Download Meta analysis

Chinese Medical Journal 2012;125():
1
Original article
Clinical experience of 3T intraoperative magnetic resonance
imaging integrated neurosurgical suite in Shanghai Huashan
Hospital
QIU Tian-ming, YAO Cheng-jun, WU Jin-song, PAN Zhi-guang, ZHUANG Dong-xiao, XU Gen,
ZHU Feng-ping, LU Jun-feng, GONG Xiu, ZHANG Jie, YANG Zhong, SHI Jian-bin, HUANG Feng-ping,
MAO Ying and ZHOU Liang-fu
Keywords: intraoperative magnetic resonance imaging; glioma; pituitary adenoma
Background Intraoperative magnetic resonance imaging (iMRI) dates back to the 1990s and has been successfully
applied in neurosurgery but they were low-field iMRI (<1.0T). This paper reports the clinical experience with a 3T
iMRI-integrated neurosurgical suite in Huashan Hospital, Shanghai, China.
Methods From September 2010 through March 2012, 373 consecutive patients underwent neurological surgery under
guidance with 3T iMRI. A retrospective analysis was conducted regarding clinical efficiency.
Results All surgery in the 373 patients was safe. The ratio of gross total resection for cerebral gliomas (n=161) was
increased from 55.90% to 87.58%. The ratio of benefit in extent of resection was 39.13%. One hundred and fifty eight of
the 161 glioma patients accomplished follow-up at 3 months postoperatively. Twenty of 161 patients (12.42%) suffered
from early motor deficit after surgery. Late motor deficit was however observed in five of 158 patients (3.16%).
Twenty-one of 161 patients (13.04%) had early speech deficit and late speech deficit was only observed in six of 158
patients (3.8%). The ratio of gross total resection for pituitary adenomas (n=49) was increased from 77.55% to 85.71%.
The ratio of benefit in extent of resection was 10.2%. There were no iMRI-related adverse events even for patients who
underwent awake craniotomy.
Conclusion The 3T iMRI integrated neurosurgical suite provides high-quality intraoperative structural functional and
functional imaging for real-time tumor resection control and accurate functional preservation, resulting in an improvement
in maximal safe brain surgery.
Chin Med J 2012;125():
T
he emergence of image-guided neurosurgery has
drastically revolutionized neurosurgical procedures,
yet brain shift is one of its limitations, decreasing both
accuracy and safety of surgery.1,2 The introduction of
intraoperative magnetic resonance Imaging (iMRI) and
various pioneering efforts in the 1990s has led to
development of minimal invasive neurosurgery.3 Between
2006 and 2012, 0.15 T PoleStar™ N-20 iMRI-guided
neurosurgery was performed >400 times at Huashan
Hospital in Shanghai, with a satisfactory outcome. In
2009, People’s Liberation Army General Hospital in
Beijing began working with 1.5 T iMRI, which was the
first neurosurgical institute in China to adapt high-field
iMRI.4 The utilization of a 3.0 T iMRI at Huashan
Hospital in 2010 prompted us to establish the iMRI
Integrated Neurosurgical Suite at Huashan Hospital,
ushering in a new digital era of minimally invasive
neurosurgery, which also became the foundation of
precision neurosurgery at our institute. Between
September 2010 and March 2012, a total of 373
procedures of consecutive iMRI-guided neurosurgery
were performed at our institute, and we take this
opportunity to share our experiences with this
state-of-the-art technology.
METHODS
Patient population
Patients were selected based on the following inclusion
criteria: (1) age ≥4 years; (2) potential benefit from the
use of iMRI as indicated by preoperative MRI such as
lesions nearby or locating at eloquent areas; and (3) no
contraindications according to the security screening table
for iMRI. The exclusion criteria included: (1) age <4
years; (2) contraindications for MRI scanning according
to the security screening table for iMRI; and (3) patient
refusal. Written informed consent was obtained from each
patient. This study was undertaken at the Huashan
DOI: 10.3760/cma.j.issn.0366-6999.2012.01.001
Glioma Surgery Division, Department of Neurosurgery, Huashan
Hospital, Fudan University, Shanghai 200040, China (Qiu TM, Yao
CJ, Wu JS, Pan ZG, Zhuang DX, Xu G, Zhu FP, Lu JF, Gong X,
Zhang J, Yang Z, Shi JB, Huang FP, Mao Y and Zhou LF)
Correspondence to: Dr. ZHOU Liang-fu, Department of
Neurosurgery, Huashan Hospital, Fudan University, Shanghai
200040, China (Tel: 86-21-52887206. Fax: 86-21-62492884.
