J Neurosurg Pediatrics 14:38–42, 2014
©AANS, 2014

Surgery for a giant arteriovenous malformation without
motor deterioration: preoperative transcranial magnetic
stimulation in a non-cooperative patient
Case report
Annick Kronenburg, M.D.,1 Tristan van Doormaal, M.D., Ph.D.,1
Pieter van Eijsden, M.D., Ph.D.,1 Albert van der Zwan, M.D., Ph.D.,1
Frans Leijten, M.D., Ph.D., 2 and Kuo Sen Han, M.D., Ph.D.1
Departments of 1Neurosurgery and 2Clinical Neurophysiology, Brain Center Rudolf Magnus, UMC Utrecht,
The Netherlands
Transcranial magnetic stimulation (TMS) is a noninvasive activation method that is increasingly used for motor mapping. Preoperative functional mapping in vascular surgery is not routinely performed; however, in cases of
high-grade arteriovenous malformations (AVMs), it could play a role in preoperative decision making. A 16-year-old
male was suffering from a giant, right-sided insular, Spetzler-Martin Grade V AVM. This patient’s history included
3 hemorrhagic strokes in the past 3 years, resulting in Medical Research Council Grade 2–3 (proximal) and 2–4
(distal) paresis of the left side of the body and hydrocephalus requiring a ventriculoperitoneal shunt. Preoperative
TMS showed absent contralateral innervation of the remaining left-sided motor functions. Subsequently, the AVM
was completely resected without any postoperative increase of the left-sided paresis. This case shows that TMS can
support decision making in AVM treatment by mapping motor functions.
(http://thejns.org/doi/abs/10.3171/2014.4.PEDS13592)

Key Words
•
arteriovenous malformation •
brain mapping
•
eloquent area
microsurgical resection
•
outcome
•
pediatric hemorrhagic stroke
•
vascular disorders

A

rteriovenous malformations (AVMs) are a major cause of pediatric hemorrhagic stroke (HS),
accounting for almost half of the strokes in children, with an average annual incidence rate of 0.5 case
per 100,000 person-years.9,17,29 The etiology of cerebral
AVMs remains unclear, but genetic factors have been
suggested to play an important role, which is supported
by associations with other diseases such as WyburnMason syndrome.1 Clinical features of this syndrome are
AVMs involving the retina, brain, and skin of the face
and result from an error in the development of vessels
at the 7th week of gestation.25 Patients present with seizures, hemorrhages, or headache.16 The annual risk of
AVM hemorrhage in pediatric patients is estimated to be

Abbreviations used in this paper: AChA = anterior choroidal
artery; AVM = arteriovenous malformation; EVD = external
ventricular drain; fMRI = functional MRI; GCS = Glasgow Coma
Scale; HS = hemorrhagic stroke; ICA = internal carotid artery; MCA
= middle cerebral artery; MEG = magnetoencephalography; MRA
= MR angiography; MRC = Medical Research Council; PCA =
posterior cerebral artery; TMS = transcranial magnetic stimulation;
VP = ventriculoperitoneal.

38

•

2%–4% per year and is even higher in patients with previously ruptured AVMs.7,24,26,29 Case fatality rates vary from
5.2% to 54%, with a reported average mortality of 25% in
children with HS.3,9,11,24
Treatment options for intracerebral AVMs are microsurgical removal, endovascular embolization, stereotactic
radiosurgery, or a combination of these techniques.1,29
Large high-grade AVMs are often located in or near eloquent areas, such as the motor cortex. Surgery can be
destructive as a result of direct damage to the brain, especially during severe intraoperative hemorrhage, or as a
result of ischemia caused by obstruction of arteries, which
have en passant feeders combined with a large or essential
cerebral perfusion territory.7,24,29
When considering neurosurgical intervention, preoperative motor mapping can be performed.28 A noninvasive
instrument that is increasingly used in tumor surgery is
transcranial magnetic stimulation (TMS). It can stimulate
the cortex by generating a magnetic field passing through
the scalp21–23,28 and may be used to map the motor cortex
by activating the cortex with single pulses and to simultaneously record motor evoked potentials.18,28
Transcranial magnetic stimulation has the advanJ Neurosurg: Pediatrics / Volume 14 / July 2014

Transcranial magnetic stimulation before AVM surgery
tage that patients do not have to lie still as in functional
MRI (fMRI) or magnetoencephalography (MEG). We
describe a 16-year-old patient with a giant, right-sided,
insular AVM in whom we performed preoperative TMS.

