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Chinese Medical Journal 2012;125():
1
Review article
Neuronavigation surgery in China: reality and prospects
WU Jin-song, LU Jun-feng, GONG Xiu, MAO Ying and ZHOU Liang-fu
Keywords: neurosurgery; neuronavigation; medical image
Objective To review the history, development, and reality of neuronavigation surgery in China and to discuss the future
of neuronavigation surgery.
Data sources PubMed, the China Knowledge Resource Integrated Database, and the VIP Database for Chinese
Technical Periodicals were searched for papers published from 1995 to the present with the key words “neuronavigation,”
“functional navigation,” “image-guided,” and “stereotaxy.” Articles were reviewed for additional ÏÔʾ×ÀÃæ.scf citations,
and some information was gathered from Web searches.
Study selection Articles related to neuronavigation surgery in China were selected, with special attention to application
to brain tumors.
Results Since the introduction of neurosurgical navigation to China in 1997, this core technique in minimally invasive
neurosurgery has seen rapid development. This development has ranged from brain structural localization to functional
brain mapping, from static digital models of the brain to dynamic brain-shift compensation models, and from preoperative
image-guided surgery to intraoperative real-time image-guided surgery, and from application of imported equipment and
technology to use of equipment and technology that possess Chinese independent intellectual property rights.
Conclusions The development and application of neuronavigation techniques have made neurological surgeries in
China more safe, precise and effective, and less invasive, and promoted the quality of Chinese neurosurgical practice to
the rank of the most advance and excellence in the world.
Chin Med J 2012;125():
D
erived from the Latin term navigare or navigat, the
term “navigation” refers to the process of
monitoring and controlling the space-temporal movement
of a craft or vehicle. Advanced navigation systems are
now widely used in the military, spaceflight, aviation,
seafaring, and positioning for land transportation and
medicine.1,2
HISTORY AND DEVELOPMENT OF
NEURONAVIGATION
The brain is the most complex and important part of the
human body. The key challenge facing neurosurgeons is
to accurately localize and resect lesions from intricate
brain while minimizing injury to the normal tissues.
Throughout its evolutionary history, operative
neurosurgical technique has developed from primary to
advanced
levels,
from
single-function
toward
multi-function, and from localization of brain surface
structures (early neurosurgery) to frame-based stereotaxy
and microsurgery (modern neurosurgery), frameless
stereotaxy and intraoperative imaging neuronavigation
surgery (minimally invasive neurosurgery).
Localization of brain surface structures
Archaeologists have discovered unusual holes on some
excavated human skulls of the Neolithic period
(7000–3000 BC). Modern X-ray has proven that such
holes were not caused by trauma or natural weathering,
but by human tools, indicating that our early ancestors
acquired the skill of cutting holes into the skull, the
simplest craniotomy. This practice of trepanation was also
described in the Chinese Inner Canon of the Yellow
Emperor and in an ancient Egyptian document known as
the Ebers Papyrus, written in 2600 BC. The great ancient
Greek doctor, poet, and philosopher Hippocrates
(460–370 BC) reported some brain and spinal cord
surgical cases. Hua-t’o (145–208 AD), a Chinese
physician highly skilled in surgery, also mastered the
operation of opening the skull.
During the 14th to 17th centuries in Europe, surgeons
from the missionary or the barber were in charge of both
trauma and general surgeries. Some performed simple
craniotomies for patients with brain trauma. Although
early surgeons opened the skull only according to the site
of force, they did manage to make some major brain
discoveries. Broca (1824–1880) is famous for his
discovery of the speech production center of the brain,
DOI: 10.3760/cma.j.issn.0366-6999.2012.01.001
Glioma Surgery Division, Department of Neurosurgery, Huashan
Hospital, Fudan University, Shanghai 200040, China (Wu JS, Mao
Y and Zhou LF)
Shanghai Medical College, Fudan University, Shanghai 200040,
China (Lu JF and Gong X)
Correspondence to: Dr. ZHOU Liang-fu, Glioma Surgery Division,
Department of Neurosurgery, Huashan Hospital, Fudan University,
Shanghai 200040, China ((Tel: 86-21-52888771. Fax:
86-21-52888771. Email: [email protected])
WU Jin-song and LU Jun-feng contributed equally to this work.
This study was supported by grants of the Ministry of Health of
China (2010-2012), National Natural Science Foundation of China
(No. 81071117), and Shanghai Municipal Health Bureau (No.
XBR2011022).
Conflicts of interest: none.