Email: [email protected])
This study was supported by grants of the Ministry of Health of
China (2010-2012), National Natural Science Foundation of China
(No. 81071117, No. 81171295), and Shanghai Municipal Health
Bureau (No. XBR2011022).
Conflicts of interest: none.
Chin Med J 2012;125():
2
Hospital (Shanghai, China) with approval from the
Huashan Institutional Review Board.
3T iMRI integrated neurosurgical suite
The 3T iMRI integrated neurosurgical suite by IMRIS
(Winnipeg, MB, Canada) includes an intraoperative room
(OR) and a diagnostic room (DR); the core equipment in
which is a 1.73-m moveable 3.0 T magnet with a 70-cm
working aperture (MAGNETOM Verio; Siemens
Healthcare, Erlangen, Germany). The
magnet
incorporated into a ceiling mount enables the scanner to
move in and out of the OR, instead of moving the
operating table. The IMRIS Matrix surgical information
management system integrates all the information in the
suite including: the picture archiving and communication
system (PACS), images for neuronavigation, videos for
the operating microscope, videos for neuroendoscopy,
videos for the operating field monitor, OR full-viewing
monitor, signals for electrocardiography (ECG) monitor,
signals for the neurophysiological monitor, and other
digital information. This suite covers an area >300 m2
consisting of OR (72 m2), DR (48 m2), iMRI control
room (23 m2), post-anesthesia care unit (PACU) (10 m2),
data processing room (9 m2), and patient locker room (25
m2) (Figure 1). The OR and DR are both shielded from
radiofrequency (RF) radiation (Figure 1). OR equipment
comprises: (1) OR table (IMRIS) constructed from
high-grade, MR-compatible stainless steel and
composites, and can be rotated 90° from the magnetic
field axis; (2) MR-safe carbon fiber head holder (DORO
Radiolucent Headrest System; PRO-MED Instrumente
GmbH, Tuttlingen, Germany); (3) head RF coil (IMRIS)
matched to the head holder, separated into two
components with four channels each, the bottom of which
is left beneath the sterile field during surgery; (4)
MRI-safe anesthetic apparatus (Aestiva/5 MRI, GE
Healthcare, Wauwatosa WI, USA) and ECG monitor
(MAGLIFE C Plus, Schiller AG, Baar, Switzerland); (5)
ceiling-mounted neuronavigation system (TRIA i7;
Medtronic Navigation, Inc., Minneapolis, MN, USA); (6)
operating microscope with high-digital video and
navigation system (OPMI Pentero; Carl Zeiss AG, Jena,
Germany); (7) Multifunctional Neurological Workstation
(Epoch XP; AXON, New York, NY, USA); and (8)
Multimedia Interactive System for awake surgery
manufactured by ourselves.
Preoperative and postoperative evaluation
For all patients, history, preoperative and postoperative
neurological signs were recorded. Muscle strength and
language function were evaluated before surgery and
discharge. All patients were followed up for 3 months
after surgery. Glioma patients with lesions adjacent to the
language cortex underwent language function assessment
using the Aphasia Battery of Chinese (ABC),5 which is
the Chinese standardized adaptation of the Western
Aphasia Battery. Speech deficit was defined by language
function deterioration compared to preoperative status
according to ABC. Motor deficit was used to describe
those patients whose muscle strength decreased
postoperatively. Early deficits referred to those existing
before discharge and late deficits to those deficits found 3
months after surgery.
MRI acquisition and volumetric analysis
Preoperative MR images were obtained in the DR 1 day
prior to surgery and postoperative images
were obtained within 3 days after surgery.
The MRI sequences included a
contrast-enhanced,
3D,
magnetization-prepared, rapid-gradient
echo
(MPRAGE)
sequence,
fluid-attenuated
inversion
recovery
(FLAIR) sequence; diffusion tensor
imaging
(DTI);
blood
oxygen-level-dependent functional MRI
(BOLD fMRI); time-of-flight MR
angiography (MRA); multi-voxel MR
spectroscopy (MRS); and MR perfusion
images. The motor or language pathways
and activation of the motor or language
areas were then reconstructed into 3D
objects and integrated into the 3D
structural data using a postprocessing
workstation
(Syngo
MultiModality
Workplace; Siemens AG).
