Feasibility of robot-assisted neuroendovascular procedures

Vitor Mendes Pereira Division of Neuroradiology, Department of Medical Imaging, Toronto Western Hospital, University Health Network, University of Toronto; and
Division of Neurosurgery, Department of Surgery, Toronto Western Hospital, University Health Network, University of Toronto, Ontario, Canada

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Patrick Nicholson Division of Neuroradiology, Department of Medical Imaging, Toronto Western Hospital, University Health Network, University of Toronto; and

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Nicole M. Cancelliere Division of Neuroradiology, Department of Medical Imaging, Toronto Western Hospital, University Health Network, University of Toronto; and

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Xiao Yu Eileen Liu Division of Neuroradiology, Department of Medical Imaging, Toronto Western Hospital, University Health Network, University of Toronto; and

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Ronit Agid Division of Neuroradiology, Department of Medical Imaging, Toronto Western Hospital, University Health Network, University of Toronto; and

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Ivan Radovanovic Division of Neurosurgery, Department of Surgery, Toronto Western Hospital, University Health Network, University of Toronto, Ontario, Canada

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Timo Krings Division of Neuroradiology, Department of Medical Imaging, Toronto Western Hospital, University Health Network, University of Toronto; and
Division of Neurosurgery, Department of Surgery, Toronto Western Hospital, University Health Network, University of Toronto, Ontario, Canada

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OBJECTIVE

Geographic factors prevent equitable access to urgent advanced neuroendovascular treatments. Robotic technologies may enable remote endovascular procedures in the future. The authors performed a translational, benchtop-to-clinical study to evaluate the in vitro and clinical feasibility of the CorPath GRX Robotic System for robot-assisted endovascular neurointerventional procedures.

METHODS

A series of bench studies was conducted using patient-specific 3D-printed models to test the system’s compatibility with standard neurointerventional devices, including microcatheters, microwires, coils, intrasaccular devices, and stents. Optimal baseline setups for various procedures were determined. The models were further used to rehearse clinical cases. Subsequent to these investigations, a prospective series of 6 patients was treated using robotic assistance for complex, wide-necked intracranial saccular aneurysms between November 2019 and February 2020. The technical success, incidence of periprocedural complications, and need for conversion to manual procedures were evaluated.

RESULTS

The ideal robotic setup for treatment of both anterior and posterior circulation aneurysms was determined to consist of an 80-cm guide catheter with a 115-cm-long intermediate catheter, a microcatheter between 150 and 170 cm in length, and a microwire with a minimum length of 300 cm. All coils, intrasaccular devices, and stents tested were compatible with the system and could be advanced or retracted safely and placed accurately. All 6 clinical procedures were technically successful, with all intracranial steps being performed robotically with no conversions to manual intervention or failures of the robotic system. There were no procedure-related complications or adverse clinical outcomes.

CONCLUSIONS

This study demonstrates the feasibility of robot-assisted neurointerventional procedures. The authors’ results represent an important step toward enabling remote neuroendovascular care and geographic equalization of advanced endovascular treatments through so-called telestroke intervention.

ABBREVIATIONS

DAC = distal access catheter; ICA = internal carotid artery; MCA = middle cerebral artery; PCI = percutaneous coronary intervention; PCoA = posterior communicating artery; VA = vertebral artery; VasoCT = cone-beam CT vascular imaging with diluted contrast injection.

OBJECTIVE

Geographic factors prevent equitable access to urgent advanced neuroendovascular treatments. Robotic technologies may enable remote endovascular procedures in the future. The authors performed a translational, benchtop-to-clinical study to evaluate the in vitro and clinical feasibility of the CorPath GRX Robotic System for robot-assisted endovascular neurointerventional procedures.

METHODS

A series of bench studies was conducted using patient-specific 3D-printed models to test the system’s compatibility with standard neurointerventional devices, including microcatheters, microwires, coils, intrasaccular devices, and stents. Optimal baseline setups for various procedures were determined. The models were further used to rehearse clinical cases. Subsequent to these investigations, a prospective series of 6 patients was treated using robotic assistance for complex, wide-necked intracranial saccular aneurysms between November 2019 and February 2020. The technical success, incidence of periprocedural complications, and need for conversion to manual procedures were evaluated.

RESULTS

The ideal robotic setup for treatment of both anterior and posterior circulation aneurysms was determined to consist of an 80-cm guide catheter with a 115-cm-long intermediate catheter, a microcatheter between 150 and 170 cm in length, and a microwire with a minimum length of 300 cm. All coils, intrasaccular devices, and stents tested were compatible with the system and could be advanced or retracted safely and placed accurately. All 6 clinical procedures were technically successful, with all intracranial steps being performed robotically with no conversions to manual intervention or failures of the robotic system. There were no procedure-related complications or adverse clinical outcomes.

CONCLUSIONS

This study demonstrates the feasibility of robot-assisted neurointerventional procedures. The authors’ results represent an important step toward enabling remote neuroendovascular care and geographic equalization of advanced endovascular treatments through so-called telestroke intervention.

In Brief

Robot-assisted neuroendovascular procedures are one of the most recent breakthroughs in the field of neurointervention that will lead to a new era of improved precision, reliability and, in the future, automation and remote surgery. The authors demonstrated an early series of complex aneurysm cases treated robotically with flow-diverting stents or stent-assisted coiling. This is a landmark study demonstrating the feasibility and safety of the CorPath GRX adapted to neurointerventions.

Endovascular techniques to secure ruptured cerebral aneurysms or to revascularize acute ischemic strokes have become the first-choice approach for these emergency, life-threatening neurovascular conditions.1–5 Although these approaches have been adopted rapidly throughout the developed world, they require significant expertise to perform. Thus, a significant portion of the global population remains without access due to a combination of geographic and socioeconomic factors. Poorer countries may lack the ability to attract the needed expertise, whereas relatively wealthier but geographically large countries such as Australia, Canada, and the US may simply have populations that are too remote or too widely dispersed for equitable access to limited resources. A recent study, for example, has estimated that more than 40% of the US population lacks timely access to an endovascular-capable stroke center.6

Robot-assisted, remote stroke treatment presents an appealing solution to these economic and geographic barriers. The concept of “telestroke” currently encompasses only remote diagnosis and treatment recommendations. The ability to perform interventional procedures in real time, over long distances, could give new meaning to the term and revolutionize the field of neuroendovascular intervention. Citizens of developing countries or remote, underserved areas could thus conceivably have equitable access to experts and state-of-the-art treatments. Realization of this goal will require identification of a suitable robotic platform and systematic evaluation of its capabilities for remote applications.