2
which was typically referred to as the pars triangularis
(Brodmann area 45) and pars opercularis (Brodmann area
44) of the inferior frontal gyrus (i.e., Broca’s area). Sir
Victor Horseley (1857–1916) also demonstrated the
relationship between the brain gyrus and the skull.
Because of localization inaccuracy, poor surgical lighting,
simple surgical instruments, and other factors, a longer
scalp incision and larger cortical exposure were necessary
for early brain surgery. The inability to locate deep brain
structures made operations of the brain parenchyma very
difficult.
Frame-based stereotactic surgery: localization of deep
brain structures
Frame-based stereotactic surgery was used to locate
targets in the brain with the help of a three-dimensional
(3D) coordinate system based on X-ray, computed
tomography (CT), or magnetic resonance imaging (MRI)
data and marked on a metal frame, which was fixed to the
head. In 1908, Horsley and Clarke created a stereotactic
frame for animal experiments. In 1947, the American
doctors Spiegel and Wycis invented the first framed
stereotactic instrument based on the data of
ventriculography and performed the first stereotactic
damage technique for mental disease. Thereafter, the
Leksell, Reichert, and other frame-based stereotactic
instruments emerged. In 1964, JIANG Da-jie, a Chinese
pioneer in severe traumatic brain injury treatment and
surgery for cranial-base tumors, developed China’s first
stereotactic instrument, which was used on patients for
two decades.
Early frame-based stereotactic surgery was performed
with
the
help
of
ventriculography,
pneumoencephalography, or X-ray; thus, it had
shortcomings of both localization inaccuracy and
invasion. In the 1960s and 1970s, the wide application of
CT and MRI technologies rejuvenated frame-based
stereotactic surgery by improving its accuracy and safety.
However, its application was limited by the following
shortcomings, which proved difficult to overcome: (1) it
is cumbersome, uncomfortable, and inflexible; (2) its
localization and orientation are not in real time and are
not intuitive; (3) the calculation method is complex; (4) it
is unsuitable for children or patients with thin skulls; and
(5) because of its impact on endotracheal intubation, the
frame must be worn after intubation in the case of general
anesthesia, which increases the anesthesia and surgery
time and prevents realization of a preoperative functional
MRI. Therefore, frame-based stereotactic surgery is
mainly used for the treatment of extrapyramidal
disorders, such as Parkinson’s disease, intractable pain,
mental illness, epilepsy, foreign body removal, biopsy,
and deep electrode placement.
Frameless stereotactic surgery: localization of the
whole brain and spine
Frameless stereotactic surgery is also known as
image-guided surgery or neuronavigation surgery. In the
Chin Med J 2012;125():
late 1980s, frameless stereotaxy was developed based on
the following technologies: (1) high-resolution, 3D
neuroimaging technologies, such as CT and MRI; (2) 3D
digital converters, which are able to accurately transmit
the image information to computers; and (3)
high-performance and high-capacity computers or
workstations, which ensure the processing of large
amounts of information effectively. In 1997, Chinese
hospitals in Shanghai, Beijing, Guangzhou, and Tianjin
have respectively introduced neuronavigation equipment
to clinical practice and research. Recently, China-based
neuronavigation equipment has been put into production
in Shanghai and Shenzhen. For example, the Fudan
dig-medical neuronavigation developed by the Digital
Medical Research Center of Fudan University and
Huashan Hospital has been approved for sale on the
market.3
Compared with frame-based stereotaxy, frameless
stereotaxy has the following advantages: (1) it can be
used for preoperative planning; (2) the real-time 3D
relationship between lesions and eloquent areas can be
visualized intraoperatively; (3) structures in the surgical
field are displayed on the navigation; (4) 3D spatial
relationships between the current position and residual
lesions are estimated; (5) intraoperative real-time
adjustment of the surgical strategy is possible; (6)
structures that may be encountered along the approach are
shown; (7) crucial structures are shown; and (8) the
extent of resection is shown. This frameless system has
greatly expanded surgical indications, including those for
various intracranial lesions such as brain tumors, cysts
and abscesses, hematomas, vascular malformations, dural
arteriovenous fistulas, skull-base tumors, epilepsy,
congenital or acquired deformities, paranasal sinuses, and
spine lesions.4-10
Frameless neuronavigation has now become a critical part
of minimally invasive neurosurgery. Such technology
contributes powerfully to microneurosurgery, keyhole
surgery, endoscopic neurosurgery, and skull-base surgery.
Frameless navigation is also used in other medical
disciplines, such as maxillofacial surgery, otolaryngology,
orthopedic surgery, radiosurgery, and conventional
radiation therapy. The latter has been developed for use in
conformal radiotherapy and 3D intensity-modulated
radiation therapy by the application of navigation and
localization technology.
