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rteriovenous malformations (AVMs) these patients are typically managed conserva-
located in the motor and language cortex tively or treated radiosurgically.3,4 Motor or
are associated with significant risk of language function may shift in the presence of an
neurological deterioration, especially in patients AVM from its anatomic location to an adjacent
presenting with unruptured AVMs and minimal gyrus or even to the contralateral hemisphere.1,5-11
or no neurological deficits.1,2 Consequently, Increasingly, sophisticated neuroradiological
imaging can detect these shifts in functional
localization with functional magnetic resonance
ABBREVIATIONS: AVM, arteriovenous malforma- imaging (fMRI), magnetoencephalography, mag-
tion; fMRI, functional magnetic resonance imaging; netic source imaging (MSI), positron emission
mRS, modified Rankin Scale; MSI, magnetic source
imaging
tomography (PET), and Wada testing. Finding an
unexpected separation between eloquent cortex
and AVM nidus on one of these imaging modalities may encourage patients underwent CT scanning, MR imaging, catheter angiography,
more aggressive intervention with surgical resection, but the reso- and fMRI and/or MSI. Patients with AVMs in the language cortex
lution of these studies is often low and significant shifts in func- underwent language testing (naming, counting, reading, and verbal
tional localization occur infrequently. Therefore, preoperative fluency tests) by a neuropsychologist. Patients with AVMs less than
10 mm from the motor or language cortex, as determined by fMRI and/
functional imaging serves only as a screening test for major re-
or MSI, and with normal neuropsychologic language testing (.90%
organization of the eloquent cortex. proficiency), were selected for intraoperative brain mapping. Of the
Electrocortical stimulation mapping is widely used with intrinsic 12 patients in this study, 7 had motor and 5 had language area AVMs.
brain tumors, facilitating more extensive resections than otherwise
possible and increasing patient survival. However, electrocortical Anesthetic Considerations
stimulation mapping has not been widely used with AVMs, Patients with motor cortex AVMs were operated on with general
probably because compact AVMs do not contain brain tissue anesthesia; and patients with language cortex AVMs were operated on
within the nidus, and they typically have a distinct plane between ‘‘awake.’’ During craniotomy and surgical exposure for awake cases,
their borders and adjacent brain. In addition, AVM resections can patients were sedated with intravenous agents that included propofol
be more technical, tedious, and prone to bleeding than glioma (50-100 mgkg21min21) and remifentanil (0.05-0.2 mgkg21min21).
resections, which makes them more daunting in awake AVM Local anesthesia with lidocaine was used for scalp and temporal muscle.
patients than in awake glioma patients. In reality, a significant After the bone flap was removed, dura was locally infiltrated with li-
portion of the dissection around an AVM is not in a subarachnoid docaine. Before mapping, sedatives were discontinued and patients were
plane and instead is in a parenchymal plane beyond pia mater. awakened under the care of the anesthesiologist. In patients operated on
with general anesthesia, muscle relaxants were not used other than during
Furthermore, a significant number of AVMs have a border or
endotracheal intubation, and a low dose of potent agent, eg, desflurane
borders that are diffuse rather than compact, forcing the dissection (2-3%) and intravenous propofol infusion (50-125 mgkg21min21) was
into brain parenchyma to completely encircle the nidus. Even maintained until the end of the surgery.
minor pial violations and parenchymal invasions can be costly
in the motor and language cortex. Stimulation mapping provides Cortical Stimulation Mapping
an intraoperative technique for identifying and preserving func- The cortical surface was widely exposed and stimulation was per-
tional cortex around motor and language area AVMs. Nonetheless, formed using standard, bipolar electrodes (5 mm). Constant current
published experiences are few and small in size. generator was set to deliver biphasic square wave pulses of 4-ms duration
Intraoperative brain mapping requires a coordinated team of at 60 Hz. Stimuli were initiated at 1.5 mA and increased to a maximum
neurosurgeons, neuroanesthesiologists, and neurophysiologists of 8 mA. Intraoperative monitoring using somatosensory evoked po-
that does not exist at many centers. The high volume of intrinsic tentials was also used in all cases. Sterile numbered labels were used to
brain tumors treated with intraoperative mapping at the identify the stimulation sites.
University of California, San Francisco makes this team readily During awake surgery, patients were asked to repeat 3 language tasks
available for AVM patients. We applied these mapping techni- tested preoperatively: counting numbers from 1 to 50, naming objects on
a computer screen, and reading single words projected sequentially on
ques to selected motor and language area AVMs to evaluate their
a computer screen. Cortical sites were stimulated 3 times for 3-second
indications, feasibility, and utility. We are confident operating durations, and language deficits (eg, counting errors, speech arrest, or
on small AVMs in these areas, but have advocated caution with alexia) during at least 2 of the 3 stimulations in the same site identified
medium-sized AVMs, the so-called grade III+ AVMs.12 We a functional speech area. A neuropsychologist conducted all preoperative
hypothesized that intraoperative stimulation mapping may be one and intraoperative language testing. Corticography was routinely used
method to improve outcomes in these and higher Spetzler-Martin during awake surgery to avoid language errors owing to subclinical
grade AVMs in these eloquent territories. seizure activity. Once the sites were identified, sedative drugs were
restarted for patient comfort. In the general anesthesia group (asleep),
PATIENTS AND METHODS stimulated sites on the motor strip showed positive motor responses
in muscles of the contralateral side of the body (eg, foot, leg, arm,
The study was approved by the University of California, San Francisco hand, or face). Intraoperative seizures induced by stimulation were
Committee on Human Research and conducted in compliance with treated with topical ice-cold Ringer’s solution and intravenous propofol
Health Insurance Portability and Accountability Act regulations. During (1 mg/kg bolus).
