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Robotics in Keyhole Neurosurgery
Robotics in Keyhole Transcranial Endoscope-assisted Microsurgery: A Critical Review of
Existing Systems and Proposed Specifications for New Robotic Platforms
Abstract (structured)
Background: Over the last decade advances in image guidance, endoscopy and tube-shaft
instruments have allowed for the development of keyhole transcranial endoscope-assisted
microsurgery; utilizing smaller craniotomies, and minimizing exposure and manipulation of
unaffected brain tissue. Although such approaches offer the possibility of shorter operating
times, reduced morbidity and mortality, and improved long-term outcomes, the technical skills
required to perform such surgery are inevitably greater than for traditional open surgical
techniques, and they have not been widely adopted by neurosurgeons. Surgical robotics, which
has the ability to improve visualization and increase dexterity, therefore has the potential to
enhance surgical performance.
Objective: To evaluate the role of surgical robots in keyhole transcranial endoscope-assisted
microsurgery.
Methods: The technical challenges faced by surgeons utilizing keyhole craniotomies were
reviewed, and a thorough appraisal of presently-available robotic systems was carried out.
Results: Surgical robotic systems have the potential to incorporate advances in augmented
reality, stereo-endoscopy, and jointed-wrist instruments, and therefore significantly impact on
the field of keyhole neurosurgery. To date, over 30 robotic systems have been applied to
neurosurgical procedures. The vast majority of these robots are best described as supervisory-
controlled, and are designed for stereotactic or image-guided surgery. Few telesurgical robots are
suitable for keyhole neurosurgical approaches, and none are in widespread clinical use in the
field.
Conclusion: New robotic platforms in minimally invasive neurosurgery must possess clear and
unambiguous advantages over conventional approaches if they are to achieve significant clinical
penetration.
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Abstract (unstructured)
Over the last decade advances in image guidance, endoscopy and tube-shaft instruments have
allowed for the development of keyhole transcranial endoscope-assisted microsurgery; utilizing
smaller craniotomies, and minimizing exposure and manipulation of unaffected brain tissue.
Although such approaches offer the possibility of shorter operating times, reduced morbidity and
mortality, and improved long-term outcomes, the technical skills required to perform such
surgery are inevitably greater than for traditional open surgical techniques, and they have not
been widely adopted by neurosurgeons. Surgical robotics, which has the ability to improve
visualization and increase dexterity, therefore has the potential to enhance surgical performance.
In this review we will: consider the evolution of cranial neurosurgery from historical extended
craniotomies to contemporary minimally invasive techniques; address the technical challenges
faced by surgeons utilizing keyhole craniotomies and the scope for robotics to assist in such
operations; thoroughly appraise presently-available robotic systems against these demands; and
propose broad specifications for our vision of new robotic platforms.
Key words
Image Guided Intervention; Minimally invasive surgery; Neurosurgery; Robotic Surgery
Running Title
Robotics in Keyhole Neurosurgery
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Introduction
Neurosurgery is inherently high risk. Pathologies within the brain invariably distort neighboring
anatomical landmarks making accurate and precise intra-operative localization challenging. In
addition, unaffected brain tissue is easily injured, frequently eloquent, and has limited scope for
regeneration. Over the last decade, neurosurgery has greatly benefited from advances in image
guidance allowing improved identification of target pathology and key brain structures. A natural
extension of these developments is the concept of keyhole transcranial endoscope-assisted
microsurgery; utilizing smaller craniotomies, and minimizing exposure and manipulation of
unaffected brain tissue. Although such approaches offer the possibility of shorter operating
times, reduced morbidity and mortality, and improved long-term outcomes, the technical skills
required to perform such surgery are inevitably greater than for traditional open surgical
techniques. Surgical robotics, which has the ability to improve visualization and increase
dexterity, therefore has the potential to enhance surgical performance.