Case Report
History and Examination. In 2009, a 12-year-old
patient presented to our institution with severe headache,
vomiting, lethargy, and progressive left-sided paresis
(Medical Research Council [MRC] Grade 4).4 Since early
childhood, our patient had suffered from coordination and
fine motor skills disorders of his left arm without evident
signs of (hemi)paresis. General examination showed redness of the forehead, nose, and right cheek. Papilledema
and a retinal vascular malformation of the right eye were
documented during eye examination; neurological examination showed a lethargic child with a slightly dilated
right pupil and MRC Grade 4 left-sided paresis. Magnetic
resonance imaging demonstrated a space-occupying lesion
in the right hemisphere without signs of stroke (Fig. 1A);
MR angiography (MRA) and digital subtraction angiography revealed a giant Spetzler-Martin Grade V AVM in
the insula with the anterior choroidal artery (AChA) and

lenticulostriate arteries as the major feeding arteries with
an additional contribution of the posterior cerebral artery
(PCA; Fig. 1B–D). Combining these findings, we diagnosed Wyburn-Mason syndrome.16,25 We faced a difficult
decision in the multidisciplinary consultation. Treatment
with embolization carried a great risk of complications,
and complete cure could not be achieved.
At that time, in our opinion, the only option was coiling the associated aneurysm. This procedure was performed and resulted in partial stenosis of the AChA. Stereotactic radiosurgery was not indicated because of the
size of the AVM. As surgery could result in a significant
chance of complete hemiplegia, we adopted a wait-andsee policy. At discharge, the left-sided paresis recovered
to an MRC Grade 5.
In the subsequent 3 years, our patient suffered from
2 major intracerebral hemorrhages with breakthrough
into the ventricular system, resulting in a poor but slowly
recovering neurological state; a temporary external ventricular drain (EVD) was needed at both admissions. At
the first HS, he presented with the acute onset of paralysis
of his left arm and MRC Grade 4 paresis of his left leg,
which recovered to Grade 5 left-sided paresis (identical to
his neurological status before the first HS). At the second
HS, he presented with Grade 2 acute paresis of his left

Fig. 1. Axial T2-weighted MR image (A) showing a space-occupying lesion in the right hemisphere suspected to be an AVM
(arrows). Axial MRA reconstruction (B) confirmed a giant AVM, with the MCA (gray arrow) and PCA (white arrow) as major feeding arteries. Anteroposterior and lateral angiograms of the right ICA (C and D) and right vertebral artery (E and F) illustrating
the complex architecture, with the AChA (white arrows) and PCA (gray arrows) as feeding arteries of the AVM. Axial CT scans
demonstrate the first (G), second (H), and third (I) HSs from the AVM; all hemorrhages involved the ventricular system and caused
hydrocephalus. Hemorrhage originating from the posterior site (black arrow) of the AVM (G), bleeding from the frontolateral part
(black arrow) of the AVM (H), and bleeding from the frontomedial site (black arrow) of the AVM in the basal ganglia (I), with bilateral EVDs inserted.