The CorPath GRX Robotic System (Corindus, A Siemens Healthineers Company) is a robotic platform initially developed for robot-assisted percutaneous coronary intervention (PCI).7,8 It is currently being evaluated for fully remote percutaneous coronary stenting, or “telestenting.”9–12 More recently, a number of key engineering modifications have been made to the system’s device-handling mechanics that may facilitate its use for robot-assisted intracranial neuroendovascular procedures.13,14 To test the robotic system’s feasibility for this application, we performed a series of in vitro experiments in which a selection of standard endovascular devices were used. Based on the favorable results of these evaluations, we have performed and now describe the first clinical experience with robot-assisted neuroendovascular intervention for stent-assisted coiling and flow-diverter insertion in the treatment of intracranial aneurysms.

Methods

Study Overview

This proof-of-concept study evaluated the feasibility of neuroendovascular procedures by using the CorPath GRX Robotic System in two phases. An experimental phase, which included in vitro experiments and patient-specific rehearsals performed using 3D-printed models, was followed by translation to a series of robot-assisted clinical interventional procedures.

Robotic System

The CorPath GRX Robotic System has been described previously.8 Briefly, the system enables simultaneous or independent robotic actuation of a catheter, wire, and therapeutic device, under the control of the operator. The bedside unit, composed of the robotic arm, drive, and single-use cassette, is mounted on the angiography suite table and houses all the controlled devices (Fig. 1). It is connected by a communications cable to a remote radiation-shielded console within the angiography suite or control room. Joystick and touchscreen controls enable precise millimetric movement.

FIG. 1.
FIG. 1.

General room (upper) and catheter stack (lower) setup for robot-assisted procedures. Note: CoPilot Y-Connectors are required for optimal compatibility with the robotic drive. Slack in the catheter stack should be minimized; sterile towels can be used for support.

Recent system modifications, also described previously,13,14 were implemented to allow the system to accommodate microcatheters, increased length of distal navigation, and increased operator control through new, automated movements.13 The system is currently cleared for PCI and peripheral vascular interventions in the US, EU, and other select countries, and for neuroendovascular intervention in the EU, Australia, and New Zealand.

It is important to note that the current iteration of the robotic system is designed to manipulate microcatheters, microwires, and interventional devices only; all procedures related to vascular access, cannulation, and placement of distal access catheters (DACs) are performed manually prior to engaging the robotic system.

In Vitro Robotic Simulation Performed Using Cataloged Patient-Specific Silicone Models

We simulated neuroendovascular procedures in patient-specific silicone models of 12 intracranial aneurysms, created from actual patient images, to test commonly used endovascular devices and implants for compatibility with the robotic system. The model set was from our institutional library, and comprised 3 levels of difficulty with various aneurysm geometries and locations, including internal carotid artery (ICA) paraclinoid segment (n = 6); basilar tip (n = 2); middle cerebral artery (MCA; n = 2); posterior communicating artery (PCoA; n = 1); and petrous carotid artery (n = 1). Flow-diversion cases included large discrepancies in vessel diameter along the stent deployment zone and tortuous parent vessels that could increase the risk of stent kinking or malapposition.

All models were connected to a closed pulsatile perfusion circuit to simulate patient hemodynamic factors. Access devices tested included the following: various microwires; microcatheters; intermediate catheters and guide catheters of varying sizes and lengths; and treatment devices including various coils, stents, flow-diverting stents, and intrasaccular devices. The first part of the investigation focused on compatibility of guiding catheters and DACs for vascular access, and the second part on compatibility assessment of microcatheters, microwires, and implanted treatment devices in intracranial procedures (Fig. 2 and Supplemental Table S1).

FIG. 2.
FIG. 2.

Outline of our translational benchtop-to-clinical approach demonstrating the feasibility of robotic assistance during endovascular neurointerventional procedures, highlighting the goals and endpoints of each phase. A total of 235 experiments were performed using a variety of access devices and intracranial implant devices in 12 in vitro silicone aneurysm models from our cataloged library. Refer to Supplemental Table S1 for the complete list of devices and compatibility.

Vascular Access

A DAC was positioned manually at the V4 segment of the vertebral artery (VA) for posterior circulation aneurysm models or at the petrous ICA for anterior circulation aneurysm models. Then, a microcatheter (SL-10; Stryker) and microwire (Synchro 300 cm; Stryker) were loaded into the respective guide tracks within the robotic single-use cassette and manipulated with the robotic system. Device compatibility was graded as “pass” or “fail.” To be graded “pass,” the microcatheter had to successfully catheterize the target aneurysm and the distal vessel under full robotic control, reaching an appropriate position for an intracranial stent placement. Vascular access catheters that were an inappropriate size or length to satisfy this criterion were graded “fail.”

Intracranial Procedures

We next evaluated compatibility of microcatheters, microwires, coils, intrasaccular devices, and stents with the robotic system (Fig. 2). Baseline vascular access setup was based on findings from the initial experiments, consisting of an 8-Fr Neuron Max guide catheter (Penumbra Medical) and a Navien 5-Fr intracranial support catheter (Medtronic).

Devices were placed in the appropriate track within the robotic cassette and manipulated robotically. For microcatheters, compatibility was graded as “pass” if they could be navigated robotically past the intracranial aneurysm and into a vessel at least 20 mm distal to the aneurysm neck. Microwires had to be successfully pushed, pulled, and rotated, and had to support microcatheter placement distally.

Coils were considered compatible with the system if they could be completely deployed inside an aneurysm, completely retracted, and successfully detached. Stents and intrasaccular devices were considered compatible if they could be deployed successfully and placed accurately under robotic manipulation, twice for each device, according to their instructions for use, in two different vascular models of standard and complex tortuosity.

Stent deployment was considered successful if stents were completely open and well opposed to the parent vessel wall, as assessed by cone-beam CT vascular imaging with diluted contrast injection (VasoCT). Stent placement was considered accurate if stents demonstrated good apposition across the aneurysm neck, with at least 5-mm neck margins on each side as shown by VasoCT.

Intrasaccular deployment of a Woven EndoBridge (WEB) device was considered successful if devices could be partially deployed, resheathed, adjusted positionally at least once, and then fully deployed robotically within the aneurysm, as assessed by VasoCT.

The full range of system functionality, including various system software automations such as Active Device Fixation,13 Limited Speed, Rotate on Retract,15 and Turbo mode, was also evaluated. We tested each of these automated robotic movements in different steps of the procedure to evaluate where each would provide the most benefit, as well as to define any safety measures for using each function.