an 11-year period, 431 patients underwent microsurgical resection of
their AVMs by a single neurosurgeon (M.T.L.), and intraoperative brain Patient Outcomes
mapping was used in 12 of these patients (2.8%). Data were obtained Neurological outcome was assessed using the modified Rankin Scale
from an ongoing registry of AVM patients treated at our institution, (mRS). A single clinical nurse, under the supervision of a neurologist,
maintained prospectively as part of the University of California, San performed all clinical assessments before any treatment, preoperatively,
Francisco, Brain Arteriovenous Malformation Study Project. at 6 months postoperatively, and during the follow-up period. All
patients had follow-up data within 6 months of analysis. Patients with
Preoperative Evaluation AVM-related seizures that were controlled with medications, and
Preoperatively, all patients underwent complete neurological exami- without any other neurological symptoms, were assigned a mRS score
nation and a baseline modified Rankin Scale score was assigned. All of 0. Alternatively, neurologically intact patients with refractory
AVM-related seizures that interfered with daily activities (working, In 3 patients (25%), the AVM was deep to the cortical surface
school, driving, etc) were assigned a score of 2. Surgical morbidity was and mapping guided the dissection through overlying sulci down
assessed by comparing mRS 6 months postoperatively with the mRS to the nidus. In addition, a small lobule of cortex was resected in
immediately before surgery. each of these cases and mapping helped avoid the language cortex
in 2 cases and the motor cortex in 1 case (Table 2).
RESULTS In 4 patients (33%), brain mapping influenced the attitude
toward the extent of resection. Two patients had AVM borders
Patients and AVM Characteristics that were too intimately associated with the functional cortex to
Twelve patients with AVMs located in the motor or language complete the resection safely. Two patients had deep, conical
cortex had a mean age of 31 years (Table 1). There were 5 men extensions of nidus into white matter near the internal capsule
and 7 women. Only 3 patients (25%) presented with hemor- and deep perforating artery supply from lenticulostriate arteries
rhage. AVM sizes ranged from 1.5 cm to 6.0 cm (mean size, and branches of the posterior cerebral artery. Further dissection
3.7 cm). Patients with Spetzler-Martin grade III+ AVMs were the across these areas was aborted. In these cases of incomplete re-
largest subgroup (5 patients), and 3 patients had high-grade AVMs. section, the nidus was circumferentially dissected in all planes
Ten patients underwent preoperative AVM embolization, except those associated with functional sites, disconnecting
and 3 of these patients were embolized twice. Four patients most arterial feeders while preserving the major draining vein.
had undergone radiosurgery previously, with incompletely Dearterialized AVMs were left in situ with the intent to treat
obliterated AVMs. with radiosurgery.
FIGURE 1. Patient 4. Axial T2-weighted magnetic resonance image (A) and sagittal T1-weighted MR image (B) demonstrated
this left temporal AVM adjacent to Wernicke’s and Broca’s areas. Digital subtraction angiography [left internal carotid artery
injection, anteroposterior (C) and lateral (D) views] demonstrated a Spetzler-Martin grade III+ AVM. AVM, arteriovenous
malformation.
(33%) had incomplete resections, with circumferentially dis- deterioration consisting of hemiparesis and expressive aphasia.
sected and subtotally disconnected AVMs left in situ, attached to She underwent embolization and complete resection.
areas of functional eloquence and with preserved venous drainage. Nine patients deteriorated postoperatively, reflecting the high
Incompletely resected AVMs included 2 Spetzler-Martin grade Spetzler-Martin grades of these AVMs and their proximity to
IV lesions and one grade V lesion, as well as a modified grade III- eloquent cortex (Table 3). Two patients were unchanged and
lesion. Residual AVM was confirmed on postoperative angiog- 1 patient with a ruptured AVM improved. The mean post-
raphy in these patients, and all were treated subsequently with operative mRS was 2.9, compared with a mean preoperative mRS
Gamma knife radiosurgery. Two of these patients are within the score of 1.3. However, much of this deterioration was transient,
3-year latency period after radiosurgery. One patient’s AVM was with a mean mRS score of 1.3 three months after surgery. At late
successfully obliterated with radiosurgery. One patient (patient 1) follow-up (mean follow-up duration, 3.3 y), 6 patients (50%)
had a new hemorrhage 1 year after radiosurgery, with associated recovered completely and 3 patients (25%) were neurologically
FIGURE 2. Patient 4. A, intraoperative mapping identified Wernicke’s area (48) and Broca’s area (40), both adjacent to the AVM. B, a distinct subarachnoid dissection
plane enabled the nidus to separate from Broca’s area. C, the dissection plane was less distinct with Wernicke’s area (behind the retractor blade). D, the nidus was
circumferentially dissected and the draining vein darkened. E, angular artery was skeletonized to preserve normal en passage arteries to distal territories. AVM, arteriovenous
malformation.
