regions, however, these loops may need to be
interrupted to avoid additional brain injury. As a result, cer-
tain compartments of the AVM may be isolated, compromis-
ing their venous outflow and leading to engorgement and
possible rupture. It is incumbent on the surgeon to continue
the dissection until control of the feeding pedicle is regained,
a strategy that again will soften the AVM. A salient point in
AVM resection is to avoid tamponading bleeding points. The
inability to control bleeding during AVM resection is likely
because the nidus has been entered. Controlled arterial dis-
section at the bleeding site again will allow control of the
ONS-166 | VOLUME 57 | OPERATIVE NEUROSURGERY 1 | JULY 2005
AVM as the edge of the nidus is identified. Tamponading a
portion of residual AVM leads to herniation below the paddy
or to the most feared complication, postoperative hemorrhage.
Skeletonization and Transection of Draining Veins
The anatomy of the venous drainage of supratentorial
AVMs figures prominently in the surgical planning for their
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resection. The care with which draining veins need to be
approached is obvious. Early sacrifice of the venous drainage
of an AVM may have disastrous consequences. In lesions with
deep venous drainage, the draining vein often is exposed only
during the final stages of resection. However, in lesions with
superficial drainage, early attention to the major draining
veins can be advantageous. Early sharp dissection of the
arachnoid surrounding a large draining vein allows its mobi-
lization (Fig. 4). Mobilizing such veins decreases the mechan-
ical stresses applied to their walls during manipulation of the
AVM, thereby decreasing the risk of inadvertent disruption. In
AVMs with complex architecture, dissecting a large draining
vein back to its point of exit from the AVM nidus can help to
clarify the anatomic relationship of the AVM to the surround-
ing brain tissue. Finally, arterial feeders often course incon-
spicuously with the venous pedicle and are not otherwise
easily identified. With circumferential dissection of the drain-
ing vein, these arterial feeders can be interrupted early during
the surgery (Fig. 4).
Intraoperative Angiography
At the conclusion of microsurgical resection of an AVM,
intraoperative angiography serves as the best means to verify
complete resection before closing. Although dysplastic or di-
lated vessels may be seen in the resection bed, the presence of
an early draining vein is an indication of residual nidus.
CONCLUSION
Effective treatment of patients with AVMs begins with se-
lection of appropriate surgical candidates. MRI and four-
FIGURE 4. Intraoperative photographs demonstrating early skeletoniza-
tion of major draining veins. A, the large draining vein under the suction
is invested with arachnoid that tethers (asterisk) it to the surface of the
brain, decreasing the surgeon’s ability to retract the AVM. B, after a sim-
ple arachnoid dissection (double-headed arrow), the vein is easily mobi-
lized, revealing an arterial vessel (arrow) traveling in the direction of the
AVM.
www.neurosurgery-online.com

vessel cerebral angiography are important for preoperative
evaluation. After appropriate patients have been selected for
surgical intervention, preoperative preparation (including ad-
junctive embolization when necessary), neuroanesthesia with
adequate cerebral protection, and careful microsurgical resec-
tion form the cornerstones of care. Essential surgical principles
include circumferential isolation and transection of arterial
feeders, preservation of vessels en passant and surrounding
neural tissue, skeletonization of venous drainage, and transec-
tion of venous drainage.
REFERENCES
1. Han PP, Ponce FA, Spetzler RF: Intention-to-treat analysis of Spetzler-Martin
grades IV and V arteriovenous malformations: Natural history and treatment
paradigm. J Neurosurg 98:3–7, 2003.
2. Lawton MT: Spetzler-Martin Grade III arteriovenous malformations: Surgical results
and a modification of the grading scale. Neurosurgery 52:740–749, 2003.
3. Spetzler RF, Martin NA: A proposed grading system for arteriovenous mal-
formations. J Neurosurg 65:476–483, 1986.
4. Spetzler RF, Wilson CB, Weinstein P, Mehdorn M, Townsend J, Telles D:
Normal perfusion pressure breakthrough theory. Clin Neurosurg 25:651–
672, 1978.
COMMENTS
A rteriovenous malformation (AVM) surgery runs the gamut from
the fairly simple surgical excision of a small superficial cortical
lesion to an extremely complex, demanding, and dangerous operation
to remove deep-seated large lesions. Size, location, and vascular anat-
omy are the critical factors in predicting good outcomes in AVM
SUPRATENTORIAL ARTERIOVENOUS MALFORMATIONS
resection. Clatterbuck et al. have provided a sound discussion of the
basic principles of AVM resection and some insight into the complex-
ity underlying this aspect of neurosurgery.
Robert A. Solomon
New York, New York
T he authors described their techniques and strategies for the micro-
surgical resection of supratentorial AVMs very well. Stable micro-
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surgical hands and minds are the prerequisites for AVM surgery to
dissect complex vascular tangles, and there is no other way than the
adequate control of feeding arteries followed by the dissection of the
nidus, while preserving passing arteries and draining veins. Particu-
larly, the surface of the nidus should not be coagulated during the
dissection to preserve intranidal venous flow (1). Presurgical plans
may include cortical functional mapping, such as functional magnetic
resonance imaging, and subcortical mapping, such as tractography, to
predict and inform the patients of the risk of neurological deficits.
Intraoperative monitoring, such as motor evoked potentials and cor-
tical electroencephalography, may also be useful to achieve good
operative outcomes. Although observation is an acceptable option,
especially in nonhemorrhagic cases and/or high-grade cases, we must
provide enough and precise information regarding surgical risks and
natural history to these patients.
Kazuhiko Nozaki
Nobuo Hashimoto
Kyoto, Japan
1. Hashimoto N. Microsurgery for cerebral arteriovenous malformations: a
dissection technique and its theoretical implications. Neurosurgery 48:1278-
81, 2001.