Based on the bench experiments, we developed treatment protocols and safety measures for each procedure type, to be used as guidelines for patient-specific rehearsals. As an example, Fig. 3 demonstrates our protocol for stent-assisted coiling of basilar tip aneurysms.

FIG. 3.
FIG. 3.

Case 2. Perioperative robotic maneuvers used in different steps of the case—stent-assisted coiling of a basilar tip aneurysm (also illustrated in Fig. 5B). Row 1: Digital subtraction angiography (DSA) roadmap images from different steps of the procedure. Row 2: Superior view of the robotic console in the cockpit and an illustration of the operator’s hands operating the joysticks and different commands. Column 1: Vessel catheterization (right VA injection roadmap)—microcatheter (orange arrow) navigation with the aid of the microwire (green arrow). We demonstrate the function “Rotate on Retract” that is an automated function on the microwire. Column 2: Deployment of the distal end of the stent (upper red arrow pointing to 3 dark markers) using millimetric control, demonstrated by the hands on the touchscreen console. Orange arrow shows the microcatheter tip marker mid-deployment, with the proximal marker of the stent (lower red arrow) still inside the microcatheter. Column 3: Final stent deployment shows microcatheter tip (orange arrow) pulled back more proximally now, closer to the proximal marker of the stent (lower red arrow), performed using the joystick controls under the “Limited Speed” function. Column 4: Entering back into the lumen of the stent with the microcatheter is performed using the robotic function “Active Device Fixation,” which functions to automatically match the distance of the forward movement of the microcatheter (orange arrow) with equal retraction of the stent wire (distal red arrow), much like a manual “pinning the wire” technique, but performed with only 1 joystick.

Presurgical Rehearsal Performed Using Patient-Specific, 3D-Printed Models

To train the team prior to clinical application, we performed procedural rehearsals using the robotic system in exact, flexible, photopolymer replicas of the aneurysms that we planned to treat, which had been 3D printed from patient-specific CTA image data (Biomodex).

We preselected the system (i.e., vascular access materials, stent, and coil sizing) that we planned to use in the real clinical case, based on the protocols we developed. The primary endpoint during in vitro rehearsal was to successfully perform all intracranial steps of the planned clinical endovascular procedure robotically in the 3D-printed model, without conversion to a manual procedure. The secondary aims were to assess how various software automations could be used to facilitate navigation and other procedural steps; to establish clear, two-way communication protocols between the bedside team and the robotic system’s operator; and to fastidiously rehearse a conversion to a manual procedure in the event that an emergency conversion was required during the patient procedure.

Clinical Case Series Overview

Following rehearsals, we performed the first prospectively collected patient series evaluating the feasibility of robot-assisted neuroendovascular procedures using the CorPath GRX Robotic System. The institutional ethics board of Toronto Western Hospital approved the study, and all patients provided informed written consent.

Patient Selection

Cases were selected during our institution’s multidisciplinary conference (representing neurosurgery, vascular neurology, and interventional neuroradiology), which reviews all elective cases and considers aneurysm characteristics such as size and location, and other risk factors for aneurysmal rupture in making treatment recommendations. Once a decision for a treatment was made, patients underwent a detailed consent process with the primary operator regarding the procedure.

All patients harboring a complex, wide-necked intracranial saccular aneurysm, defined as an aneurysm with a neck diameter greater than 4.0 mm or a dome-to-neck ratio of less than 2, and requiring treatment with intracranial stenting and/or coiling were considered for this study. Intracranial arterial dissections and fusiform, inflammatory, or infectious aneurysms were excluded.

Neuroendovascular Robot-Assisted and Remote-Controlled Procedure

The robot-assisted procedures required a new workflow and logistical setup inside the angiography suite compared to more traditional neuroendovascular cases (Fig. 1 and Supplemental Fig. S1). The primary operator controlled the robotic drive from a console that was physically removed from the patient but located within the angiography suite for these initial cases. Because the workstation is shielded from radiation, the primary operator was able to forgo leaded garments.

The bedside team was composed of a technologist with specialized training in the use of the robot, and an endovascular physician (Supplemental Fig. S1). Together, this team prepared the devices, loaded them into the robotic system, and provided for an emergency conversion to manual procedure if needed. The bedside physician established vascular access and placed the necessary guide catheters in the relevant vessel before connecting and loading the robotic drive and cassette. In order to perform these tasks, control of the procedure and of the fluoroscopic and robotic equipment had to be shifted continuously between the robotic system’s operator and the bedside team. For this reason, clear communication between the teams was vital because they are physically separated from one another, with no direct line of sight. We used a combination of call-out and closed-loop communication, which we rigorously rehearsed in the patient-specific aneurysm model rehearsals. These established teamwork techniques are used in many other scenarios in order to enhance patient safety.16

All procedures were performed under general anesthesia. The manual portion of the procedure began with gaining radial or femoral arterial vascular access and placing an 8-Fr or 6-Fr short vascular sheath (Terumo Medical Corp.). The bedside team navigated a guiding catheter (Neuron Max 8-Fr or Benchmark 6-Fr; Penumbra) into either the proximal ICA or the subclavian artery. A DAC (SOFIA 5-Fr or 6-Fr; Microvention) was then navigated as far as the planned distal access parking position, in either the petrous ICA or the V4 segment of the VA, taking into consideration the forward distal travel capacity of the robotic arm. Subsequently, the microcatheter and microwires were connected to the robotic arm by using a specific rotating hemostatic valve. All subsequent intracranial steps were performed robotically.

Endpoints and Data Analysis

Demographic, clinical, and procedural characteristics were recorded. The prespecified primary outcome was defined as technical success without periprocedural complications or conversion to a manual procedure. We defined technical success as the completion of all intracranial steps of the procedure using the robotic system. A conversion to manual was defined as the removal of all catheters and devices from the robotic system in order to continue the case manually. Periprocedural complications were defined as any perioperative adverse clinical event, including arterial dissection, aneurysm perforation, stent misplacement, coil migration, coil stretching, or any procedural issues occurring during the robot-controlled manipulation by the operator.

Secondary safety endpoints were defined as follows: 1) any distal emboli or other thromboembolic complications during the final angiogram; or 2) any new neurological symptoms or changes in modified Rankin Scale score during the hospital stay. Other technical secondary outcome measures were aneurysm occlusion, stent-wall apposition, and stent positioning related to the neck of the aneurysm, as assessed with VasoCT. We also allowed the exchange of up to 2 sterile robotic system cassettes during the procedure in case of cassette error or malfunction, as long as this step could be performed without interfering with the overall procedure or resulting in an unplanned conversion to a manual procedure.

