Acta Neurochir (2012) 154:12551262

DOI 10.1007/s00701-012-1357-6

CASE REPORT

Navigated three-dimensional intraoperative

ultrasound-guided awake resection of low-grade glioma
partially infiltrating optic radiation
Andrej teo & Martin Karlk & Peter Mendel &
Miroslav k & Juraj teo

Received: 16 February 2012 / Accepted: 6 April 2012 / Published online: 4 May 2012
# Springer-Verlag 2012

Abstract We report a case of awake resection of temporal

low-grade glioma infiltrating the optic radiation (OR). The
OR was localized by direct electrical stimulation (DES) and
the tumor was delineated by navigated intraoperative 3D
ultrasound. Ultrasound artifacts were eliminated by 3Dultrasound data acquisition with a miniature probe inserted
into the resection cavity. A total of 97 % resection was
achieved, and small tumor portion involving OR was intentionally left in place. Functional result was partial quadrantanopia instead of more profound visual deficit, which
would follow gross-total resection. To our knowledge,
DES of OR was reported once; the aforementioned method
of ultrasound artifact elimination has not been reported
before.

A. teo : J. teo (*)

Department of Neurosurgery, Derers Hospital,
Comenius University School of Medicine,
Limbova 5,
833 05 Bratislava, Slovakia
e-mail: juraj.steno.ba@gmail.com
J. teo
e-mail: juraj.steno@fmed.uniba.sk
M. Karlk
Department of Neurology, Derers Hospital, Comenius University,
Bratislava, Slovakia
P. Mendel
Department of Anesthesiology, Derers Hospital,
Slovak Medical University,
Bratislava, Slovakia
M. k
Institute of Diagnostic Imaging,
Trnava, Slovakia

Keywords Awake resection . Direct electrical stimulation .

Intraoperative ultrasound . Optic radiation . Low-grade
glioma

Introduction
Literature regarding monitoring of visual functions during
awake resection (AR) of infiltrative gliomas is sparse [2, 3,
12, 17, 18].
We report a case of right-sided temporal grade II oligodendroglioma infiltrating the optic radiation (OR). Direct
electrical stimulation (DES) of OR and navigated threedimensional intraoperative ultrasound (3D-iUS) contributed
to the achievement of an extensive resection and to a satisfactory functional result.
Clinical report
Presentation and examination A 43-year-old man, a medical doctor, initially presented with an epileptic seizure.
Magnetic resonance imaging (MRI) revealed a nonenhancing, hyperintense tumor in his right temporal lobe
(Fig. 1a, b). Digital tensor imaging (DTI) fused with fluidattenuated inversion recovery (FLAIR) MRI sequence
showed infiltration of inferior portion of OR at the level of
atrium of lateral ventricle (Fig. 2a, b). Ophthalmologic
investigation showed no visual deficit. The patients wish
was to preserve as much visual function as possible. An AR
with DES of OR and navigated 3D-iUS was proposed.
Operating procedure General anesthesia was inducted by
using intravenously administered remifentanil and propofol.
A laryngeal mask was used to secure airways. The patient
was positioned on his left side, and his head was fixed in a

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Acta Neurochir (2012) 154:12551262

Fig. 1 a, b 3D FLAIR MRI

sequence (axial scans) showing
hyperintense tumor in the right
temporal lobe. c, d Follow-up
MRI 3 months after resection;
full white arrow small residuum
at the level of atrium of lateral
ventricle