FUNCTIONAL NEURONAVIGATION
Compared with conventional neuronavigation, functional
neuronavigation allows the combination of anatomic
imaging, which reveals the presence of tumors, and
functional imaging, which shows the eloquent cortex and
subcortical fibers based on multi-image fusion
technology. It therefore contributes favorably to
achieving optimal surgical results; i.e., the maximal
extent of resection and minimal injury of critical
structures with the optimal functional outcome. The
Chinese Medical Journal 2012;125():
functional neuronavigation has been widely used in
protecting neurological functions, such as motor,
language, and vision.
Functional brain imaging
The cerebral cortex comprises many functional areas that
control movement, sensation, language, vision, and so on.
The functional areas were previously localized based on
their approximate anatomical location, which is
inaccurate and vulnerable to interference by various
factors because their appearances are similar to other
areas of the cortex in terms of appearance. Until 1990,
Ogawa et al11 first proposed the blood oxygen
level-dependent (BOLD) technique, which could display
the eloquent areas such as the motor cortex (the primary
motor areas, premotor area, and supplementary motor
area), somatosensory cortex, language cortex, and visual
areas. This specialized technique is used to measure the
hemodynamic response (change in blood flow) related to
neural activity in human or animal brains.
Between the functional areas and dominant target organs
or among brain areas, there are different connective
pathways that send or receive a variety of important
information to ensure the implementation of various brain
functions. These dense, delicate fibers located within
subcortical white matter are difficult to distinguish and
are vulnerable to damage during surgery. Basser et al12
and Pierpaoli et al13 first reported a fiber imaging
technology (i.e., diffusion tensor imaging (DTI)) in 1996,
opening the door to subcortical fiber tractography on
MRI. During the past decade, a variety of subcortical
pathways have been applied in functional navigation
(such as pyramidal tract, arcuate fasciculus, and optic
radiation).
Proposition of functional neuronavigation surgery
Resection of lesions within or adjacent to eloquent areas
(such as tumors, arteriovenous malformations, and
cavernoma) often damage functional cortex and/or
subcortical
tracts,
resulting
in
postoperative
complications such as paralysis, aphasia, alexia, or visual
field defects. Therefore, the balance between maximizing
lesion removal while minimizing functional damage has
been a common challenge. Based on experimental and
clinical studies, the new concept of functional
neuronavigation surgery was proposed and verified in our
center in 2003.14-17 The primary principles are as follows:
(1) the datasets of multiple images (including structural
MRI and functional images such as BOLD and DTI) are
acquired, (2) accurate image fusion of structural and
functional images is conducted through multi-modal
medical image fusion technology based on rigid
registration, and (3) the fused images are integrated with
neuronavigation to guide the process of brain surgery,
increasing the rate of lesion removal and avoiding
neurological deficits.
Clinical application of functional neuronavigation
The most common central nervous system tumors are
3
gliomas, accounting for approximately 28.9% of 55 889
cases of brain tumors and 76.4% of 18 151 cases of
malignant brain tumors treated in Shanghai Huashan
Hospital from 1951 to 2010. Less than 60% of these cases
achieve image-verified complete resection despite the
continuing progression of surgical technology. This is
because there is no grossly distinguishable boundary
between the tumor and normal brain tissue. It is
particularly difficult to achieve “complete resection of the
tumor with maximum preservation of brain function,”
especially for tumors within eloquent areas. Considering
individual differences and the reorganization and
plasticity caused by disease, location of the distribution of
cortical function using traditional anatomical landmarks
has been unreliable. The BOLD technique, because of its
advantages aforementioned, is widely used in
preoperative brain function localization, intraoperative
navigation, and postoperative assessment of brain
function. Lehericy et al18 and Wu et al15 compared BOLD
localization and the “gold standard” of intraoperative
direct electrical stimulation of the motor cortex with
highly consistent results. Studies by Rutten et al19 and
Lang et al20 also showed substantial consistency between
these two approaches in localization of the language
cortex.
Similarly, the combination of DTI images with MRI
structural images can clearly show the relationship
between lesions and neurological pathways. It took 5
years for Huashan Hospital to complete large-scale
prospective randomized controlled trials (n=238) of
functional neuronavigation surgical treatment of glioma
localization in the motor area and to show, using
evidence-based medicine, that the new technologies can
(1) increase the total gross resection rate of glioma in
eloquent areas from 51.7% to 72.0% (nearly the cut rate
of non-functional areas), (2) reduce postoperative
morbidity from 32.8% to 15.3%, and (3) increase the
long-term Karnofsky Performance Scale score of patients
from 74 to 86. The study also confirmed significant
independent survival advantages of functional
neuronavigation.