Results

Device Compatibility

We performed a total of 235 experimental tests in 12 patient-specific aneurysmal models representing both anterior (ICA and MCA) and posterior (basilar) circulation. We assessed 8 guiding catheters, 12 DACs, 19 microcatheters, 10 microwires, 6 types of coils (in a full range of sizes and lengths), 7 intracranial stents (including both laser-cut bridging stents and braided flow-diverting stents), and 1 intrasaccular device in 90 simulated procedures (Fig. 2). The results of these experiments are summarized in Supplemental Table S1.

Simulated Vascular Access

We tested 96 combinations of guide catheters and DACs for the ability to reach the intracranial circulation and to advance the microcatheter to the target aneurysm. All combinations of devices were compatible with 80- and 90-cm guide catheters in the anterior circulation models, but the 90-cm catheters were incompatible for treatment of posterior circulation aneurysms. All DACs were effectively placed up to their maximum limited distal position; however, only DACs with a length between 105 and 120 cm (ideally, 115-cm length) provided enough distal intracranial support. With a guide catheter length of 80 cm, 7/12 DACs (58%) failed compatibility. DACs 105 cm or shorter provided inadequate microcatheter working length distally and DACs 120 cm or longer provided inadequate physical microcatheter length proximally.

Simulated Intracranial Procedure

Within the baseline vascular access setup of a Neuron Max (80-cm length) and a Navien 5-Fr (115-cm length), microcatheters between 150 and 170 cm in length (n = 15/19; 79%) were compatible with the robotic system. Microcatheters 110 cm in length (4/19; 21%) were too short to complete the intracranial procedure.

Only 0.014-inch microwires more than 300 cm in length (n = 5/10 tested; 50%) were compatible. Although all microwires could be precisely advanced forward and backward, the hydrophilic coating on some intracranial endovascular wires affected rotational movements. We discovered that drying the proximal end of wires prior to loading gave the robotic actuators better grip, allowing for 1:1 rotation capability and increasing the success rates from 75% to 97%.

In summary, we determined that the ideal robotic setup for treatment of both anterior and posterior circulation aneurysms consisted of an 80-cm guide catheter with a 115-cm-long intermediate catheter, a microcatheter between 150 and 170 cm in length, and a microwire with a minimum length of 300 cm.

All coils and intrasaccular devices tested were compatible with the system and could be advanced or retracted safely and placed inside an aneurysm. All coils tested were successfully detached once placed inside the aneurysm. All intracranial stents tested were compatible with the device track and its respective microcatheter. Stents could be navigated as far as the distal tip of the microcatheter and successfully placed across the neck of the aneurysm in 100% of the cases on the standard vascular geometry models. In the tortuous vascular anatomy, all but one device were successfully placed. We used 6 cassettes to perform 235 experimental tests, during which we encountered 2 cassette errors (in one the device and/or microwire could not be advanced, and in the other there was a system or mechanical cassette failure) that required device repositioning or cassette change.

Presurgical Rehearsal

We performed a total of 3 patient-specific rehearsals using preplanned combinations of access and treatment devices (Fig. 4 and Table 1). All combinations were successful, with accurate manipulation, placement, and deployment of all intracranial microcatheters, microwires, and implant devices and with no manual conversions. We used 1 cassette for each rehearsal, with no cassette errors or changes required. Table 1 lists the various automated robotic functions used and highlights safety concerns for each rehearsal. We found the software automations to be useful in the following scenarios:

  • Millimetric control allowed deployment of stents and intrasaccular devices 1 mm at a time while the microcatheter was being retracted 1 mm at a time, improving the precision of placement.

  • Limited Speed allowed for more controlled movements during placement of coils and other devices.

  • Turbo mode allowed for rapid removal of the microwire, once safely retracted into the microcatheter.

  • Rotate on Retract enabled torquing of the microwire in various directions while removing microwire slack.

  • Active Device Fixation approximated the manual technique of “pinning” the wire and advancing the microcatheter by using an over-the-wire technique, and was very useful to allow careful advancement of the microcatheter over the wire once the wire was in the aneurysm sac. We found that an important safety consideration when using Active Device Fixation is that it must be deactivated before removing the wire when the microcatheter is positioned inside the aneurysm sac; otherwise, the microcatheter could jump forward during removal of the wire.

FIG. 4.
FIG. 4.

Select in vitro experiments in patient-specific aneurysm models. A: Stent-assisted coiling of a basilar aneurysm model (patient-specific to clinical case 2). B: Flow-diverting stent treatment of an ICA aneurysm model. C: Flow-diverting stent treatment of an MCA bifurcation aneurysm model. Column 1: Pictures of the physical model. Column 2: A 3D (row A only) or 2D endoluminal image of the model. Column 3: Subtracted (row A only) or unsubtracted images showing the devices midtreatment. Column 4: Unsubtracted (row B only) or subtracted images demonstrating final device apposition.

TABLE 1.

Details of preclinical procedure rehearsals performed using patient-specific 3D-printed aneurysm models

DetailPatient-Specific Model
123
ProcedureStent-assisted coilingStent-assisted coilingFlow-diverter insertion
No. of coils106NA
Stent typeNeuroform AtlasNeuroform AtlasSurpass Evolve
Stent size, mm4.5 × 213.0 × 244.5 × 20
Stent positioningGoodGoodGood
Stent appositionGoodGoodGood
Final angiogramGood aneurysm occlusionGood aneurysm occlusionGood aneurysm occlusion
Automated robotic functions successfully performedRoR, millimetric control, LS, ADF, Turbo speed RoR, millimetric control, LS, ADF, Turbo speed RoR, millimetric control, LS, ADF, Turbo speed
Safety concernsADF must be deactivated when removing wire when microcatheter is positioned inside aneurysm sacNoneNone
Cassette changes during op000
Manual conversionNoNoNo
Robotic system failureNoNoNo

ADF = Active Device Fixation; LS = Limited Speed; NA = not applicable; RoR = Rotate on Retract.

Clinical Cases

Between November 2019 and February 2020, we treated 6 patients (5 female) ranging from 63 to 84 years old. Patient and aneurysm characteristics and procedural data are described in Tables 2 and 3. We performed 4 stent-assisted coiling and 2 flow-diverting stent procedures. Radiographic images are provided in Fig. 5, and technical details for each procedure are summarized in Table 3. The mean fluoroscopy time of robotic intervention across all 6 cases was 62.4 ± 11.5 minutes.