Mayfield headrest. For navigation, a system that integrates

standard neuronavigation and 3D-iUS and provides automatic fusion of both modalities (SonoWand Invite, SONOWAND AS, Trondheim, Norway) was used.
A tailored temporal craniotomy was performed. The initial
3D-iUS scan was performed on the dural surface. Obtained
data were automatically fused with the preoperative navigation MRI sequence (Fig. 3). After opening of the dura, the
patient was fully woken up. Subsequently, a black-and-white
line drawing portraying a dog (size 60 40 cm), with a cross
in the center of the picture, was fixed in front of the patients
face (Fig. 4, left). The drawing was set up at a distance
approximately 50 cm from the patients eyes, in a position in
which the dogs head was in the left superior quadrant and the
back legs were in the right inferior quadrant of the patients
visual field. Afterwards, the neurologist started to investigate
patients visual field using a laser pointer directing consecutively to all parts of the picture. When the patient saw the red
point, he confirmed the localization verbally. Only binocular
(both eyes open) visual field was investigated.
The tumor resection was performed in a standard fashion
using microsurgical techniques. After entering the subcortical

tumor part, the visual field was continuously investigated in

the manner described above. When the resection came close to
the expected location of the OR, bipolar subcortical stimulation at 4 mA was used in order to localize the OR.
After the opening of lateral ventricle, the 3D-iUS data
was updated via scanning the brain with the large linear
ultrasound probe placed on the surface of the brain. The
structures alongside the resection cavity were distinctly
depicted, but, as expected, ultrasound acoustic enhancement
artifacts (AEAs) appeared at the bottom of the resection
cavity during the scanning from the brain surface (Fig. 5a,
b). To eliminate AEAs, 3D-iUS data acquisition was performed with a miniature ultrasound probe inserted into the
resection cavity. A distinct depiction of structures under the
bottom of resection cavity was achieved (Fig. 5c). A small
tumor residuum in the presumed localization of right OR
was visible at the updated 3D-iUS scan (Fig. 6). Stimulation
of this glioma-infiltrated tissue repeatedly elicited bright
phosphenes in the left superior quadrant of patients visual
fieldhe could not see the dogs head, neck, or chest, while
the other body parts were distinct (Fig. 4, right). Residuum
involving OR was intentionally left in place. Visual

Acta Neurochir (2012) 154:12551262

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Fig. 2 a, b DTI fused with 3D

FLAIR MRI sequence showing
partial infiltration of inferior
portion of optic radiation (bold
arrows) at the level of atrium of
lateral ventricle. c, d
Postoperative tractography
showing OR partially infiltrated
by the residual tumor (thin
arrows)

functions were investigated again, and no obvious visual

field deficit was detected. Subsequently, the patient was
introduced into general anesthesia, and the operation was
terminated.
Postoperative course Although the patient did not report
any visual disturbance postoperatively, automated perimetry
performed on the second postoperative day (Fig. 7a, b)
showed incongruous homonymous left superior quadrantopia (complete in the right eye, and incomplete in the left
eye). The follow-up automated perimetry performed
3 months after the surgery showed partial left superior
quadrantopia in visual field of the right eye, and a minor
scotoma within left superior quadrant of the left eye (Fig. 7c,
d); visual acuity was normal.
The histopathological examination revealed WHO grade
II oligodendroglioma. The follow-up MRI obtained
3 months after the tumor resection showed a small tumor
residuum (Fig. 1c, d) with a part of OR infiltrated (Fig. 2c,
d). According to volumetry based on postoperative FLAIR
MRI sequence, resection of 97 % of hyperintensive tissue
was achieved. One month after the surgery, the patient
returned to his normal socio-professional life.

Discussion
For significant improvement of patients prognosis, the resection of LGG tissue should be at least subtotal [11]. However,
surgery of LGG is complicated by frequent infiltration of
cortical and subcortical structures that still may be functional
[1, 4, 16, 20]. Subcortical injuries are often far more devastating than cortical injuries of comparable volume [7]. Therefore,
the eloquent subcortical tracts must be intraoperatively
detected in order to preserve the anatomo-functional connectivity while optimizing the extent of resection [5].
Intraoperative detection of optic radiation
Literature regarding intraoperative neuromonitoring of OR
is sparse, despite the fact that some level of visual field
defect is a frequent occurrence after resection close to this
structure [6, 22].
At the level of atrium of lateral ventricle, all three bundles of OR (anterior bundle, i.e., Mayers loop, central
bundle, and posterior bundle) form the lateral ventricular
wall; resection of this part of OR causes a complete homonymous hemianopia [6].