Figure 1. Plane chart of iMRI integrated neurosurgical suite in Huashan Hospital.
For high-grade glioma (HGG) or pituitary
adenoma, 3D MPRAGE images (plus
gadolinium) were used for volume
determination before and after resection.
FLAIR was considered for low-grade
Chinese Medical Journal 2012;125():
glioma (LGG). All pre-, intra- and postoperative tumor
segmentations were manually performed using the
OSIRIS software tool (Pixmeo, Switzerland) by a
neurosurgeon and were verified by an additional
neurosurgeon. The volumes of original or residual tumor
were measured. In this case series, gross total resection
(GTR) was defined as 100% resection of the tumor
volume.
Intraoperative procedure
The full-time team working in the 3T iMRI integrated
surgical suite includes six neurosurgeons, three nurses,
one neuronavigation technician, two anesthetists, one
radiologist, one radiology technician, and one OR worker.
All staff and patients were required to sign the security
screening table for iMRI. After endotracheal intubation
with intravenous anesthesia, the OR table was rotated 90°
to the magnetic field axis. The patient’s head was fixed in
position using a carbon fiber head holder, integrated with
the bottom part of the eight-channel coil and navigation
reference frame. The navigation technician registered the
patient’s head space to the MR images in the navigation
system. After craniotomy, we used functional
neuronavigation and electrophysiological techniques to
localize the eloquent brain cortex. After tumor resection,
all instruments and tables, with the exception of MRI-safe
equipment, were withdrawn by the nurses beyond the 5-G
boundary line. After draping the patient, the top part of
the coil was matched to the bottom part. Then the
neurosurgeons, nurses and radiology technician
completed the MRI safe checklist together. The RF
shielding door was opened and the scanner was moved
into the OR from the DR. When the scanner was moved,
all staff in the OR were required to ensure the safety of
the patient until his/her head was situated in the center of
the working aperture. All medical personnel then left the
OR and closed the RF shielding door. During
intraoperative MRI, the signals from the anesthetic
apparatus and ECG monitor were transmitted wirelessly
to the control room. When intraoperative MRI acquisition
was finished, the RF shielding door was reopened. The
wound was re-draped. If further resection were indicated,
the navigation technician would update the navigation
using the real-time intraoperative MR images.
RESULTS
There were 373 cases, including 125 male and 248
female, aged from 5 to 78 years (mean: 45.5 years). When
classified by surgical approach there were: 288
craniotomies, 57 trans-sphenoidal approaches, 25
biopsies, and three neuroendoscopic surgery. When
classified by pathology there were: 203 gliomas, 55
pituitary adenomas, 20 meningiomas, 19 moyamoya
disease, and 76 others. When classified by main lesion
location there were: 146 cases in the left hemisphere, 76
in the right hemisphere; 79 in the saddle area, 87 in the
frontal lobe, 46 in the temporal lobe, 32 in the parietal
lobe, 22 in the insular lobe, 17 in the occipital lobe, and
3
14 in the basal ganglia area. When classified by
anesthesia pattern there were: 339 with general
anesthesia, and 34 with awake craniotomy (Table 1).
All 373 patients received 1–4 intraoperative scans (mean:
1.88) at OR, and during the same time span a total of
6500 diagnostic MRI scans were performed for more
patients at DR. The image quality was sufficient in all
cases. Histopathological diagnosis confirmed 203 cases
of glioma, consisting of 112 HGGs (72 glioblastomas, 29
anaplastic
astrocytomas,
six
anaplastic
oligodendrogliomas, three gliosarcomas, one anaplastic
oligoastrocytoma, and one anaplastic ependymoma), and
91 LGGs (58 astrocytomas, 20 oligodendrocytomas, six
oligodendroastrocytomas, four gangliogliomas, two
pilocytic astrocytomas and one ependymoma). Both
preoperative and postoperative tumor volumes of 161
patients who underwent craniotomy for glioma resection
were acquired. The mean preoperative lesion volume was
59.24 cm3. iMRI revealed that 90 of 161 cases (55.9%)
achieved GTR and 71 had glioma residue, of which 63
cases (88.73%) required further resection, which gave a
benefit ratio was of 39.13% (63/161). Although eight
cases revealed tumor residue in eloquent areas, the
amount of tumor resected reached preoperative surgical
planning expectations and required no further resection.