In this review we will: consider the evolution of cranial neurosurgery from historical extended
craniotomies to contemporary minimally invasive techniques; address the technical challenges
faced by surgeons utilizing keyhole craniotomies and the scope for robotics to assist in such
operations; thoroughly appraise presently-available robotic systems against these demands; and
propose broad specifications for our vision of new robotic platforms.
The Evolution of Cranial Neurosurgery towards Keyhole Transcranial Endoscope-assisted
Microsurgical Approaches
Keyhole transcranial endoscope-assisted microsurgery is the product of over century of
technological progress in surgical approach, visualization and manipulation (see Fig. 1). Early
pioneers such as Sir Victor Horsley, who was appointed the world’s first neurological surgeon in
1886, habitually performed extended craniotomies to treat intracranial lesions1. Extended
craniotomies were needed for a number of reasons2, 3. In these early cases pathologies were
localized clinically and a large craniotomy was necessary to ensure the operating surgeon could
locate the lesion. Intra-operative visualization relied on ambient lighting in the operating theatre
and a large craniotomy was required to illuminate the surgical field. Additionally, instruments
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used at the time were designed for general surgery rather than neurosurgery, necessitating large
openings.
Several advances contributed to the replacement of extended craniotomies with mini-
craniotomies2, 3. The introduction of Computed Tomography (CT) in the early 1970s and
Magnetic Resonance Imaging (MRI) in the 1980s allowed brain pathologies such as tumors to be
directly visualized, permitting far more targeted surgical approaches. Intra-operative
visualization was also greatly enhanced with the introduction of the operating microscope in the
1960s, improving illumination and magnification of the surgical field. In parallel to these
developments, surgical instruments were adapted for use in microneurosurgery. Leonard Malis
and M. Gazi Yasargil described the use of bipolar coagulation and purpose-designed
microinstruments that allowed careful surgical dissection.
Over the last decade, further technological progress has led to the development of keyhole
transcranial endoscope-assisted microsurgical techniques. Image guidance systems that combine
pre-operative imaging with live instrument tracking data to bring the real surgical field into
alignment have been widely adopted by neurosurgeons, and are associated with shorter operating
times, reduced blood loss and fewer major complications when compared with standard surgery4.
Endoscopes provide a method of further increasing illumination and magnification, while
extending the viewing angle, with keyhole approaches. Furthermore novel tube-shaft based
surgical instruments have been designed for keyhole surgery permitting improved surgical
manipulation through narrow surgical corridors compared with conventional microinstruments.
Axel Perneczky at the Johannes-Gutenberg University described a number of image-guided
endoscope-assisted keyhole techniques utilizing natural anatomical corridors within the brain to
reach surgical targets. One large case series reported the use of a short eyebrow incision, a
supraorbital keyhole craniotomy approximately 15mm x 25mm in diameter, and a subfrontal or
fronto-lateral approach to the anterior cranial fossa and suprasellar regions. Over a 10-year
period more than 450 patients underwent surgery to treat various pathologies including
intracranial aneurysms, meningiomas, craniopharyngiomas and pituitary adenomas, with the vast
majority making a good recovery (Glasgow Outcome Scale 5 in 86%, and 4 in 6.4%) in this
heterogeneous group5. Keyhole modifications of the subtemporal, retrosigmoid, suboccipital,
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supracerbellar and interhemispheric approaches have also been successfully utilized, providing a
number of routes to reach the deep intracranial cisterns2.