TABLE 2.

Baseline and clinical characteristics in 6 patients with complex aneurysms who underwent robot-assisted treatment

CharacteristicCase No.
123456
SexFemaleMaleFemaleFemaleFemaleFemale
Age, yrs656484766363
AccessCFACFARACFACFACFA
Aneurysm locationBasilar (midsegment—sidewall)Basilar tipRt PCoA (previously ruptured, coiled, early recurrence)Rt PCoA (previously ruptured, coiled, early recurrence)BasilarParaclinoid ICA
Aneurysm height, mm6.86.57.36.25.37.9
Aneurysm width, mm11.06.914.45.36.77.7
Aneurysm neck, mm6.16.16.65.55.75.1
Dome-to-neck ratio (width/neck)1.81.12.21.01.21.5
Procedure Stent-assisted coilingStent-assisted coilingFlow-diverter insertionStent-assisted coilingStent-assisted coilingFlow-diverter insertion
Robotic time (intracranial procedure)1 hr 19 mins1 hr 32 mins2 hrs 14 mins52 mins1 hr 31 mins1 hr 1 min
Total procedure time2 hrs 23 mins2 hrs 1 min2 hrs 46 mins1 hr 23 mins2 hrs 57 mins1 hr 58 mins
Radiation (total DAP), mGycm225225616024935556069046225626148439
Total fluoroscopy time, mins82.055.683.918.690.544.0
Baseline mRS score113111

CFA = common femoral artery; DAP = dose area product; mRS = modified Rankin Scale; RA = radial artery.

TABLE 3.

Technical case details

VariableCase No.
123456
ProcedureStent-assisted coilingStent-assisted coilingFlow-diverter insertionStent-assisted coilingStent-assisted coilingFlow-diverter insertion
No. of coils146NA56NA
Stent typeNeuroform AtlasNeuroform AtlasSilk Vista BabyNeuroform AtlasNeuroform AtlasSurpass Evolve
Stent size, mm4.5 × 213 × 242.75 × 104.5 × 214 × 214.5 × 20
Stent positioningGoodGoodGoodGoodGoodGood
Stent appositionGoodGoodGoodGoodGoodGood
Final angiogramGood aneurysm occlusionGood aneurysm occlusionEarly stasis in aneurysm remnantEarly stasis in aneurysm remnantGood aneurysm occlusionGood aneurysm occlusion
Periprocedural complicationsNo thromboembolic complicationsNo thromboembolic complicationsNo thromboembolic complicationsNo thromboembolic complicationsNo thromboembolic complicationsNo thromboembolic complications
Cassette changes during op100001
Manual conversionNoNoNoNoNoNo
Robotic system failureNoNoNoNoNoNo
FIG. 5.
FIG. 5.

Radiographic imaging from procedures of clinical cases 1–6 (i.e., rows A–F). Column 1: 3D DSA demonstrating the aneurysm and proximal parent artery anatomy for each case. Column 2: DSA showing the working projection. Column 3: Perioperative unsubtracted DSA imaging showing the stent and/or coils in place. Column 4: Final subtracted DSA (rows A, B, and E) or VasoCT (rows C, D, and F) of final angiographic control showing complete aneurysm occlusion and patency of the stents. Aneurysm locations included basilar sidewall (A); basilar tip (B and E); PCoA (C and D); and supraclinoid (F).

The prespecified primary endpoint of technical success was met in all patients, with no periprocedural complications during navigation, vessel catheterization, or device deployment, and no conversions to a manual procedure. All patients were discharged within 24 to 48 hours after the procedure with no changes to baseline neurological status. We had to change robotic cassettes once each during procedures 1 and 6 due to possible hardware errors with the single-use cassettes. Total procedure times ranged from 1 to 3 hours, with the robot-assisted intracranial part of the procedure ranging between 52 and 134 minutes. In all cases, the robotic arm was compatible with the patient and angiographic setup. All team members described the communication between the bedside and operator teams as clear and efficient.

Discussion

This translational, benchtop-to-clinical study demonstrates the feasibility of using robotic assistance during neuroendovascular procedures. In a stepwise fashion, we assessed device compatibility, established a clinical workflow, defined various safety measures, planned and rehearsed clinical cases, established protocols for effective team communication, and defined safety measures for the automated robotic functions. We met our prespecified primary experimental and clinical endpoints by successfully performing a consecutive series of stent-assisted coiling and flow-diverting stent placements in 6 technically challenging neurointerventional cases, without requiring conversion to a manual case at any stage. The robotic system allowed the operator to safely perform the planned procedures away from the bedside without complications or safety concerns.

Regarding our impressions after becoming comfortable with the robotic system, we initially questioned whether the lack of haptic (physical, force-sensing) feedback, such as resistance that might be felt when delivering a coil under pressure, would present an obstacle during procedures. Empirically, we found that this was not a significant issue, instead finding that visual feedback ("snaking" of coils, microcatheter kickback) was more than sufficient to compensate for any lack of haptics. In this regard, it is worth noting that senior staff routinely evaluate the technical performance of junior staff or fellows by using only visual feedback during training procedures; thus, experienced interventionalists already rely on visual cues more than they might realize.

In our setup, the control console and robotic arm were connected directly instead of over a network, and we were therefore unable to evaluate the potential effect of communication network latency on the procedure. Other groups have reported that the delay threshold for perceptible operator latency (> 250 msec) is much higher than that provided by dedicated network connections,17 but this will be an area for further study as the field develops.

We were interested in assessing how the robotic system affected the precision and accuracy of our procedures. According to the manufacturer, the robotic system measures the linear position of joystick movements and the robotic drive, independent of the drive train in the cassette, with an error of less than or equal to ± (10% + 0.1) mm. Accuracy is within 3° for rotatory movements, and the movements of the drives in response to the 1-mm touchscreen movements are validated to an accuracy of 0.1 mm. Consistent with these parameters, our qualitative assessment was that the robotic system enhanced the precision of our procedures. The use of the robotic system allowed for stable device deployment, facilitating submillimetric precision particularly when deploying stents. We also found that procedure visualization was improved over manual bedside procedures, with widescreen monitors just a few inches away from the operator. We found that this decreased the cognitive load on the primary operator, potentially allowing for safer procedures.18,19

Physical demands on the primary operator were also reduced. This is important because there is already a shortage of physicians trained in endovascular stroke treatment,20 and the number of significant occupational health hazards associated with long-term work in an angiography suite further exacerbate workforce shortages. Studies have estimated the incidence of spinal problems in interventionalists ranges from 42% to 75%,21 and up to one-third of cases are serious enough to limit work.22 Other detrimental effects to interventionalists include potential radiation-induced illnesses, such as CNS malignancies.23

Adoption of the system did require some changes to staffing and workflow. For now, two physicians are required for safety. At bedside, a physician and a robotic system technologist need experience in manual procedures, although it is possible that, with experience, the dedicated bedside physician may be safely replaced with an on-call physician to manage emergencies, similar to the evolution of robot-assisted PCI safety procedures. Similarly, the primary operator will require extensive experience in planning and performing the robotic intervention, and may need to spend a small amount of additional training to familiarize themselves with reliance on visual inputs.