Compared
with
conventional
neuronavigation surgery, this new technology reduces the
risk of death after surgery by 43.0% in patients with
malignant glioma (WHO grades III–IV) in functional
areas.14
BRAIN SHIFT IN NEURONAVIGATION SURGERY
One of the major technical challenges in conventional
neuronavigation with preoperative imaging data is brain
shift. Because brain tissue is non-rigid, brain deformation
(i.e., brain shift or drift) inevitably appears during surgery
because of tissue biomechanical properties, gravity,
changes in intracranial pressure, cerebrospinal fluid loss,
operative manipulation, and anesthesia. A review of 1000
neuronavigation surgical cases seen at our department21
revealed that during surgeries, a dura shift of (2.80±2.48)
mm, a cerebral cortex shift of (5.14±4.05) mm, and a
tumor shift of (3.53±3.67) mm occurred. These values
4
were especially high in surgeries involving the cerebral
hemispheres. Brain shift reduces the localization accuracy
of preoperative imaging navigation, resulting in reduced
surgical accuracy and safety, an increased potential for
residual tumor formation after surgery, and a higher risk
of damage to normal neurovascular structures. Therefore,
how to compensate for brain shift has become a popular
issue.22,23 There are three general solutions to this issue:
(1) micro-catheter localization technology, (2)
computational model-updated imaging, and (3)
intraoperative imaging.
Micro-catheter localization technology
In micro-catheter localization technology,21 the targets at
the surface or periphery of the cerebrum show more shift
than do the targets that are deep-seated or located in the
center of the brain. For resection of multiple cavernomas,
a
1.5-mm-diameter
micro-catheter,
guided
by
neuronavigation, is inserted into deep-seated lesions
before dural opening. After resection of the superficial
cavernoma, brain shift occurs, but the micro-catheter
concomitantly shifts. Therefore, it is not difficult to reset
the shifted cavernoma along the micro-catheter. We
believe that this technique is useful, practical, and
economical.6
Computational model-updated imaging
Computational model-updated imaging is based on
non-rigid registration of brain images using a physical or
mathematic model with compensation of 70% to 80%.24,25
Precision and reliability of the technique,24 however, are
imperfect, and it is practically impossible to accurately
model all complex phenomena that intraoperatively
impact brain shift. One solution is to use additional
intraoperative imaging (ultrasound, MRI, or CT) to drive
the computational model, matching any preoperative
data.26-29 The potential benefit of the technique is less
interruption of the surgical technique for image
acquisition.
Intraoperative imaging
Current intraoperative imaging models include
radiography, X-ray fluoroscopy, ultrasonography, CT, and
MRI. The first imaging techniques used in neurosurgery
was CT and ultrasound, reported respectively by Shalit
(1979) and Rubin (1980). Recent improvements permit
CT of good resolution, especially for bones, but not yet
for soft tissue. Nevertheless, intraoperative CT will not
represent the leading direction for development of
image-guided technology because of the radiation burden
to patients. Recently, the rapid development of
intraoperative ultrasound technology has allowed 2D and
3D imaging, but its resolution still cannot match that of
CT or MRI; its penetration is inversely proportional to
resolution. Therefore, the disadvantages of intraoperative
CT and ultrasound have limited their application.
Intraoperative MRI (iMRI) is currently the main
technique with which to compensate for brain
deformation.30-35
Chin Med J 2012;125():
INTRAOPERATIVE MRI AND
NEURONAVIGATION
iMRI navigation
iMRI navigation requires preoperative, intraoperative,
and postoperative MRI scanning, image acquisition, and
processing. The earliest report on its application came
from Dr. E. Alexander III (1996).36 For more than 10
years, iMRI equipment and technology have been
developed in three stages. The first two stages involved
moving the operating room into the MRI room. The third
stage employs design innovation of the scanning and
magnets, enabling establishment of a true MRI system in
the operating room. For example, the Medtronic PoleStar
N20 0.15-T MRI, with vertical dual-plane magnets and
low field strength, is mobile and flexible enough to be
placed in conventional neurosurgical operating rooms. A
digital integrated neurosurgical center devoted to iMRI
has also been built. Now, 1.5- and 3.0-T iMRI have been
installed and run in People’s Liberation Army General
Hospital Beijing34,37 and Huashan Hospital Shanghai,38,39
respectively. Since 2006, the Huashan Hospital has
performed nearly 1000 surgeries with good results using
both 0.15- and 3.0-T iMRI.