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Acta Neurochir (2012) 154:12551262

Fig. 3 Left column: 3D FLAIR

MRI navigation sequence.
Right column: Initial 3D-iUS
image scanned from the dural
surface fused with the preoperative navigation MRI; arrows
lateral ventricle containing
hyper-echogenic choroid plexus

Permanent hemianopia is not a minor deficit, and often

interferes with a patients everyday activities [15, 27]. On
the contrary, superior quadrantopia resulting from Mayers
loop damage is often not recognized by the patients and the
degree of functional disability is minimal [19]. However,
quadrantopia can also pose a substantial problem [12] because it can preclude the ability of safe driving [14]. Similarly to speech and language or motor functions,
preservation of visual functions should be considered in
glioma patients. The only acceptable reason for voluntarily
generated hemianopia could be a glioma, in which the
removal with an impact on patients prognosis is not possible without complete unilateral resection of OR and/or visual cortex [26].
Fig. 4 Left: Visual field testing
before tumor resection (whole
line drawing is displayed in red
frame upper left); red arrow:
red point emitted by laser
pointer. Right: Intraoperative
photograph of the resection
cavity. The bipolar stimulation
probe stimulating the infiltrated
part of OR (empty yellow
arrow). The choroid plexus is
prolapsing into the resection
cavity (full yellow arrow)

Apart from OR tractography implemented into conventional neuronavigation (which can become inaccurate due to
the brainshift) there are three methods of detection and/or
neuromonitoring of the OR during a glioma resection: monitoring of cortically recorded VEPs [9, 13], intraoperatively
updated OR tractography [21, 22], and subcortical OR stimulation in an awake patient [3]. Subcortical stimulation of
OR during AR was first reported by Duffau et al. [3]. OR
constituted the posterior and deep functional boundary of
the resection. The detection of OR helped the surgeon to
avoid postoperative hemianopia in spite of a quadrantopia.
Mapping of visual functions in awake patients without
stating whether visual cortex or visual pathways were stimulated was documented by Serletis and Bernstein [17] and

Acta Neurochir (2012) 154:12551262

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Fig. 5 a Initial 3D-iUS image scanned from the dural surface showing
the lower part of the tumor. b 3D-iUS scan performed from the dural
surface during the resection. Center of the yellow cross AEAs. c
Eliminated AEAs. 3D-iUS data were acquired with a miniature probe

inserted within the resection cavity. The tumor was removed; only a
thin rim of edematous brain tissue is present at the bottom of the
resection cavity (center of the yellow cross)

by Shinoura et al. [18]; DES of the visual cortex during an

awake tumor resection was published by Danks et al. [2] and
Nguyen et al. [12].

Intraoperative ultrasound provides real-time imaging [23]

and allows re-scanning of operating field as often as necessary. On the other hand, the main disadvantage of older 2D
ultrasound systems was low image quality [24]. The orientation problem of the 2D ultrasound plane was considerable for
most surgeons [23]. Differentiation of brain structures was
challenging, and required extensive experience. Especially
problematic is ultrasonic depiction of medial tumor borders
after some tumor debulking [8] due to the presence of AEAs at
the bottom of resection cavity. AEAs appear when ultrasound
penetrates through a higher column of water.