Notably, our average fluoroscopy time for robotic intervention for these cases was 62.4 ± 11.5 minutes. This is slightly longer than published median fluoroscopy times for stent-assisted coiling cases from various series, which range from 43.8 ± 5.5 minutes to 55 ± 31 minutes.24,25 We believe this case time will continue to shorten as the team becomes increasingly comfortable and efficient with the procedure.

The ability to perform remote surgery is not restricted to science fiction. As early as 2001, surgeons in New York performed a robot-assisted cholecystectomy on a patient who was physically located in Strasbourg, France.26 Longer-distance PCI is currently under active investigation.9–12,27 We are thus entering an era when robotic telestroke interventions represent a realistic possibility for the near future. Essential steps toward this reality include validation of the system’s procedure-specific safety, safety of the system over truly “remote” distances, and ultimately, efficacy of remote stroke procedures.

Although our discussion of the utility of remote, robot-assisted neuroendovascular procedures focuses on the treatment of ischemic stroke, in this study we have demonstrated the feasibility of aneurysm repair; therefore, remote treatment of hemorrhagic conditions is a use-case scenario that should also be discussed. The same geographical discrepancies that affect stroke care also exist in relation to endovascular aneurysm repair, and the majority of intracranial aneurysms—especially ruptured ones—are now treated by endovascular approaches.28

Of course, there are many questions to consider before adopting these procedures. For example, what will be the referral pathways for these patients? Should there be a neurosurgeon on site at the robotic center where patients are being treated, in case of complications? Where does remote robotic surgery fit into the care pathway for patients with subarachnoid hemorrhage, for whom a dedicated neuro-ICU and neurorehabilitation services are also crucial?

We look forward to helping answer these questions and many more as our experience with this system evolves. It should be noted that the cases we present here were all relatively complex, elective aneurysm treatments, which were successfully treated without complication using the first generation of the robotic system. It is thus very likely that comprehensive, remote, robot-assisted aneurysm repair will be a realistic possibility in the next decade, and that we should not confine our vision to ischemic stroke.

In summary, intrafacility, transnational, or even transoceanic procedures will truly represent a paradigm-changing event in stroke treatment.9–12,27 A patient’s geographical environment—in terms of physical proximity to resources, population density, and socioeconomic equity—would play a diminished role in dictating access to life-saving care. This could have a significant impact on patient outcomes, and will allow us to establish a truly remote, comprehensive, global stroke-care network in the future.

Limitations

Our study has a number of limitations. This is a single-center pilot study, and our center has been working closely with this robotic system for almost 2 years now. It is therefore as yet unclear how generalizable our technical results are to other centers. It is likely that robotic procedures will take longer than traditional endovascular procedures, especially in the early stages of its adoption. It is also likely that these procedures will be more expensive than traditional neuroendovascular procedures, given the costs associated with the system.

We focused on feasibility and safety of the robotic procedure and did not perform a direct comparison with manual procedures at this time. Furthermore, with safety as the top priority, we were limited in the physical distance we chose to put between operator and patient. Therefore, the feasibility of performing these procedures at longer physical distances is speculative at this time. Larger studies are warranted to confirm the reproducibility of our results and to understand the benefits and limitations of long-distance remote procedures.

With respect to limitations of the robotic system, it should be noted that the current generation has several technical limitations that should be taken into consideration for surgical planning, and that will probably have to be addressed before its full potential for remote surgery performed at long distances can be realized. These limitations include limited compatibility with some current-generation guide catheters, guidewires, and devices; the ability to manage a total of only one microcatheter and one microwire or device at a time; and the requirement that DACs be placed manually. Future generations of the robotic system are expected to overcome these issues.

Conclusions

We have demonstrated the feasibility of robot-assisted neuroendovascular procedures in a clinical case series. This study represents a critical first step toward the eventual realization of truly remote telestroke interventional procedures.

Acknowledgments

Jeanne McAdara, PhD, provided professional medical editing assistance, which was funded by Corindus.

Disclosures

Dr. Mendes Pereira has previously served on the steering committee for Corindus. This work was funded by institutional resources. Corindus provided funds for a medical editor to assist with manuscript preparation and coordination of author feedback. Single-patient-use cassettes were provided by Corindus.

Author Contributions

Conception and design: Mendes Pereira. Acquisition of data: all authors. Analysis and interpretation of data: Mendes Pereira. Drafting the article: Mendes Pereira, Nicholson, Cancelliere, Agid, Radovanovic, Krings. Critically revising the article: Mendes Pereira. Approved the final version of the manuscript on behalf of all authors: Mendes Pereira.

Supplemental Information

Online-Only Content

Supplemental material is available with the online version of the article.

References

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    • Crossref
    • PubMed
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    • Export Citation
  • 2

    Goyal M, Menon BK, van Zwam WH, et al. Endovascular thrombectomy after large-vessel ischaemic stroke: a meta-analysis of individual patient data from five randomised trials. Lancet. 2016;387(10029):17231731.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Lawton MT, Vates GE. Subarachnoid hemorrhage. N Engl J Med. 2017;377(3):257266.

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    Molyneux A, Kerr R, Stratton I, et al. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet. 2002;360(9342):12671274.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Molyneux AJ, Kerr RS, Yu LM, et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet. 2005;366(9488):809817.

    • PubMed
    • Search Google Scholar
    • Export Citation
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    Adeoye O, Albright KC, Carr BG, et al. Geographic access to acute stroke care in the United States. Stroke. 2014;45(10):30193024.

  • 7

    Smitson CC, Ang L, Pourdjabbar A, et al. Safety and feasibility of a novel, second-generation robotic-assisted system for percutaneous coronary intervention: first-in-human report. J Invasive Cardiol. 2018;30(4):152156.