iMRI navigation has been widely used in neurosurgery,
particularly for gliomas,32,33,40-47 pituitary tumors,48
functional neurosurgery,31 and needle biopsy.49 iMRI has
the following advantages: it (1) provides real-time
structural and functional images for neuronavigation to
correct errors caused by brain tissue deformation and
brain shift, (2) improves the extent of resection and
avoids significant structural and functional damage, (3)
provides real-time guidance and precise localization for
stereotactic needle biopsy and surgical implants, and (4)
allows for monitoring of early complications, such as
cerebral ischemia and hemorrhage during surgery.
Comparison between different MRI magnets’ fields in
neurosurgery
In terms of field strength, the MRI magnet’s field can be
categorized as low-field (<0.5 T), middle-field (0.5–1.0
T), high-field (1.0–1.5 T), and ultra-high-field (>2.0 T).
High-field iMRI
As the signal-to-noise ratio (SNR) decreases with the
low-field strength, the Maxwell term increases, and vice
versa. Therefore, the overall image quality of high-field
iMRI is better than that of low-field iMRI. The former
also has the following advantages: (1) the acquisition
time can be shortened by increasing the magnet field
strength in the same SNR, (2) quantitative chemical
analysis of metabolites based on chemical-shift
information can be performed by magnetic resonance
spectroscopy (MRS), (3) enhanced susceptibility effects
allow functional brain imaging (fMRI) of BOLD and
DTI, and (4) a high gradient field and switching rate
ensure the quality of angiography (magnetic resonance
angiography (MRA) and magnetic resonance venography
Chinese Medical Journal 2012;125():
(MRV)), diffusion-weighted imaging, DTI, and perfusion
imaging. Therefore, high-field iMRI has obvious
advantages in the structural and functional imaging of the
central nervous system despite its shortcomings, which
include high cost, increased noise, accumulation of radio
frequency pulse energy in the body, and metal artifacts.
Low-field iMRI
Compared with high-field iMRI, low-field iMRI has the
following advantages: (1) less accumulation of radio
frequency pulse energy in the body, (2) less ECG-gated
signal distortion, and (3) increased comfort and safety.
With the help of high-performance gradient systems, RF
systems, and computer systems, low-field iMRI is now
capable of producing brain structural images comparable
with those of high-field iMRI. Furthermore, it is
relatively low-cost, small in size, and easy to operate and
promote in a certain range.
However, low-field iMRI cannot acquire functional brain
imaging, vascular imaging, or quantitative analysis of
tissue metabolites. To address functional neuronavigation
using PoleStar N20 (0.15-T), we successfully integrated
the preoperative functional images, fMRI, BOLD, and
DTI obtained from a 3.0-T MRI system and the
intraoperative structural images obtained from the
PoleStar N20 using a thin-plate spline model, thus
realizing functional neuronavigation surgery in low-field
iMRI. Further confirmation using 3.0-T iMRI is
underway.
In summary, high-field iMRI not only opened up a new
world for neuronavigation because of its efficient
real-time imaging, high spatial and temporal resolution,
and imaging of brain function and metabolism, but also
inspired people to look for more technological advances.
FUTURE OF NEURONAVIGATION
Man and tool
During its 10 years of development, neuronavigation has
made great strides in terms of equipment and techniques.
Neuronavigation-related technologies have been broadly
applied in China. Today, there are more than 150
neuronavigation systems and 7 iMRIs in China since their
introduction in 1997.
Although the application of advanced neuronavigation
systems will undoubtedly promote the development of
minimally invasive neurosurgery and better patient
service, we must be fully aware that such systems still
require manual operation. Thus, the operator’s
intelligence and three fundamental skills (basic theory,
knowledge, and technique (especially microsurgical
technique)) are critical for successful neuronavigation.
Future trends
Further development of hardware and software will make
navigation systems more convenient, highly automated,
5
and intelligent, with automatic registration and bias
correction.
(1) A rapid processing system and high-performance
personal computer can potentially replace the current
workstation, making much smaller and cheaper portable
navigation systems possible.
(2) A high-resolution 3D monitor screen will be
conducive to the 3D display of complex, deep-brain
structures.
(3) A touch control panel will enable neurosurgeons to
directly manipulate the console, eliminating the need for
a technician’s help.
(4) Multiple-image fusion (e.g., CT, MRI, Ultrasound,
fMRI, DTI, MRA, MRV, MRS, PET, and CTA) will
provide multimodal neuronavigation with those
advantages already mentioned in this paper.