Technical Challenges of Keyhole Craniotomies and the Scope of Robotics to Assist Surgical
Performance
Despite the purported advantages of minimally invasive techniques over conventional
microsurgical techniques, they have not been widely embraced by neurosurgeons. Keyhole
craniotomies remain very technically challenging in spite of the aforementioned advances in
approach, visualization and manipulation. First, although image guidance systems are widely
used for planning surgery, their use intra-operatively generally requires neurosurgeons to
momentarily stop operating, apply a probe to the region of interest (potentially near critical
structures), and then take their eyes off the surgical field to view the image guidance monitors. In
minimally invasive neurosurgical procedures, the relative paucity of anatomical landmarks often
necessitates more frequent use of image guidance, which may considerably impact on surgical
performance. Second, while endoscopes do provide an extended viewing angle compared to
operating microscopes, some deliver lower quality imaging, and most lack stereoscopy, limiting
appreciation of complex spatial relationships within the brain. Third, the use of endoscopes
makes bimanual manipulation difficult or impossible. Within the brain, which is incompatible
with gas insufflation, debris quickly clouds the endoscopic field unless a sucker is concurrently
used; a single surgeon can therefore not easily view and manipulate tissue simultaneously.
Although an additional surgeon may assist, the use of a single anatomical corridor makes it
difficult to do so without the operating surgeons obstructing each other or their instruments
clashing. Instrument holders have recently been developed but can again lead to crowding of
instruments, and inevitably interrupt the operative workflow, as they must be repeatedly
repositioned. Moreover, even when using specially designed tube-shaft instruments,
manipulation through uniportal keyhole neurosurgical approaches is almost co-axial, to the major
detriment of surgical dexterity.
Future technological advances that overcome these technical barriers to keyhole neurosurgery
have the potential to greatly increase the adoption of such techniques by surgeons, and yield
significant improvements in patient outcomes. Augmented reality systems, which fuse virtual
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three-dimensional brain models and the actual operating field, may enhance the operating room
workflow and improve safety by eliminating the need for surgeons to repeatedly interrupt
operations and look away from the surgical field. Such systems are already commercially
available for use with surgical microscopes, but have not yet been widely applied to neuro-
endoscopy. The use of a single-shaft design with a stereo-endoscope and working channels for
instruments may allow for fully endoscopic approaches while preventing instrument clashing.
Although such single-shaft designs do exist, few compatible instruments are available and
control is entirely coaxial limiting their use to relatively straightforward operations such as
Endoscopic Third Ventriculostomy (that requires perforation through the floor of the third
ventricle, rather than tissue manipulation). Therefore, when implementing single-shaft designs,
the development of instruments with a jointed-wrist design would allow for greatly increased
surgical dexterity.
Surgical robotic systems have the potential to incorporate advances in augmented reality, stereo-
endoscopy, and jointed-wrist instruments, and therefore significantly impact on the field of
minimally invasive surgery. In addition, these systems offer the possibility of greater precision,
reduced physiological tremor, and motion scaling.
Appraisal of Existing Robotic Systems for Neurosurgery
Surgical robots can be broadly classified into three categories on the basis of how surgeons
interact with them6: supervisory-controlled robot systems in which the surgeon plans the
operation, and the robot then carries it out autonomously under the supervision of the surgeon;
telesurgical (master-slave) systems in which the surgeon (master) remotely controls the robots
actions (slave); and handheld shared-controlled systems in which the surgeon and robot share
control of the instrument.
To date, over 30 robotic systems have been applied to neurosurgical procedures (see Table 1;
robots performing endovascular or radiosurgical procedures were excluded). The vast majority of
these robots are best described as supervisory-controlled, and are designed for stereotactic or
image-guided surgery7-58. The first such robot, a modified Puma 560 industrial robot (Advance
Research & Robotics, Oxford, CT), was used in 1985 to define the trajectory of a frame-based
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brain biopsy7. In this system the surgeon entered the co-ordinates of a brain lesion, the effector
arm with the probe holder moved to the predefined location, and the surgeon then used the probe
as a guide for trephination and biopsy. Many other supervisory-controlled robots have since been
developed, with clinical studies illustrating their use in brain biopsy, and the implantation of
Deep Brain Stimulation electrodes. Perhaps the most widely used supervisory-controlled robots
within neurosurgery are the SpineAssist and Renaissance systems (Mazor Surgical Technologies,
Caesarea, Israel). Although principally developed for pedicle screw placement, they have also
received regulatory approval for use in the brain35-46. These robots offer a theoretical advantage
over conventional surgery because of their high precision and accuracy6, and may reduce
radiation exposure of the patient and surgical team59.