J Neurosurg: Pediatrics / Volume 14 / July 2014

39

A. Kronenburg et al.
arm and Grade 3 paresis of his left leg, which recovered
to Grade 4 left-sided paresis at discharge.
At the age of 16, he suffered from a third HS. He presented with a Glasgow Coma Scale (GCS) score of 3 and
fixed dilated pupils, and bilateral EVDs were emergently
inserted. Finally, a ventriculoperitoneal (VP) shunt was
placed for shunt-dependent hydrocephalus (Fig. 1G–I).
He recovered from his coma slowly but considerably well.
Thirty days after the hemorrhage, he recovered to a GCS
score of E4M6V4, and neurological examination showed
a lethargic patient with left-sided paresis (left arm: Grade
4 proximally and Grade 2–3 distally; left leg: Grade 4
proximally and Grade 2 distally) and hemianopia.
At this phase, we were concerned about a large AVM
located in a part of the brain—a presumed eloquent area—
that had bled repeatedly. Untreated, the AVM could rebleed
with a high chance of death. Complete embolization was
not feasible because of the complex architecture and size of
the AVM (Fig. 1E and F). Preoperative embolization was
extensively discussed with the intervention radiologists, but
the procedure was not performed for the following reasons:
1) access to the AVM was very challenging, 2) rupture risks
were expected to be high, 3) partial embolization of this
type of AVM could result in difficult intraoperative mobilization and resection, and 4) the AVM had bled at 3 different sites. We concluded that the disadvantages of embolization were greater than the theoretical benefits. Stereotactic
radiosurgery was not indicated for this large AVM. Therefore, we finally decided that surgery was the only option.
We assumed that surgery would mean a significant chance
of complete hemiparesis; therefore, we used a noninvasive
tool to determine to what extent we could expect postoperative motor deficits. We used a MagPro Compact TMS
round coil (Medtronic) generating biphasic single-pulsed
stimuli (protocol described elsewhere15). Motor responses
were recorded with electromyography electrodes from the
right and left thenar muscles. Transcranial magnetic stimulation over the left central sulcus produced an intact contralateral motor response, but the contralateral response was
absent during stimulation over the right central sulcus. We
assumed that the remaining left-sided motor function was
innervated ipsilaterally as a consequence of brain plasticity, because of the AVM and repeated right-sided HSs.

Operation. The AVM had 3 main feeding sites: 1)
frontal/basal: lenticulostriate arteries of the middle cerebral artery (MCA) and the AChA (Fig. 1C and D), 2)
posterior/basal: PCA/posterior communicating artery
(Fig. 1E and F), and 3) posterior/cranial: posterior choroidal branches. Our surgical approach consisted of a
right-sided pterional approach combined with extension
toward a subfrontal and pretemporal route. We achieved
this by first meticulously occluding the lenticulostriate
feeders from M1, which led to a significant reduction in
flow through the AVM and consequently its size, allowing access to the tip of the basilar artery and the proximal
right PCA, seen through the triangle formed by oculomotor nerve and internal carotid artery (ICA). Subsequently,
feeders arising from the basilar tip and the proximal PCA
were coagulated. The AVM was then exposed in the medial wall of the right ventricle through a frontal corticoto40

my, which allowed occlusion of the anterior and posterior
choroidal feeders and complete resection. No complications occurred during surgery. The total duration of the
procedure was 11 hours.

Postoperative Course. Our patient recovered well
from surgery with no additional deficits except for complete right-sided oculomotor paresis. Revision of the VP
shunt was required 1 week postoperatively because of
blood clots in the pump. The patient was discharged to
a rehabilitation center 2 weeks after surgery. Computed
tomography angiography documented complete resection
of the AVM (Fig. 2). At the 6-week follow-up, neurological examination revealed stable residual hemiparesis as
had appeared preoperatively. The oculomotor nerve paresis improved, with a lateral position of the right eye and
disappearance of the vertical gaze paresis.