(5) Virtual Reality technology will allow neurosurgeons
to preoperatively demonstrate each of the steps and
possible surgical problems and treatment strategies,
making navigation safer and more individualized and
effective.50-53 Meanwhile, this technology benefits the
training of young neurosurgeons as well as the
preparation and review for complex surgery required for
experienced neurosurgeons.
(6) Automatic compensation of brain shift is expected to
increase the accuracy and safety of surgical navigation
through the development of universal compensation
software.
(7) iMRI hardware will be optimized. The modified
equipment with higher resolution will obtain high-quality
real-time images and make more space for surgical
procedures which could acquire images during the
operation
without
interruption.
Special
image
anti-jamming technology will obtain images free from
interference by external factors.
(8) Robots and mechanical arms have recently been
applied to manipulate the surgical microscope, burr,
traction control, electrode, and endoscope without being
influenced by tremors, shaking, or the surgeon’s
emotions. In the near future, robots will likely become
widespread to neurosurgical treatment. Telesurgery,
surgery performed by a robot under the control of a
surgeon, will become a reality.
REFERENCES
1.
2.
Alexander E, 3rd, R M. Advanced Neurosurgical Navigation.
In: Advanced Neurosurgical Navigation. New York: Thieme
Medical Publishers; 1999: 3-14.
Zhou LF. Modern Neurosurgery Shanghai: Fudan University
Press; 2001.
Chin Med J 2012;125():
6
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
Jin Y, Wu JS, Chen XC, Zhao F. Experimental study of
domestic Excelim-04TM neuronavigation system. Fudan
Univ J Med Sci (Chin) 2007; 34: 741-743.
Cao GB, Lu YJ, Zhu JK, Shu JH, Yang H, Wang JG, et al.
Clinical Use of Neuronavigator-Assisted Microsurgery for
Intracranial Diseases. Chin J Clin Neurosurg (Chin) 2005; 10:
182-184.
Che XM, Gu SX, Yang F, Shi W, Shi JB, Wu JS, et al.
Vertebral bone fixation with the help of neuronavigation.
Chin J Nerv Ment (Chin) 2007; 33: 136-138.
Du G, Zhou L. Neuronavigation for the resection of
cavernous angiomas. Chin Med J 1999; 112: 725-727.
Du GH, Zhou LF. Preliminary Application of
Neuronavigation System in Neurosurgery. Chin J Clin
Neurosci (Chin) 1998; 6: 94-97.
Du GH, Zhou LF, Mao Y. Application of neuronavigation in
glioma surgery. Chin J Surg (Chin) 2003; 41: 238-239.
Jia PF, Wu JS, Li SQ. Neuronavigator-guided transsphenoidal
removal of invasive sellar tumors. Chin J Microsurg 2004;
27: 258-259.
Sha L, Li G, Li XG, Xu SJ, Jia DZ, Jiang YQ, et al.
Application of neuronavigation in the biopsy procedures of
intracranial lesions. Chin J Min Inv Neurosurg (Chin) 2005;
10: 251-253.
Ogawa S, Lee TM, Kay AR, Tank DW. Brain magnetic
resonance imaging with contrast dependent on blood
oxygenation. Proc Natl Acad Sci U S A 1990; 87: 9868-9872.
Basser PJ, Pierpaoli C. Microstructural and physiological
features of tissues elucidated by quantitative-diffusion-tensor
MRI. J Magn Reson B 1996; 111: 209-219.
Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G.
Diffusion tensor MR imaging of the human brain. Radiology
1996; 201: 637-648.
Wu JS, Mao Y, Zhou LF, Tang WJ, Hu J, Song YY, et al.
Clinical evaluation and follow-up outcome of diffusion tensor
IMAGING-BASED
functional
neuronavigation:
A
prospective, controlled study in patients with gliomas
involving pyramidal tracts. Neurosurgery 2007; 61: 935-948.
Wu JS, Zhou LF, Chen W, Lang LQ, Liang WM, Gao GJ, et
al. Prospective comparison of functional magnetic resonance
imaging and intraoperative motor evoked potential
monitoring for cortical mapping of primary motor areas. Chin
J Surg (Chin) 2005; 43: 1141-1145.
Wu JS, Zhou LF, Gao GJ, Hong XN, Mao Y, Du GH.
Application of
multi-image-merged
techniques
in
neuronavigation surgery. Chin J Neurosurg (Chin) 2005; 21:
227-231.