A number of telesurgical robots have been utilized in neurosurgery60-85. One of the earliest
examples of such a system was the Robot Assisted Microsurgery (RAMS) robot (NASA,
Pasadena, California, USA)63. In a feasibility study, carotid arteriotomies were created and
closed using either RAMS or conventional microsurgical techniques in 10 rats; the precision and
technical quality, and error rate were comparable but the use of the RAMS robot was associated
with a twofold increase in the procedure length.
NeuroArm (University of Calgary, Calgary, Canada) is a robot purpose built for
microneurosurgery that is endowed with a number of distinct features64, 65. The console provides
visual, auditory and tactile feedback to the operating surgeon. The robot is MRI compatible,
allowing real-time imaging during procedures to account for brain shift. The manipulator
consists of two arms, each with 8 degrees of freedom (DOF), with end-effectors that mimic a
surgeon’s hand, and interface with microinstruments. Early reports from the NeuroArm case
series’ have been promising but its use at present is limited to microneurosurgery rather than
endoscope-assisted neurosurgery.
A team in Tokyo, Japan has also constructed a telesurgical robot to assist with
microneurosurgery. The MM-1 robot consists of a passive base with 6 DOF, and two robotic
arms each with 6 DOF66. In validation studies, closure of partial arteriotomies and end-to-end
anastomosis of the ICA was performed successfully in 20 rats. The frontotemporal transsylvian
approach, suboccipital retrosigmoid, and endonasal transphenoidal approaches were also
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performed in cadavers. Although a significant learning curve was demonstrated initially surgical
performance quickly reached a plateau, and the procedure durations were still unacceptably long.
Furthermore, the manipulators were felt to be too bulky to be used in the delicate operative field.
Recently, the same research group has developed a modified master-slave robot platform, with
two robotic arms each with 7 DOF, and either bent- or straight-forceps as end-effectors 85. In
feasibility studies the robot was able to perform a number of maneuvers including end-to-end
anastamoses of 0.3mm artificial vessels, which is very difficult to do manually, though with a
longer task completion time.
The da Vinci surgical system (Intuitive Surgical, Sunnyvale, California, USA) is the most
frequently used telesurgical robot worldwide but is not as yet widely used for neurosurgery.
Unlike the abovementioned robots, the da Vinci system is designed for endoscopic keyhole
surgery. A camera arm equipped with two lenses is used to generate a high-resolution
stereoscopic image display. Instruments are carried by two or three working arms, which include
articulated endo-wrists that increase surgical dexterity. In addition, the system allows for tremor
filtering and motion scaling, allowing more delicate tissue manipulation. A major advantage of
the da Vinci system is the ergonomic benefit provided by the anthropomorphic master console
that restores the motor-visual alignment of the camera and surgical instruments. The da Vinci
robot has been successfully used in a broad range of surgical procedures, particularly within the
field of urology. Several groups have demonstrated the feasibility of using the da Vinci system in
spinal surgery68-76. Unfortunately, the fact that the da Vinci system consists of several arms,
rather than possessing a single-shaft design, makes it ill suited to keyhole surgical procedures
within the brain. In a recent cadaveric study the da Vinci system was used during a supraorbital
approach and the issue of arm collisions within a narrow surgical corridor was cited as a key
drawback, which could interrupt operative workflow, and also raises safety concerns86.
NeuRobot (Shinshu University School of Medicine, Matsumoto, Japan) was the first telesurgical
robot designed specifically for keyhole neurosurgery77-82. The system has a single-shaft design
approximately 10mm in diameter containing a three-dimensional endoscope, and three sets of
micromanipulators, each with 3 DOF (rotation, neck swinging, and forward/backward motion).