Discussion

We described a 16-year-old patient with a giant,
right-sided, insular AVM. During the preoperative workup, cortical motor function was mapped using TMS and
showed absent contralateral innervation of the remaining
left-sided motor functions. A longer wait-and-see policy
was not an option, and aggressive treatment seemed justified because of the size of the AVM and the apparent high
chance of hemorrhage.
Because most AVMs are congenital, the developing
brain is able to take over behavioral functions for the affected hemisphere, resulting in ipsilateral innervation,
especially in children with the plasticity of the maturing
CNS in which reorganization of motor control occurs, in
particular in the context of early developed lesions.5,15,24
Preoperative counseling is beneficial in managing patient expectations and influences neurosurgical decision
making. Transcranial magnetic stimulation revealed that
our patient’s motor function was not served by the contralateral hemisphere. Although TMS did not fully demonstrate ipsilateral innervation, the postoperative course
fits the assumption that there was ipsilateral innervation.
Brain mapping in children is challenging because
of the reduced level of cooperation, which is required in
procedures like fMRI. Multiple types of functional brain
mapping have been reported (mostly applied in tumor
surgery), and several advantages specific to each mapping

Fig. 2. Postoperative axial (left) and coronal (right) reconstruction
CT angiograms showing complete resection of the AVM in the right
hemisphere.

J Neurosurg: Pediatrics / Volume 14 / July 2014

Transcranial magnetic stimulation before AVM surgery
type have been described.2,5,6,8,12,13,21–23,27,28 Regardless of
the suggested benefits of other mapping methods, TMS
offers the advantage of being the only noninvasive, reversible inhibition technique and is more commonly used
in the neurosurgical field for motor mapping in patients
incapable of fully cooperating.13,28 Transcranial magnetic
stimulation results on lateralization of motor innervation were confirmed using fMRI in a recent study.15 An
important limitation of fMRI is its inability to show the
complete area involved in motor performance.13 Mapping
using this method can be inaccurate, defining functionally active brain as inactive as a result of the altered hemodynamics surrounding an AVM.13 Furthermore, TMS
recordings have been shown to be more accurate than
fMRI in preoperative mapping, providing information
on cortical neurons without being influenced by cerebral
hemodynamics.10,13,28 Our patient was insufficiently cooperative and could not lie completely still for successful
fMRI and MEG, and TMS seemed the optimal and most
reliable mapping method, because it does not rely on a
patient’s full participation nor does it require strict immobility. Clear estimations of the positive and negative predictive value of TMS in neurosurgical motor lateralization are lacking. In recent studies, preoperative navigated
TMS results correlated well with direct cortical stimulation data in identifying the primary motor cortex; the
negative predictive value of navigated TMS, as compared
with direct cortical stimulation, in preoperative language
mapping was 83.9%.19,20 To definitely establish the accuracy of TMS in preoperative mapping, prospective trials
are needed to relate the results of TMS with intraoperative or postoperative findings.14
The age of and the hemiparesis and hemodynamic
problem in our patient made for difficult decisions in
which TMS helped as a feasible and robust mapping
method. This technique enabled us to manage patient
expectations and perform a microsurgical removal that
resulted in a satisfying outcome.
Disclosure
The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this
paper.
Author contributions to the study and manuscript preparation
include the following. Conception and design: Han, Kronenburg, van
Doormaal, van Eijsden. Acquisition of data: Kronenburg. Analysis
and interpretation of data: Han, Kronenburg, van Doormaal, van
Eijsden, Leijten. Drafting the article: Kronenburg, van Doormaal,
van Eijsden. Critically revising the article: all authors. Reviewed
submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Han.
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Manuscript submitted November 7, 2013.
Accepted April 7, 2014.
Please include this information when citing this paper: published online May 9, 2014; DOI: 10.3171/2014.4.PEDS13592.
Address correspondence to: Kuo Sen Han, M.D., Ph.D., Department of Neurology and Neurosurgery, Brain Center Rudolf Magnus, UMC Utrecht, Heidelberglaan 100, Postbus 85500, 3508 GA
Utrecht, The Netherlands. email: khan@umcutrecht.nl.

J Neurosurg: Pediatrics / Volume 14 / July 2014