Among the 63 cases that required further resection, iMRI
confirmed that 45 cases achieved GTR, with the
remaining 18 cases still suggesting tumor residue. Six
cases achieved GTR and 12 had tumor residue adjacent to
critical areas that warranted no additional surgery.
Table 1. Distribution of 373 cases with regard to histopathological
diagnosis, surgical approach, main lesion location, and anesthesia
pattern
Items
Histopathological Diagnoses
Glioma
Pituitary adenoma
Meningioma
Moyamoya disease
Craniopharyngioma
Lymphoma
Vascular malformation
Metastatic tumor
Chordoma
Others
Surgical approach
Craniotomy
Transsphenoidal
Biopsy
Endoscopic
Lesion mainly location
Frontal lobe
Saddle area
Temporal lobe
Parietal lobe
Insular lobe
Occipital lobe
Basal ganglia area
Others
Anesthesia pattern
General anesthesia
Awake craniotomy
n=373
203
55
20
19
13
11
8
6
3
35
288
57
25
3
87
79
46
32
22
17
14
76
339
34
Chin Med J 2012;125():
4
Eventually, 141 gliomas (87.58%, 141/161) achieved
GTR in 161 craniotomies. Therefore, the GTR rate for
patients improved from 55.9% (90/161) to 87.58%
(141/161). One hundred and fifty-one operations required
functional neuronavigation guidance due to the proximity
of the tumor and surrounding eloquent cortex and
subcortical tracts. Twenty of 161 patients (12.42%)
suffered from early motor deficit after surgery. Follow-up
at 3 months for 158 patients suggested five patients
(3.16%) had late motor deficit. Twenty-one of 161
patients (13.04%) presented with early speech deficit.
Follow-up at 3 months revealed that late language deficits
were observed in six of 158 patients (3.80%). Seven of
161 patients (4.35%) presented with severe postoperative
intracranial hematoma which required reoperation; one
died from severe infection and multiple organ failure.
Of the 49 trans-sphenoidal pituitary tumor resection
cases, histopathology confirmed that 31 were
nonfunctioning pituitary adenomas. Thirty-eight of 49
cases (77.55%) achieved GTR, while 11 cases showed
tumor residue on iMRI; five of which required further
resection and four eventually achieved GTR. Finally, 42
of 49 pituitary adenomas achieved GTR (85.71%). The
benefit ratio was 10.20% (5/49). The total resection rate
improved from 77.55% (38/49) to 85.71% (42/49).
Among 25 iMRI-guided biopsies, all histopathological
diagnoses were confirmed, comprising 14 gliomas, seven
lymphomas, three inflammatory granulomas, and one
germinoma.
Preoperative and intraoperative MRI lengthened surgery
by 1–3 hours (mean: 1.9 hours). Preoperative MRI
sequences included: T1 with contrast, T2 FLAIR, DTI,
multi-voxel MRS, BOLD fMRI, resting state fMRI, and
MR perfusion. Intraoperative MR sequences included: T1
with contrast, T2 FLAIR, and DTI. Superior images were
acquired resulting from the improved signal-to-noise ratio
due to increased field strength and redesigned RF coils.
There were no MR-related adverse events. Average
hospital stay for all cases was 18.81 days and the average
total expense for hospitalization was RMB 72043.20
Yuan. No iMRI-related infectious occurred in the
consecutive cases.
Illustrative case
A 39-year-old woman presented with a 2-month history
of repeated seizure attacks without motor or language
deficit. Preoperative MRI revealed a lesion located in the
right frontal lobe, with proximity to the motor cortex and
pyramidal tracts. The lesion was not enhanced and LGG
was considered to be the preliminary diagnosis based on
the increased ratio of choline/N-aceytl aspartate
(Cho/NAA) on the multi-voxel MRS (Figure 2C).
Presurgical planning was made following tractography of
the pyramidal tracts (Figure 3C) and mapping of the
motor cortex (Figure 2D) by fMRI. We performed an
awake craniotomy and revealed the hand and mouth areas
by brain mapping (Figure 4). The first iMRI scan showed
a small amount of residual deep tumor (Figure 3D, 3E).
Further resection was followed by updated
neuronavigation. Final iMRI suggested GTR (Figure 3G,
Figure 2. Preoperative series of MRI sequences for
patient-specific surgical planning in the illustrative case.
2A and 2B: Lesion in the right frontal lobe. LGG was
diagnosed according to the increased ratio of Cho/NAA
(2C). Motor cortex was indicated on BOLD fMRI
activation (orange spots in 2D).