    • PubMed
    • Search Google Scholar
    • Export Citation
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    Weisz G, Metzger DC, Caputo RP, et al. Safety and feasibility of robotic percutaneous coronary intervention: PRECISE (Percutaneous Robotically-Enhanced Coronary Intervention) Study. J Am Coll Cardiol. 2013;61(15):15961600.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Madder RD, VanOosterhout SM, Jacoby ME, et al. Percutaneous coronary intervention using a combination of robotics and telecommunications by an operator in a separate physical location from the patient: an early exploration into the feasibility of telestenting (the REMOTE-PCI study). EuroIntervention. 2017;12(13):15691576.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Madder RD, VanOosterhout S, Mulder A, et al. Feasibility of robotic telestenting over long geographic distances: a pre-clinical ex vivo and in vivo study. EuroIntervention. 2019;15(6):e510e512.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Madder RD, VanOosterhout S, Parker J, et al. Robotic telestenting performance in transcontinental and regional pre-clinical models. Catheter Cardiovasc Interv. 2021;97(3):E327E332.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Patel TM, Shah SC, Pancholy SB. Long distance tele-robotic-assisted percutaneous coronary intervention: a report of first-in-human experience. EClinicalMedicine. 2019;14:5358.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Britz GW, Panesar SS, Falb P, et al. Neuroendovascular-specific engineering modifications to the CorPath GRX Robotic System. J Neurosurg. 2020;133(6):18301836.

  • 14

    Britz GW, Tomas J, Lumsden A. Feasibility of robotic-assisted neurovascular interventions: initial experience in flow model and porcine model. Neurosurgery. 2020;86(2):309314.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Al Nooryani A, Aboushokka W. Rotate-on-retract procedural automation for robotic-assisted percutaneous coronary intervention: first clinical experience. Case Rep Cardiol. 2018;2018:6086034.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Hunt EA, Shilkofski NA, Stavroudis TA, Nelson KL. Simulation: translation to improved team performance. Anesthesiol Clin. 2007;25(2):301319.

  • 17

    Madder RD, VanOosterhout S, Mulder A, et al. Network latency and long-distance robotic telestenting: Exploring the potential impact of network delays on telestenting performance. Catheter Cardiovasc Interv. 2020;95(5):914919.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Dalsgaard T, Jensen MD, Hartwell D, et al. Robotic surgery is less physically demanding than laparoscopic surgery: paired cross sectional study. Ann Surg. 2020;271(1):106113.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Lee GI, Lee MR, Clanton T, et al. Comparative assessment of physical and cognitive ergonomics associated with robotic and traditional laparoscopic surgeries. Surg Endosc. 2014;28(2):456465.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Cloft H. Workforce needs for endovascular acute ischemic stroke therapy: myth or reality? Neurosurg Focus. 2014;36(1):E8.

  • 21

    Ross AM, Segal J, Borenstein D, et al. Prevalence of spinal disc disease among interventional cardiologists. Am J Cardiol. 1997;79(1):6870.

  • 22

    Goldstein JA, Balter S, Cowley M, et al. Occupational hazards of interventional cardiologists: prevalence of orthopedic health problems in contemporary practice. Catheter Cardiovasc Interv. 2004;63(4):407411.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Carozza SE, Wrensch M, Miike R, et al. Occupation and adult gliomas. Am J Epidemiol. 2000;152(9):838846.

  • 24

    Chalouhi N, McMahon JF, Moukarzel LA, et al. Flow diversion versus traditional aneurysm embolization strategies: analysis of fluoroscopy and procedure times. J Neurointerv Surg. 2014;6(4):291295.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Cheung NK, Boutchard M, Carr MW, Froelich JJ. Radiation exposure, and procedure and fluoroscopy times in endovascular treatment of intracranial aneurysms: a methodological comparison. J Neurointerv Surg. 2018;10(9):902906.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Marescaux J, Leroy J, Rubino F, et al. Transcontinental robot-assisted remote telesurgery: feasibility and potential applications. Ann Surg. 2002;235(4):487492.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Smilowitz NR, Moses JW, Sosa FA, et al. Robotic-enhanced PCI compared to the traditional manual approach. J Invasive Cardiol. 2014;26(7):318321.

  • 28

    Etminan N, Rinkel GJ. Unruptured intracranial aneurysms: development, rupture and preventive management. Nat Rev Neurol. 2016;12(12):699713.

  • Collapse
  • Expand

Illustration from Zipfel (937–938). Copyright Gregory J. Zipfel. Published with permission.

  • FIG. 1.

    General room (upper) and catheter stack (lower) setup for robot-assisted procedures. Note: CoPilot Y-Connectors are required for optimal compatibility with the robotic drive. Slack in the catheter stack should be minimized; sterile towels can be used for support.

  • FIG. 2.

    Outline of our translational benchtop-to-clinical approach demonstrating the feasibility of robotic assistance during endovascular neurointerventional procedures, highlighting the goals and endpoints of each phase. A total of 235 experiments were performed using a variety of access devices and intracranial implant devices in 12 in vitro silicone aneurysm models from our cataloged library. Refer to Supplemental Table S1 for the complete list of devices and compatibility.

  • FIG. 3.

    Case 2. Perioperative robotic maneuvers used in different steps of the case—stent-assisted coiling of a basilar tip aneurysm (also illustrated in Fig. 5B). Row 1: Digital subtraction angiography (DSA) roadmap images from different steps of the procedure. Row 2: Superior view of the robotic console in the cockpit and an illustration of the operator’s hands operating the joysticks and different commands. Column 1: Vessel catheterization (right VA injection roadmap)—microcatheter (orange arrow) navigation with the aid of the microwire (green arrow). We demonstrate the function “Rotate on Retract” that is an automated function on the microwire. Column 2: Deployment of the distal end of the stent (upper red arrow pointing to 3 dark markers) using millimetric control, demonstrated by the hands on the touchscreen console. Orange arrow shows the microcatheter tip marker mid-deployment, with the proximal marker of the stent (lower red arrow) still inside the microcatheter. Column 3: Final stent deployment shows microcatheter tip (orange arrow) pulled back more proximally now, closer to the proximal marker of the stent (lower red arrow), performed using the joystick controls under the “Limited Speed” function. Column 4: Entering back into the lumen of the stent with the microcatheter is performed using the robotic function “Active Device Fixation,” which functions to automatically match the distance of the forward movement of the microcatheter (orange arrow) with equal retraction of the stent wire (distal red arrow), much like a manual “pinning the wire” technique, but performed with only 1 joystick.

  • FIG. 4.