Wu JS, Zhou LF, Hong XN, Mao Y, Du GH. Role of
diffusion tensor imaging in neuronavigation surgery of brain
tumors involving pyramidal tracts. Chin J Surg (Chin) 2003;
41: 662-666.
Lehericy S, Duffau H, Cornu P, Capelle L, Pidoux B,
Carpentier A, et al. Correspondence between functional
magnetic resonance imaging somatotopy and individual brain
anatomy of the central region: comparison with intraoperative
stimulation in patients with brain tumors. J Neurosurg 2000;
92: 589-598.
Rutten GJ, Ramsey NF, van Rijen PC, Noordmans HJ, van
Veelen CW. Development of a functional magnetic resonance
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
imaging protocol for intraoperative localization of critical
temporoparietal language areas. Ann Neurol 2002; 51:
350-360.
Lang LQ, Xu QW, Pan L, Chen ZA, Wu JS. BOLD-fMRI in
preoperative assessment of language areas: correlation with
direct cortical stimulation. Chin J Med Comput Imag (Chin)
2005; 11: 156-160.
Du GH, Zhou LF, Mao Y, Wu JS. Intraoperative brain shift in
neuronavigator-guided surgery. Chin J Min Inv Neurosurg
2002; 7: 65-68.
Dorward NL, Alberti O, Velani B, Gerritsen FA, Harkness
WF, Kitchen ND, et al. Postimaging brain distortion:
magnitude, correlates, and impact on neuronavigation. J
Neurosurg 1998; 88: 656-662.
Hill DL, Maurer CR, Jr., Maciunas RJ, Barwise JA,
Fitzpatrick JM, Wang MY. Measurement of intraoperative
brain surface deformation under a craniotomy. Neurosurgery
1998; 43: 514-526; discussion 527-518.
Liu Y, Song Z. A robust brain deformation framework based
on a finite element model in IGNS. Int J Med Robot 2008; 4:
146-157.
Miga MI, Paulsen KD, Lemery JM, Eisner SD, Hartov A,
Kennedy FE, et al. Model-updated image guidance: initial
clinical experiences with gravity-induced brain deformation.
IEEE Trans Med Imaging 1999; 18: 866-874.
Keles GE, Lamborn KR, Berger MS. Coregistration accuracy
and detection of brain shift using intraoperative
sononavigation during resection of hemispheric tumors.
Neurosurgery 2003; 53: 556-562; discussion 562-554.
Nakao N, Nakai K, Itakura T. Updating of neuronavigation
based on images intraoperatively acquired with a mobile
computerized tomographic scanner: technical note. Minim
Invasive Neurosurg 2003; 46: 117-120.
Skrinjar O, Nabavi A, Duncan J. Model-driven brain shift
compensation. Med Image Anal 2002; 6: 361-373.
Zhuang DX, Liu YX, Wu JS, Yao CJ, Mao Y, Zhang CX, et
al. A sparse intraoperative data-driven biomechanical model
to compensate for brain shift during neuronavigation. AJNR
Am J Neuroradiol 2011; 32: 395-402.
Black PM, Alexander E, 3rd, Martin C, Moriarty T, Nabavi
A, Wong TZ, et al. Craniotomy for tumor treatment in an
intraoperative
magnetic
resonance
imaging
unit.
Neurosurgery 1999; 45: 423-431; discussion 431-423.
Buchfelder M, Ganslandt O, Fahlbusch R, Nimsky C.
Intraoperative magnetic resonance imaging in epilepsy
surgery. J Magn Reson Imaging 2000; 12: 547-555.
Nimsky C, Ganslandt O, Buchfelder M, Fahlbusch R. Glioma
surgery evaluated by intraoperative low-field magnetic
resonance imaging. Acta Neurochir Suppl 2003; 85: 55-63.
Nimsky C, Ganslandt O, Von Keller B, Romstock J,
Fahlbusch R. Intraoperative high-field-strength MR imaging:
implementation and experience in 200 patients. Radiology
2004; 233: 67-78.
Sun GC, Chen XL, Zhao Y, Wang F, Hou BK, Wang YB, et
al. Intraoperative high-field magnetic resonance imaging
combined with fiber tract neuronavigation-guided resection
of cerebral lesions involving optic radiation. Neurosurgery
2011; 69: 1070-1084; discussion 1084.
Zhou LF. Intraoperative MRI Neuronavigation: Current
Chinese Medical Journal 2012;125():
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
Status and Advances. Chin J Mini Inv Neurosurg (Chin)
2007; 12: 97-100.
Alexander E 3rd, Moriarty TM, Kikinis R, Jolesz FA.