Figure 3. Pre- (3A–3C), intra- (3D–3F), and
postoperative (3G–3I) series of the illustrative case. First
intraoperative MRI indicated a small amount of residual
tumor beneath the surgical cavity (3D, 3E). GTR was achieved after further resection (3G, 3H) and pyramidal tracts were protected (3I).
Chinese Medical Journal 2012;125():
5
clinical practice suggests that these advantages are most
prominent in glioma craniotomy, pituitary tumor
resection, and biopsies. More than one-third glioma cases
and more than one-fifth pituitary adenoma cases acquired
further resection under updated neuronavigation. The use
of 3 T iMRI benefits the patients by improving overall
GTR rates, while preserving the eloquent areas of the
brain.
Figure 4. Intraoperative braining mapping (A) was performed to
locate the hand area (label H) and mouth area (label M) of the
motor cortex, which were protected after tumor removal (B).
3H) without any injury to the motor cortex or pathway
(Figure 3I). Histopathology confirmed an astrocytoma.
No motor deficit was observed in this patient at 3 months
postoperatively.
DISCUSSION
High-field MRI is the priority for image-guided
neurosurgery due to its high resolution in brain imaging,
precise temporal and spatial resolution, random flat 3D
imaging, flow and temperature sensitivity, functional
brain imaging, nonionizing radiation, and other
advantages. The first iMRI system, based on a 0.5 T
magnet, was introduced 15 years ago at Brigham and
Women’s Hospital, Boston, USA.3
The following decade has witnessed enormous
developments in MRI equipment and technology.6,7 Gone
are the days when surgical beds had to be brought into an
MRI suite, and MRI equipment and operating room have
evolved into a single unit. The ability to image the brain
during surgery has become a reality. Our institute started
utilizing the 0.15 T PoleStar ™ N20 in 2006, which has
good mobility and easy installation. However, suboptimal
image quality, longer scanning times, and lack of
functional applications are the limitations of this device.8
High-field iMRI brings real-time diagnostic quality
imaging, and such functional applications as MR
spectroscopy, fMRI and DTI may be carried out during
surgery.9,10 This has brought substantial improvement to
microsurgical and minimally invasive neurosurgery. In
this study, all cases benefited from real-time diagnostic
quality imaging and most of them benefited from
functional applications.
iMRI has the following advantages: (1) real-time
diagnostic quality imaging, correcting the dynamic brain
shift and improving the overall accuracy of surgery; (2)
improving GTR rates while preserving vital
neurovascular structures and eloquent areas; and (3)
giving accurate real-time guidance for biopsies and
implantations, minimizing surgical damage.6,10 Our initial
Pioneering efforts in high-field iMRI have brought
revolutionary
changes
to
minimally
invasive
neurosurgery. An increasing number of studies11,12 have
demonstrated that the extent of resection is a predictor of
survival for glioma patients despite a lack of class I
evidence. Some studies have even shown that supratotal
resection might improve the outcome of LGGs.13,14
However, extensive resection may carry the risk of
neurological morbidity, which affects the quality of life
and subsequent overall survival.15 The evidence-based
grade for recommendation of the clinical efficiency of
iMRI for glioma resection still stands at level II.7,11 We
are now performing a randomized controlled trial for
investigating the application of iMRI in patients with
glioma, which were registered at clinicaltrials.gov. This
randomized controlled study, instead of the present study,
will help us answer the following questions. What are the
indications for iMRI operation? What is the efficacy of
iMRI operation? Does iMRI operation have a higher
incidence rate of unplanned second operations?
Our preliminary results suggest that iMRI benefits both
the patient and the surgeon. The utilization of iMRI
dramatically decreases surgical morbidity, especially in
those who have a lesion adjacent to eloquent areas.
Dynamic tissue shifting occurs during the course of the
operation and neuronavigation alone decreases the safety
and accuracy of surgery. Radical resection may even
cause late severe deficits, forcing many neurosurgeons to
take a more conservative approach in order to preserve
function, which may result in more residual tumor than
anticipated. We also observed an increase in early speech
and/or motor deficit rates, but both decreased during 3
months follow-up after surgery. This may be a result of a
more radical surgical approach than previous
conventional craniotomy, causing more edema in the
eloquent areas adjacent to the resected lesions. There is
no damage to the eloquent cortex or subcortical tracts
themselves, thus, the function could be better preserved
than with conventional craniotomy, and most patients
motor and verbal abilities improve to preoperative
baseline levels. We believe that 3 T iMRI provides
neurosurgeons with dynamic functional and anatomical
maps of brain structures, which improves the overall
accuracy and safety of surgery, and helps decrease
permanent surgical morbidity. At the same time, the fact
that iMRI increases both the cost and length of surgical
treatment should also be taken into account. We advocate
further research and investigation in understanding the
implications of iMRI on surgery and patient outcome, and
Chin Med J 2012;125():
6
potential trials in integrating iMRI with additional
technologies such as endoscopic and robotic surgical
devices in the near future.