    Select in vitro experiments in patient-specific aneurysm models. A: Stent-assisted coiling of a basilar aneurysm model (patient-specific to clinical case 2). B: Flow-diverting stent treatment of an ICA aneurysm model. C: Flow-diverting stent treatment of an MCA bifurcation aneurysm model. Column 1: Pictures of the physical model. Column 2: A 3D (row A only) or 2D endoluminal image of the model. Column 3: Subtracted (row A only) or unsubtracted images showing the devices midtreatment. Column 4: Unsubtracted (row B only) or subtracted images demonstrating final device apposition.

  • FIG. 5.

    Radiographic imaging from procedures of clinical cases 1–6 (i.e., rows A–F). Column 1: 3D DSA demonstrating the aneurysm and proximal parent artery anatomy for each case. Column 2: DSA showing the working projection. Column 3: Perioperative unsubtracted DSA imaging showing the stent and/or coils in place. Column 4: Final subtracted DSA (rows A, B, and E) or VasoCT (rows C, D, and F) of final angiographic control showing complete aneurysm occlusion and patency of the stents. Aneurysm locations included basilar sidewall (A); basilar tip (B and E); PCoA (C and D); and supraclinoid (F).

  • 1

    Emberson J, Lees KR, Lyden P, et al. Effect of treatment delay, age, and stroke severity on the effects of intravenous thrombolysis with alteplase for acute ischaemic stroke: a meta-analysis of individual patient data from randomised trials. Lancet. 2014;384(9958):19291935.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Goyal M, Menon BK, van Zwam WH, et al. Endovascular thrombectomy after large-vessel ischaemic stroke: a meta-analysis of individual patient data from five randomised trials. Lancet. 2016;387(10029):17231731.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Lawton MT, Vates GE. Subarachnoid hemorrhage. N Engl J Med. 2017;377(3):257266.

  • 4

    Molyneux A, Kerr R, Stratton I, et al. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet. 2002;360(9342):12671274.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Molyneux AJ, Kerr RS, Yu LM, et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet. 2005;366(9488):809817.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Adeoye O, Albright KC, Carr BG, et al. Geographic access to acute stroke care in the United States. Stroke. 2014;45(10):30193024.

  • 7

    Smitson CC, Ang L, Pourdjabbar A, et al. Safety and feasibility of a novel, second-generation robotic-assisted system for percutaneous coronary intervention: first-in-human report. J Invasive Cardiol. 2018;30(4):152156.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Weisz G, Metzger DC, Caputo RP, et al. Safety and feasibility of robotic percutaneous coronary intervention: PRECISE (Percutaneous Robotically-Enhanced Coronary Intervention) Study. J Am Coll Cardiol. 2013;61(15):15961600.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Madder RD, VanOosterhout SM, Jacoby ME, et al. Percutaneous coronary intervention using a combination of robotics and telecommunications by an operator in a separate physical location from the patient: an early exploration into the feasibility of telestenting (the REMOTE-PCI study). EuroIntervention. 2017;12(13):15691576.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Madder RD, VanOosterhout S, Mulder A, et al. Feasibility of robotic telestenting over long geographic distances: a pre-clinical ex vivo and in vivo study. EuroIntervention. 2019;15(6):e510e512.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Madder RD, VanOosterhout S, Parker J, et al. Robotic telestenting performance in transcontinental and regional pre-clinical models. Catheter Cardiovasc Interv. 2021;97(3):E327E332.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Patel TM, Shah SC, Pancholy SB. Long distance tele-robotic-assisted percutaneous coronary intervention: a report of first-in-human experience. EClinicalMedicine. 2019;14:5358.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Britz GW, Panesar SS, Falb P, et al. Neuroendovascular-specific engineering modifications to the CorPath GRX Robotic System. J Neurosurg. 2020;133(6):18301836.

  • 14

    Britz GW, Tomas J, Lumsden A. Feasibility of robotic-assisted neurovascular interventions: initial experience in flow model and porcine model. Neurosurgery. 2020;86(2):309314.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Al Nooryani A, Aboushokka W. Rotate-on-retract procedural automation for robotic-assisted percutaneous coronary intervention: first clinical experience. Case Rep Cardiol. 2018;2018:6086034.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Hunt EA, Shilkofski NA, Stavroudis TA, Nelson KL. Simulation: translation to improved team performance. Anesthesiol Clin. 2007;25(2):301319.

  • 17

    Madder RD, VanOosterhout S, Mulder A, et al. Network latency and long-distance robotic telestenting: Exploring the potential impact of network delays on telestenting performance. Catheter Cardiovasc Interv. 2020;95(5):914919.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Dalsgaard T, Jensen MD, Hartwell D, et al. Robotic surgery is less physically demanding than laparoscopic surgery: paired cross sectional study. Ann Surg. 2020;271(1):106113.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Lee GI, Lee MR, Clanton T, et al. Comparative assessment of physical and cognitive ergonomics associated with robotic and traditional laparoscopic surgeries. Surg Endosc. 2014;28(2):456465.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Cloft H. Workforce needs for endovascular acute ischemic stroke therapy: myth or reality? Neurosurg Focus. 2014;36(1):E8.

  • 21

    Ross AM, Segal J, Borenstein D, et al. Prevalence of spinal disc disease among interventional cardiologists. Am J Cardiol. 1997;79(1):6870.

  • 22

    Goldstein JA, Balter S, Cowley M, et al. Occupational hazards of interventional cardiologists: prevalence of orthopedic health problems in contemporary practice. Catheter Cardiovasc Interv. 2004;63(4):407411.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Carozza SE, Wrensch M, Miike R, et al. Occupation and adult gliomas. Am J Epidemiol. 2000;152(9):838846.

  • 24

    Chalouhi N, McMahon JF, Moukarzel LA, et al. Flow diversion versus traditional aneurysm embolization strategies: analysis of fluoroscopy and procedure times. J Neurointerv Surg. 2014;6(4):291295.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Cheung NK, Boutchard M, Carr MW, Froelich JJ. Radiation exposure, and procedure and fluoroscopy times in endovascular treatment of intracranial aneurysms: a methodological comparison. J Neurointerv Surg. 2018;10(9):902906.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Marescaux J, Leroy J, Rubino F, et al. Transcontinental robot-assisted remote telesurgery: feasibility and potential applications. Ann Surg. 2002;235(4):487492.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Smilowitz NR, Moses JW, Sosa FA, et al. Robotic-enhanced PCI compared to the traditional manual approach. J Invasive Cardiol. 2014;26(7):318321.

  • 28

    Etminan N, Rinkel GJ. Unruptured intracranial aneurysms: development, rupture and preventive management. Nat Rev Neurol. 2016;12(12):699713.

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