Innovations in minimalism: intraoperative MRI. Clin
Neurosurg 1996; 43: 338-352.
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.
Lu JF, Zhang J, Wu JS, Yao CJ, Zhuang DX, Qiu TM, et al.
Awake craniotomy and intraoperative language cortical
mapping for eloquent cerebral glioma resection: preliminary
clinical practice in 3.0 T intraoperative magnetic resonance
imaging integrated surgical suite. Chin J Surg (Chin) 2011;
49: 693-698.
Wu JS, Zhu FP, Zhuang DX, Yao CJ, Qiu TM, Lu JF, et al.
Preliminary application of 3.0 T intraoperative magnetic
resonance imaging neuronavigation system in China. Chin J
Surg (Chin) 2011; 49: 683-687.
Bradley WG. Achieving gross total resection of brain tumors:
intraoperative MR imaging can make a big difference. AJNR
Am J Neuroradiol 2002; 23: 348-349.
Fountas KN, Kapsalaki EZ. Volumetric assessment of glioma
removal by intraoperative high-field magnetic resonance
imaging. Neurosurgery 2005; 56: E1166; author reply E1166.
Hadani M, Spiegelman R, Feldman Z, Berkenstadt H, Ram Z.
Novel, compact, intraoperative magnetic resonance
imaging-guided system for conventional neurosurgical
operating rooms. Neurosurgery 2001; 48: 799-807;
discussion 807-799.
Moriarty TM, Quinones-Hinojosa A, Larson PS, Alexander
E, 3rd, Gleason PL, Schwartz RB, et al. Frameless
stereotactic neurosurgery using intraoperative magnetic
resonance imaging: stereotactic brain biopsy. Neurosurgery
2000; 47: 1138-1145; discussion 1145-1136.
Muragaki Y, Iseki H, Maruyama T, Kawamata T, Yamane F,
Nakamura R, et al. Usefulness of intraoperative magnetic
resonance imaging for glioma surgery. Acta Neurochir Suppl
2006; 98: 67-75.
Schulder M, Carmel PW. Intraoperative magnetic resonance
7
46.
47.
48.
49.
50.
51.
52.
53.
imaging: impact on brain tumor surgery. Cancer Control
2003; 10: 115-124.
Wirtz CR, Knauth M, Staubert A, Bonsanto MM, Sartor K,
Kunze S, et al. Clinical evaluation and follow-up results for
intraoperative magnetic resonance imaging in neurosurgery.
Neurosurgery 2000; 46: 1112-1120; discussion 1120-1112.
Wu JS, Mao Y, Yao CJ, Zhuang DX, Zhou LF. Preleminary
application of intraoperative magnetic resonance imaging in
glioma surgery: experience with 61 cases. Chin J Min Inv
Neurosurg (Chin) 2007; 3: 105-109.
Wu JS, Shou XF, Yao CJ, Wang YF, Zhuang DX, Mao Y, et
al. Transsphenoidal pituitary macroadenomas resection
guided by PoleStar N20 low-field intraoperative magnetic
resonance imaging: comparison with early postoperative
high-field magnetic resonance imaging. Neurosurgery 2009;
65: 63-71.
Daniel BL, Birdwell RL, Butts K, Nowels KW, Ikeda DM,
Heiss SG, et al. Freehand iMRI-guided large-gauge core
needle biopsy: a new minimally invasive technique for
diagnosis of enhancing breast lesions. J Magn Reson Imaging
2001; 13: 896-902.
Qiu TM, Zhang Y, Wu JS, Tang WJ, Zhao Y, Pan ZG, et al.
Virtual reality presurgical planning for cerebral gliomas
adjacent to motor pathways in an integrated 3-D stereoscopic
visualization of structural MRI and DTI tractography. Acta
Neurochir (Wien) 2010; 152: 1847-1857.
Yang de L, Xu QW, Che XM, Wu JS, Sun B. Clinical
evaluation and follow-up outcome of presurgical plan by
Dextroscope: a prospective controlled study in patients with
skull base tumors. Surg Neurol 2009; 72: 682-689; discussion
689.
Zhang XL, Wu JS, Mao Y, Zhou LF, Li SQ, Wang YF.
Application of virtual reality technique in preoperative
planning of neurosurgery. Chin J Microsurg (Chin) 2006; 29:
415-418.
Zhang XL, Zhou LF, Mao Y, Wu JS. Preoperative planning of
cranial base tumor in virtual reality environment. Chin J Nerv
Ment Dis 2008; 34: 135-138.
(Received August 14, 2012)
Edited by JI Yuan-yuan