Although the system was able to perform relatively simple surgical procedures in cadavers and
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human studies, the authors report the system was limited by lack of maneuverability of the
micromanipulators and robot itself.
Another Japanese group have recently developed a similar Neurosurgical Robot for Brain Tumor
Removal (Nagoya Institute of Technology, Nagoya, Japan)83, 84. As with NeuRobot the robot has
a single-shaft design approximately 10mm in diameter, containing a three-dimensional
endoscope, an irrigation system, and a volume control suction tool, with 2 DOF at the instrument
tips. Although preliminary evaluation of the robot on a phantom demonstrated feasibility it is
likely that, as with NeuRobot, the restricted working space will limit its clinical use.
Only a handful of handheld shared-controlled systems have been described in the literature for
use in neurosurgery87-90. Shared-controlled systems exploit both the precision of a robot in the
control of the surgical instruments and the natural manipulation skill of the surgeon. In the
Steady Hand System (John Hopkins University, Baltimore, USA), for example, the surgical
instrument is held by both the robot and operator which allows finer, tremor-free motion control
of the instrument, and also lets surgeons to define critical ‘no-go’ areas to be avoided 87, 88.
Similarly, the Craniostar (University of Heidelberg, Heidelberg, Germany) and Safe
Trephination System (RWTH-Aachen, Aachen, Germany) allow surgeons to fashion
craniotomies along predefined paths, while reducing the risk of dural injury89, 90. Another
advantage of these hand-held systems is ease in which they can be integrated into the surgical
workflow compared to telesurgical systems that suffer from long setup times.
Proposed Specifications for New Robotic Platforms
Although a multitude of robots have been applied to neurosurgery, few are applicable to
minimally invasive techniques, and no robots are in widespread clinical use in the field. New
robotic platforms in minimally invasive neurosurgery must possess clear and unambiguous
advantages over conventional approaches if they are to achieve significant clinical penetration.
Here we outline broad specifications for our vision of new robotic platforms designed to assist
with keyhole transcranial endoscope-assisted microsurgical approaches (see Fig. 2).
It is likely that most systems in the near future will adopt a master-slave arrangement with the
surgeon sitting comfortably at a console controlling the robots actions. This will restore
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visuomotor alignment and provide considerable ergonomic benefits, particularly in cases in
which the patient is placed in a seated position, such as those utilizing the supracerebellar
infratentorial approach, that presently require the operator to stand hunched over with their arms
outstretched for several hours.
In order to safely approach pathology, new surgical robots must be fully integrated with image
guidance systems, and augmented reality displays utilized at the surgical console to improve the
operating room workflow. The use of intra-operative imaging such as ultrasound, CT or MRI to
compensate for brain shift is also desirable to ensure accuracy of the system is maintained
throughout the course of an operation.
The overall design of robots themselves should be a single shaft with visualization and
manipulation features located at their ‘head’. The length of the shaft should be approximately
300mm, long enough to access deep-sited lesions using the keyhole concept. The diameter of the
shaft should be as small as possible to minimize trauma. In animal studies brain retraction
pressures of 20mmHg or less do not appear to be associated with cortical damage91, and
subsequent case series’ using cylindrical retractors up to 20mm in diameter have recorded
surrounding intracranial pressures of less than 10 mmHg92 with no approach-related neurological
deficits observed post-operatively. Nonetheless, it is suggested that robots be no more than
12mm in diameter to reduce the risk of brain injury.
