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Review article
a r t i c l e i n f o a b s t r a c t
Article history: Neurosurgeons are faced with the challenge of planning, performing, and learning complex surgical pro-
Received 28 November 2018 cedures. With improvements in computational power and advances in visual and haptic display tech-
Accepted 22 December 2018 nologies, augmented and virtual surgical environments can offer potential benefits for tests in a safe
and simulated setting, as well as improve management of real-life procedures. This systematic literature
review is conducted in order to investigate the roles of such advanced computing technology in neuro-
Keywords: surgery subspecialization of intracranial tumor removal. The study would focus on an in-depth discussion
Virtual reality
on the role of virtual reality and augmented reality in the management of intracranial tumors: the current
Mixed reality
Augmented reality
status, foreseeable challenges, and future developments.
Brain tumor Ó 2018 Elsevier Ltd. All rights reserved.
Intracranial tumor
Neurosurgery
https://doi.org/10.1016/j.jocn.2018.12.036
0967-5868/Ó 2018 Elsevier Ltd. All rights reserved.
C. Lee, G.K.C. Wong / Journal of Clinical Neuroscience 62 (2019) 14–20 15
Clinical application/surgical domain Device PICO (populations, intervention, comparison, outcome) – if applicable
Presurgical plan for skull base tumor Dextroscope [70] P 48 patients with skull base tumor divided into 2 groups,
I surgery with/without plan provided by Dextroscope
C Tumor’s resection rate, the preoperative evaluation: duration of operation,
total blood loss, the postoperative LOS, cerebrovascular injury,
complications, and postoperative KPS of patients on discharge/6mo follow-
up
O The duration of operation and the postoperative LOS of each patient were
5.25 ± 0.64 h and 8.50 ± 1.10 days in the test group and 7.36 ± 0.87 h and
12.50 ± 1.52 days in the control group (P < 0.05) KPS of patients in the test
group improved from discharge to the 6 month after (P < 0.05), there were
adverse results in the test group (P < 0.05)
VR in the planning of tumor Dextroscope [71] P – 60 patients with sellar region tumors
resection in the sellar region I – VR models of the tumor and simulation of different approaches to its
removal (transmononasal sphenoid sinus, pterional, and other)
C – survey questionnaire filled by 11 neurosurgeons
O – models were helpful for the individualized planning of surgery in the
sellar region
VR in presurgical planning for Dextroscope [72] P 45 patients with suspected glioma
cerebral gliomas and I – MRI (tractography, DTI, 3d) simulation
tractography C – amplitude of the number of effective fibers at affected sides, KPS at
6 months
O – optimization of surgical trajectory, maximization of safe tumor removal
VR simulator as an assessment of NeuroTouch [39] P 71 participants (10 medical students, 18 junior residents, and 44 senior
performance in brain tumor residents)
resection I – Participants completed the internal resection of a simulated convexity
meningioma
C – the volume of tissues removed, tool path lengths, duration of excessive
forces applied and efficient use of the aspirator
O – a significant increase in a tumor removed and efficiency of ultrasonic
aspirator use between medical students and residents
VR simulator as an assessment of NeuroTouch [73] P – 18 (6 neurosurgeons, 6 senior residents, 6 junior residents)
bimanual performance in brain I – Bimanual resection of 8 simulated brain tumors with differing color,
tumor resection stiffness, and border complexity
C – blood loss, tumor percentage resected, total simulated normal brain
volume removed, total tip path lengths, maximum and sum of forces used
by instruments, efficiency index, ultrasonic aspirator path length index,
coordination index, ultrasonic aspirator bimanual forces ratio
O – metrics differentiate novice from expert neurosurgical performance
VR simulator as assessment of force NeuroVR [54] P – 16 neurosurgeons, 15 residents, 84 medical students
application I – 18 cases on simulator
C – ultrasonic aspirator force application was continually assessed during
resection of simulated brain tumors
O – Handedness, ergonomics, and visual and haptic tumor characteristics
resulted in distinct well-defined 3D force pyramid patterns
AR/VR for functional Functional Neuronavigation [74] P 79 glioma patients and 55 control subjects.