8.
Acknowledgments: The authors would like to thank all the nurses
in the operating rooms and wards for their co-operation during data
collection; SHI Jian-bing and YANG Zhong for management and
collection of the image database; XU Gen for volumetric
measurement, WANG Zhen-xiao; and WANG Yan for the input of
clinical information.
9.
10.
REFERENCES
11.
1.
2.
3.
4.
5.
6.
7.
Samii M, Brinker T, Samii A. Image-guided
neurosurgery--state of the art and outlook. Wien Klin
Wochenschr 1999; 111: 618-628.
Galloway RL Jr, Maciunas RJ, Edwards CA 2nd. Interactive
image-guided neurosurgery. IEEE Trans Biomed Eng 1992;
39: 1226-1231.
Black PM, Moriarty T, Alexander E 3rd, Stieg P, Woodard EJ,
Gleason PL, et al. Development and implementation of
intraoperative magnetic resonance imaging and its
neurosurgical applications. Neurosurgery 1997; 41: 831-842;
discussion 842-835.
Chen X, Xu BN, Meng X, Zhang J, Yu X, Zhou D.
Dual-room 1.5-T intraoperative magnetic resonance imaging
suite with a movable magnet: implementation and
preliminary experience. Neurosurg Rev 2012; 35: 95-109;
discussion 109-110.
Wang Y. Relations between the sides of linguistic cerebral
dominance and manuality in Chinese aphasics. Chin Med J
1996; 109: 572-575.
Lang MJ, Greer AD, Sutherland GR. Intra-operative MRI at
3.0 Tesla: a moveable magnet. Acta Neurochir Suppl 2011;
109: 151-156.
Kubben PL, ter Meulen KJ, Schijns OE, ter Laak-Poort MP,
12.
13.
14.
15.
van Overbeeke JJ, van Santbrink H. Intraoperative
MRI-guided resection of glioblastoma multiforme: a
systematic review. Lancet Oncol 2011; 12: 1062-1070.
Acevedo CV, Vinas FC, Dujovny M. Intraoperative use of
magnetic resonance imaging: neurosurgical applications and
technical limitations. Crit Rev Neurosurg 1999; 9: 279-286.
Zhao Y, Chen X, Wang F, Sun G, Wang Y, Song Z, et al.
Integration of diffusion tensor-based arcuate fasciculus fibre
navigation and intraoperative MRI into glioma surgery. J Clin
Neurosci 2012; 19: 255-261.
Pamir MN. 3 T ioMRI: the Istanbul experience. Acta
Neurochir Suppl 2011; 109: 131-137.
Kuhnt D, Becker A, Ganslandt O, Bauer M, Buchfelder M,
Nimsky C. Correlation of the extent of tumor volume
resection and patient survival in surgery of glioblastoma
multiforme with high-field intraoperative MRI guidance.
Neuro Oncol 2011; 13: 1339-1348.
Sanai N, Berger MS. Operative techniques for gliomas and
the value of extent of resection. Neurotherapeutics 2009; 6:
478-486.
Duffau H. Awake surgery for incidental WHO grade II
gliomas involving eloquent areas. Acta Neurochir (Wien)
2012; 154: 575-584; discussion 584.
Yordanova YN, Moritz-Gasser S, Duffau H. Awake surgery
for WHO Grade II gliomas within "noneloquent" areas in the
left dominant hemisphere: toward a "supratotal" resection.
Clinical article. J Neurosurg 2011; 115: 232-239.
McGirt MJ, Mukherjee D, Chaichana KL, Than KD,
Weingart JD, Quinones-Hinojosa A. Association of surgically
acquired motor and language deficits on overall survival after
resection of glioblastoma multiforme. Neurosurgery 2009;
65: 463-469; discussion 469-470.
(Received August 14, 2012)
Edited by JI Yuan-yuan