Visualization in new robotic systems will be achieved through cameras providing uninterrupted
illumination, magnification and wide-angle images of the operative field. High-definition and
three-dimensional neuro-endoscopes have recently been developed, and the incorporation of
such devices into surgical robots would allow for unparalleled views within the brain. In
addition, endoscopes may be used in conjunction with photosensitizing agents such as 5-
aminolevulinic acid (5-ALA) for fluorescence guided tumor resection. In a randomized
controlled multicentre trial of patients undergoing surgery for malignant glioma, resection was
achieved in 65% with the use of 5-ALA versus 36% using white light alone93. A number of
emerging technologies may ultimately allow real-time in-vivo visualization of tumor tissue, with
the promise of even greater identification of tumor cells. In confocal microendoscopy, for
example, the principles of confocal microscopy and fiber-optic endoscopy are combined to
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reveal cellular morphology and micro-architecture in a similar manner to cytological and
histological analysis respectively94, 95.
Bimanual manipulation of delicate tissue will require at least two working channels for
instruments in putative robotic systems. Robotic end-effectors should be miniaturized to a size
comparable with conventional microinstruments, with the smallest tips measuring approximately
1-2mm. Perhaps most importantly these instruments must have sufficient degrees of freedom to
operate within the small working spaces used in keyhole approaches; jointed-wrist designs will
almost certainly be invaluable in this context (see Fig. 3). In the first instance, a range of
standard microinstruments such as bayonet forceps, bipolar coagulation, scissors, dissectors,
needle-holders, and suction tubes would likely be used. Additional instruments such as waterjet
dissection, which may allow for more rapid dissection around delicate neurovascular structures,
may also be developed in subsequent iterations.
Control of slave-micromanipulators will rely on intuitive human-machine interfaces at the
master-console. The development of systems that provide haptic-feedback has proved
challenging for researchers within surgical robotics. However, surgical robots such as NeuroArm
demonstrate the technological feasibility of incorporating force-feedback, and such robots will
undoubtedly provide a more immersive environment.
Conclusions
The keyhole concept holds arguably greater potential to improve patient outcomes in
neurosurgery than in other surgical fields because, in addition to reducing the length of scalp
incisions and size of craniotomies, minimally invasive techniques entail reduced exposure and
manipulation of unaffected brain tissue, which may reduce the risk of serious approach-related
complications such as stroke or death. Although keyhole approaches utilizing image-guidance,
endoscopy and tube-shaft instruments have been developed as alternatives to most conventional
open microsurgical techniques, they remain highly challenging and have not been widely
accepted into neurosurgical practice. The development of master-slave robots encompassing
improvements such augmented-reality, stereo-endoscopy, and jointed-wrist instruments, may
herald a paradigm shift in neurosurgery towards minimally invasive neurosurgical techniques
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that most neurosurgeons find almost impossible to perform safely using presently available
surgical tools.
In the long-term, technological progress may see robots becoming smaller, more powerful and
less costly, in a way comparable to the growth of digital computing over the last 50 years.
Perhaps the world’s first digital computers were the Colossus machines developed for
cryptanalysis during World War 2, each of which weighed approximately a ton and occupied an
entire room. Over the proceeding decades personal computers such as desktops and laptops were
popularized. More recently, further miniaturization has led to the integration of digital computing
into everyday ‘smart’ devices such as mobile phones or wristwatches. The result, paradoxically,
has been the regression of digital computing into the background of people’s lives. There is some
evidence that robotic may be evolving along a similar path, and it is possible that the large and
cumbersome robots of today will eventually be replaced with a range of ‘smart’ handheld
instruments each encompassing robotic qualities, and performing a different task96.
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Figures
Fig. 1. Evolution of cranial neurosurgery towards keyhole transcranial endoscope-assisted
microsurgical approaches. CT = Computed Tomography; MRI = Magnetic Resonance
Imaging
Fig. 2. Proposed working specifications of new robotic platforms. HD = High Definition
Fig. 3. Comparison of visualization and manipulation in present-day and proposed robot-assisted
keyhole approaches. (A) At present bimanual dissection occurs under a microscope with
a narrow field of view, using rigid instruments with limited dexterity, making
triangulation difficult. (B) In the future robotic platforms with integrated endoscopy will
allow a wider field of view, and joint-wristed instruments will improve dexterity, and
facilitate triangulation.
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