neuronavigation I – Neuronavigation based on presurgical tractography or anatomical
landmarks
C – resection rate, the average extent of resection, the rate of preservation of
neural functions
O – the complete resection subjects, with average resection rates of
95.2% ± 8.5% and average extent of resection differed between the 2 groups
(P < 0.01)
Presurgical planning of feeder Virtual operation field (VOF) by high-spatial- P – 8 cases with cerebellopontine angle meningioma
resection resolution three-dimensional computer graphics I – (1) operation (2) presurgical simulation with VOF
(hs-3DCG) [75] C – the point at which main feeding artery penetrated meningioma
O – By using VOF, the point at which the main feeder penetrated the tumor
was estimated
AR system to assist novice surgeons AR goggles [76] Compared to conventional planning environments, the proposed system
greatly improves the non-clinicians’ performance, independent of the
sensorimotor tasks performed (p < 0.01). The time to perform clinically
relevant tasks is always reduced (p < 0.05).
VR system for training simulation Robotic Operative Microscope [67] Case study as an assessment of assessed robotic, exoscopic, endoscopic,
for a robotic surgery system fluorescence functionality.
VR systems as a base for Mathematical model [30] The velocity of expansion is linear with time and varies about 10-fold, from
mathematical modeling of about 4 mm/year for low-grade gliomas to about 3 mm/month for high-
glioma tumor growth grade ones.
AR system with back-facing camera Tablet-AR [77] The alignment errors in the skull specimen study were 4.6 pixels (1.6 mm)
and clinical experiment 6 pixels (2.1 mm).
AR system for neuronavigation AR system based on open-source software 3D The images were overlaid in all 3 cases with the AR error was 2–3 mm for
Slicer, Polaris and web cameras [78] meningioma cases
AR system for neuronavigation for Endoscopic AR navigation system [6] AR system superimposes 3-d virtual representations of the patient’s tumor
pituitary tumors and local anatomy, indicate position and direction of the endoscopic beam,
color changes of wire-frame images with the moving distance between
endoscope tip and tumor. A useful addition to the transsphenoidal surgery.
AR system for image-guided AR system [79] Technical note and visualization on the model skull with mean projection
neurosurgery error: 0.3 mm
C. Lee, G.K.C. Wong / Journal of Clinical Neuroscience 62 (2019) 14–20 17
ultrasound inserted into the microscopic beam during the opera- difference between learner specialties was observed for situation
tion, which enables the surgeon to focus the sight solely on the awareness, decision making, communications and teamwork, or
operating field [31]. leadership evaluations. Learners reported the simulation realistic,
Head-mounted devices such as smart glasses have been well beneficial, and highly instructive [36].
studied and their usage was proven in the field of neurosurgery: Urology is also the field with one of the earliest robotic surgery
for craniotomy, lumbar biopsy, ventriculoperitoneal shunt and introduction more than 20 years with the daVinci system (Intuitive
endoscopy – especially useful for visualization of ultrasound image Surgical, Sunnyvale, US). It enables for 3D high-definition visual-
during nerve blockage, where the surgeon is no longer forced to ization, precise hand–eye coordination, physiological tremor filter-
move his sight away from the patient. As of today, there is no ing, and motion-scaling. As of 2016, some 2500 da Vinci systems
assessment of head-mounted devices for the removal of intracra- have been installed and have performed almost half a million pro-
nial tumors [14]. cedures (radical prostatectomy, radical cystectomy, partial
The accuracy of presurgical mapping degrades over the course nephrectomy). The training curricula on virtual reality-robotic sys-
of the operation. The IBIS platform (Intra-operative Brain Imaging tems with mentorships are already well established to provide
System) is created in 2012 an open-source image-guided neuro- excellence in procedures [35]. For general surgery robotics entered
surgery research platform which attempts to fill this gap by valida- only around 2010 for procedures like cholecystectomy, bariatric
tion of intraoperative ultrasound facilitated through AR. Image-to- surgery, hernia repair and other. Virtual reality surgical simulation
patient registration accuracy is on the order of 3.72 ± 1.27 mm and has also proved to be a validated method for robotic training. It
can be improved with ultrasound to a median target registration improves basic skillsets, demonstrates good content and con-
error of 2.54 mm [32]. An updated patient model can be obtained structs validity for laparoscopic and robotic training as well as
within less than 20 s by capturing tracked ultrasound images, translates into improved skills in the operating room [37].