Ultrasound in glioma surgery

Resections of LGG are faced with the problem of macroscopic
similarity of LGG and normal brain. After the occurrence of
brainshift, neuronavigation can become inaccurate [3]. The
only way to differentiate the LGG tissue during the entire
operating procedure is intraoperative imaging.
Fig. 6 Left column Initial 3DiUS image. Right column 3DiUS image acquired via scanning with mini-probe inserted
within the resection cavity; yellow arrows small tumor residuum involving the lower part of
the OR at the level of the atrium
of lateral ventricle. Hyperechogenic choroids plexus prolapsing into the resection cavity
(blue arrow). Center of the yellow cross (the tip of the pointer)
area where the DES elicited
phosphenes

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Acta Neurochir (2012) 154:12551262

Fig. 7 Postoperative
automated perimetry. Two days
after surgery: left eye (a), right
eye (b). Three months after
surgery: left eye (c), right eye
(d)

Contrary to older systems, newer 3D-iUS systems provide image quality comparable to high-field MRI [25].
Depiction of glioma tissue is at least as accurate as T2weighted MRI sequences [25]. Intraoperative fusion with
preoperative MRI, and the possibility of intraoperative image rendering in axial, coronal, and sagittal planes make
recognition of brain structures relatively simple [10]; application of anatomical knowledge is rather straightforward.
Presented case
To the best of our knowledge, our case is the second
reported case of DES of OR. Subcortical stimulation
allowed detection of OR. In general, the current intensity
adapted to each patient is determined at eloquent cortex by
progressively increasing the amplitude by 1-mA increments
from a baseline of 2 mA until a functional response is
elicited, with 6 mA as the upper limit for an awake patient
[4, 5]. Subsequently, the same current intensity is used for
subcortical stimulation in the given patient. However, as no
visual (or any other eloquent) cortex was approachable for
DES in our patient, we selected the current intensity

according to the data published by Nguyen et al., who

successfully stimulated visual cortex at the current intensity
level of 4 mA [12]. After the detection of OR by DES, a
small tumor residuum involving a part of OR fibers was
intentionally left in place. The functional result was an
incongruous partial homonymous left upper quadrantanopia, in spite of more profound visual field deficit, which
would inadvertently follow further resection. However, like
the authors who first presented the method [3], we were not
able to avoid the permanent visual field deficit completely.
We believe that a plausible explanation of this phenomenon
could be as follows: the important information that OR is
already reached can only be gained by DES of OR (presenting with phosphenes or other visual disturbances) and not by
the presence of a developing visual field deficit (due to
gradual OR resection) because this deficit may not be in
its initial stages recognized by the patient. Thus, we most
probably used DES too late (after the opening of the inferior
part of the atrium), when anterior bundle of OR had already
been interrupted. Similar assumption was stated by Duffau
et al. [3]. The negative result during the final visual field
testing performed intraoperatively by the neurologist may be

Acta Neurochir (2012) 154:12551262

explained by the fact that visual field of the left eye was
minimally affected. Because the visual field was tested with
both eyes open (in order to preserve effective visual
functions), the sparsely affected visual field in the left eye
could preclude the detection of the scotoma in the left upper
hemifield of the right eye.
The method of ultrasound artifact elimination via intracavitary 3D-iUS data acquisition has not been reported
before. In this way of scanning, the column of water between the tip of the miniature probe and scanned tissue at
the bottom of resection cavity was naturally much smaller
than in scanning with a larger probe placed on the brain
surface. AEAs at the bottom of resection cavity were successfully eliminated, and the structures in the medial part of
resection cavity were distinctly depicted.

Conclusions
DES of OR repeatedly elicited phosphenes, and thus
allowed intraoperative OR identification. The intracavitary
3D-iUS data acquisition enabled distinct depiction of the
structures at the median part of resection cavity. Resection
of the residuum involving part of OR would lead to a more
profound visual deficit than the partial quadrantopia. The
patient does not report any change in his visual functions
when compared to the preoperative status. Although a new
visual field deficit could not be completely avoided, the
functional result was satisfactory. However, studies with a
larger number of patients are needed to validate the presented methodology.

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7.

8.
9.

10.

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12.

13.

14.

15.
16.

17.
Conflicts of interest None.
18.

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