improved relative to their preoperative mRS score. Three patients none of the patients experienced any significant discomfort
(25%) remained with new neurological deficits. Nine patients or complained about awake anesthesia. We did not develop
(75%) had good outcomes (living independently with mRS # 2). novel mapping techniques, but our experience with established
There was no mortality in this series. techniques has encouraged us to be more surgically minded in
Of the 5 patients presenting with seizures, only 1 patient had our management of carefully selected language and motor
seizures at late follow-up evaluation. Three patients had seizures area AVMs.
during the perioperative period and none had seizures at the
late follow-up. Indications for Mapping With AVMs
Preoperative functional imaging was performed in all 12 of our
DISCUSSION patients and it demonstrated proximity of the AVM to the
language or motor cortex. Many functional imaging options are
The safety of electrocortical stimulation mapping during available, and we have used PET scans, MSI, and fMRI. Our
surgery for brain AVMs has been reported previously,13-19 and current imaging modality of choice is fMRI because it is easy to
our small experience with 12 AVMs in motor and language areas acquire, is convenient to review on our hospital network, and
confirms its feasibility and safety. There were no complications enables excellent correlation with brain and AVM anatomy.
associated with its use. Motor mapping required minimal alter- fMRI is based on changes in imaged blood flow with functional
ation in the usual operative routine, but the neurosurgeon must activation, and we have found, like others, that abnormal
be prepared to control intraoperative seizures. Language mapping hemodynamics of AVMs interfere with functional imaging,
required significant alteration in the usual operative routine, but overestimating the area of functional cortex.6,7,20,21 However, the
there were no awkward circumstances for the neurosurgeon and information from fMRI is sufficient to apply the algorithm that
FIGURE 3. Patient 10. Digital subtraction angiography [left internal carotid artery injection, lateral (A) and anteroposterior (B) views] demonstrated a Spetzler-Martin
grade II AVM adjacent to motor cortex. C, the AVM was located in the central sulcus, and motor mapping confirmed motor function immediately anterior to the nidus (10).
D, the superficial dissection was in subarachnoid spaces, but deep dissection was in parenchymal planes. The nidus was encircled (E) and resected completely (F). AVM,
arteriovenous malformation.
the absence of a control group of patients with AVMs operated on Securing the airway may interrupt surgery at a critical juncture.
without mapping make it impossible to conclude that brain Intraoperative anesthetic management should include vigilance
mapping with language and motor AVMs improves outcomes. for sudden hemodynamic changes that might require mas-
However, mapping does allow for safe surgical dissection that sive fluid resuscitation and pharmacological manipulation of the
resulted in more complete resections in these 12 patients than circulation. The anesthesiologist must be prepared with large bore
might have otherwise been achieved. intravenous access, numerous intravenous sites for multifaceted
There are, however, substantial risks to resecting an AVM in an resuscitation, vasoactive agents, and warm fluids.
awake patient that should not be underestimated. Loss of airway
patency, significant hemorrhage, and hemodynamic instability An Alternative Strategy for Language and Motor
can present daunting challenges in a patient in rigid pin fixation Cortex AVMs
with an unsecured airway. Even mild hypoxemia or CO2 The AVMs in 4 patients treated with incomplete circum-
retention can impair brain relaxation and surgical exposure. dissection (dearterializing the nidus while preserving the
TABLE 3. Surgical Results and Patient Outcomes After AVM Surgery With Brain Mappinga
Seizures mRS
Additional F/U,
Patients AVM Resection Complications Postop 3 mo Treatment Preop Postop Last y Obliteration
Awake
1 Incomplete None No No Radiosurgery 1 2 3 1.0 Hemorrhage, embolization,
complete resection
2 Total None No No None 2 3 3 0.8
3 Total None Temporal Temporal None 1 1 1 6.0
4 Total ICH No No None 1 3 1 1.0
5 Total EDH No No None 1 3 0 2.0
Asleep
6 Incomplete None No No Radiosurgery 1 4 3 Within latency period
7 Total None No No None 3 4 1 11.0
8 Incomplete Intraop seizure Focal motor No Radiosurgery 1 4 1 2.0 Obliterated
9 Total Intraop seizure No No None 1 1 0 2.0
10 Total None No No None 0 4 0 2.0
11 Total None No No None 3 1 1 1.0
12 Incomplete None Generalized No Radiosurgery 1 3 1 8.0 Within latency period
a
AVM, arteriovenous malformation; mRS, modified Rankin Scale; EDH, epidural hematoma; ICH, intracerebral hematoma; Preop, preoperative; Postop, postoperative;
F/U, follow-up; Intraop, intraoperative.
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