reconstructing a 3D volume and using this volume to automatically NeuroTouch is a VR simulator developed by researchers at McGill
realign preoperative plans. Its clinical application ranges from University, Montreal, Canada, for neurosurgical procedures training.
brain shift assessment, vascular neurosurgery, tumor surgery, It is the work summary of 50 experts out of 20 neurosurgical centers
and spine surgery to DBS/epilepsy electrode implantation [32]. across Canada. It is composed out of 3 main elements: high-end
computer, stereovision system (binoculars which provide 3-D view)
3.3. Surgical training and bimanual haptic tool manipulators. The simulator components
are mounted on the on a special frame, which enables to adjust the
The current healthcare environment demands the best patient height and tilt angle to every participant. As for visualization: a
outcomes with maximal cost efficiency. It heavily restricts the time Wheatstone stereoscope was designed with the usage of binocular
of surgical resident spent under supervision of senior colleagues pieces and two 17-inch LCS screens (1280 1024 px) and surface
and disturbs the ideal Halsted’s approach to surgery education mirrors instead of lenses. The size and distance of the screens shows
[33]. Moreover, it is very dangerous for an inexperienced operator 30 degree of visual field and are focused around 40 cm for eye strain
to start immediately with a living patient, as any move could be reduction. The haptic system is based on linkages connected by
the last. The overriding importance of patient safety, the complex- joints and in NeuroTouch simulator is based on Phantom Desktop
ity of surgical techniques, and the challenges associated with and Freedom 6s system. The data gathered by haptic devices is called
teaching surgical trainees in the operating room are all the factors degree of freedom (DOF) and tells about the tool position (up-down,
driving the need for mixed reality as a new, exciting solution to left-right, forward-backward) and orientation (azimuth, elevation,
these problems. Simulation provides a unique opportunity for roll). Moreover, the foot pedal, tool handle sensors, dial knobs and
learners to practice clinical skills in a low stakes setting before push buttons can be incorporated to the haptic system by Arduino
operating room (OR) experience [33]. connection. The simulation software was developed in-house and
As it is easy to calculate the number of procedures and compli- is based on 3 asynchronous processes updating the multiple tasks
cations, it is much harder to validate their quality. More than 75% (graphics, haptics and tissue mechanics) [38].
of neurosurgical errors are deemed to be technical in nature and Researchers created the first conceptual framework for stan-
therefore preventable [34]. Adequate assessment and room for dardized training with NeuroTouch: Five tasks of increasing diffi-
improvement is necessary – simulation training embrace both of culty were selected as representative of basic and advanced
the tasks. It also enhances learning by implementing mental neurosurgical skill: 1) ventriculostomy, 2) endoscopic nasal navi-
rehearsal practice and staged motor learning. gation, 3) tumor debulking, 4) hemostasis and 5) microdissection.
In general surgery, several randomized controlled trials have Cases are under continuous progress, but the proficiency metrics
shown that virtual reality simulation not only is an efficient use are already obtained for the basic procedures [39–41]. It is worth
of learning time, but can decrease initial and subsequent errors noticing that the simulator may not only judge hard technical skills
in the operating room [34]. In urology simulation is well integrated but also provide input into psychomotor ability and cognitive input
into training curriculum. The 10 attributes of simulation are high- [42]. Moreover, the simulator provides the opportunity to upload a
lighted: (1) Feedback can be provided during the learning experi- particular case and practice it before the real surgery [43].
ence, (2) Learners can use repetitive practice, (3) Simulation can NeuroTouch is a part of Canadian ‘‘rookie camp” for junior res-
be integrated, (4) Level of difficulty can be varied, (5) Simulation idents available in some residency programs across country –
can be adapted to different learning strategies, (6) Clinical varia- though only for the limited time of 1–5 days per year. It has poten-
tion can be incorporated, (7) The environment can be controlled tial to compensate for the limited exposure to certain complex
and changed, (8) The process can safely permit individual learning, neurosurgical cases such as aneurysm clipping. Moreover, simula-
(9) Learning outcomes can be defined and measured, (10) and The tor could provide objective measurement of certain surgical skills
simulation can approximate clinical practice. In the end simulation and knowledge. However, its usage nowadays is limited. Due to
assess not only technical skills, but also non-technical communica- nation-wide survey in Canada lack of funding is the biggest prob-
tion skills and ability to deal with complications [35]. Lately the lem due to program directors whereas residents pinpoints lack of
concept of simulation of not only technical skills, but also team free time as a highest obstacle [44]. The summary of case perfor-
working was introduced in Crisis Management Simulation study, mance may help studies on the acquisition and development as
where neurosurgery residents were teamed with anesthesia resi- well as maintenance of psychomotor skills of young and experi-
dent and had to manage intraoperative crisis. No significant enced neurosurgeons [45].
18 C. Lee, G.K.C. Wong / Journal of Clinical Neuroscience 62 (2019) 14–20
The simulator enables not only to simulate the brain tumor sur- VR set under the guidance of mentor achieve better results than
gery via craniotomy route, but also lets to practice endoscopic unsupervised colleagues. After the simulation training, self-
sinus approach [46]. The McGilll simulator from Canada gathered learners showed substantially lower simulation task scores
high score in both realism (7.97 ± 0.29 out of 10) and usefulness (82.9 ± 6.0) compared with mentored group (93.2 ± 4.8). Both
(8.57 ± 0.69 out of 10). [47] The study from Australia clearly indi- groups demonstrated improved physical model tasks performance
cated that the opinions of participants group are different based in comparison with the actual robot. The mentored group exhib-
on specialty level: students and residents were more likely to give ited lower global mental workload/distress, higher engagement,
a positive realism feedback for the simulator than specialist [48]. and a better understanding of methods that improve performance
Virtual reality training has been introduced into neurosurgery [55].
training program in USA with the help of ImmersiveTouch – the
firm with more than 20 years of experience in simulation. They
started as a flight simulator in the University of Chicago and cur- 3.4. Further directions
rently they provide the wide range of cases: from the basic,
anatomical concepts to the complex procedures and management Current challenges in surgery of brain tumors are: selection of
of rare complications. It enables to upload new, patient-specific surgical approach, balance between extent of resection and leaving
cases [34]. Surgeons can practice difficult procedures under com- parts involved in functional networks [56]. The assessment of neu-
puter control without putting a patient at risk. In addition, sur- ral pathways is currently achieved by awake surgery or intraoper-
geons can practice on these simulators at any time, immune ative electrophysiological monitoring and mapping [57] and
from case-volume or location limitations [15,49]. researched with the use of pre-operative fMRI [58], diffusion ten-
Gasco et al. for the first time assessed not only educational ben- sor imaging [59] – for those methods brain shift during surgery
efit of virtual reality simulation, but also its costs. They created is a problem [60]. Moreover, assessment of post-surgical brain
curriculum for neurosurgery simulation that included basic and tumor treatment response by MRI is fraught with pitfalls such as
advanced skills. 68 core exercises were distributed in individual- differentiating progression from treatment-related changes and
ized sets of 30 for 6 neurosurgery residents and consisted of 79 pseudoprogression [56].
simulations with physical models, 57 cadaver dissections, and 44 The most formidable challenge for mixed reality in the neuro-
haptic/ computerized sessions. Total of 180 procedures and sur- surgical field is a gap between the theoretical concept in a labora-
veys of self-perceived performance were analyzed. Junior residents tory and the real experience. Kersten-Oertel et al. showed that only
(year 1–3) reported proficiency improvements in 82% of simula- 16% of the peer-reviewed articles were evaluated in the operating
tions performed, whereas Senior residents (year 4–6) – in 42.5%. room and only 6% measured the impact on clinical outcome of the
Initial cost of simulation system implementation is $341 978.00, patient [61]. The DVV (data, visualization processing view) taxon-
with $27 876.36 for annual operational expenses [49]. omy has been proposed to support structured discussion in the
In 2000 the VR system Dextroscope with VIVIAN (Virtual future studies to fill this gap [62]. All the major components of
intracranial Visualization and Navigation) was developed for sim- AR environment are highlighted and create an understandable con-
ulation of presurgical planning and procedures. It coregisters tact route between creators of mixed-reality system and end-users
MRI, MRA and CT images into a fused 3D visualization as well as [62]. Moreover, the visualization of complex brain relationship to
is equipped with simulation tools for VR. The registration accuracy pathologies borders and blood supply is hard to implement, though
is 1.0 ± 0.6 mm. It has proved to be useful in both research and clin- it is constantly improving in parallel to changes in real-life brain
ical settings – especially in cranial base surgery, the simulation imaging advancements (like diffusion tensor imaging) [15].
decreased the pre- and intraoperative guesswork and increased The data overload is another contemporary problem [63,64]. It
the surgeon’s confidence in carrying out complex procedures is hard to synthetize all information available for the particular
[50]. It proved to be useful in vascular neurosurgery: aneurysm stage of surgery at once for a one person in the long term. Taking
clipping and arterio-venous malformation excision. Simulation of into consideration an insufficient supply of adequately trained spe-
procedures enabled to rehearse the microsurgical procedure and cialists as compared to the increasing demands and value of their
select the best approach to head positioning, size of craniotomy time, the easiness of mixed-reality devices implementation should
and visualization from different angles [51,52]. be in the center of attention [65].
Dextroscopic virtual reality stimulation can provide an illus- The main limitation for a wide implementation of neurosurgical
trated preoperative planning and training for excision of cerebral simulators is the fact that they require physical space, teachers and
AVM. Dextroscope could help to obtain an anatomical understand- large capital – for the primary investment and on-going mainte-
ing of arterial feeders, nidus, and draining veins in relationship to nance [34].
surrounding cerebral cortex. It allowed one to see the exposure Moreover, mixed reality training poses an opportunity to safely
with the different angles of visualization, similar to what happened test and validate the automated surgery robot, like NauroBlate or
under the operative microscope [51]. PUMA [66], that will support surgeons in their work in the future
To prepare for complicated procedures of the ruptured intracra- [67]. We can envision systems ranging from semiautomated
nial aneurysm clipping patient-specific imaging data from com- devices with integrated scanners and surgical arms, to a fully oper-
puted tomographic angiography of the intracranial circulation ational humanoid machine [68]. Additionally, the emerging serious
and cranium were transferred to the workstation (Dextroscope; medical gaming can become a base for future training programs
Volume Interactions Pte. Ltd., Singapore, Singapore). An aneurysm [69].
clip database was loaded into the patient data set. 3-D volume ren-
dering was followed by data co-registration and fusion. With the
virtual head positioning and craniotomy and angle of application, 4. Conclusions
it allows for assessment of different degree of obliteration of vari-
ous approaches [52]. The technological revolution is a sign of our times. Solutions
Many studies addressed the benefit of VR training system for provided by the technology are embraced by medicine and gradu-
surgeons [16,53,54], but there is only one study found on its limi- ally introduced into everyday clinical practice. This article serves as
tation. According to study performed by Lee and Lee in 2017, which a contemporary summary of virtual and augmented environment
involved 32 participants proved that pupils who were learning on in the field of brain tumor surgery.
C. Lee, G.K.C. Wong / Journal of Clinical Neuroscience 62 (2019) 14–20 19
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