Abstract
Introduction
Maximal extent of resection (EOR) of glioblastoma (GBM) is associated with greater progression free survival (PFS) and improved patient outcomes. Recently, a novel surgical system has been developed that includes a 2D, robotically-controlled exoscope and brain tractography display. The purpose of this study was to assess outcomes in a series of patients with GBM undergoing resections using this surgical exoscope.
Methods
A retrospective review was conducted for robotic exoscope assisted GBM resections between 2017 and 2019. EOR was computed from volumetric analyses of pre- and post-operative MRIs. Demographics, pathology/MGMT status, imaging, treatment, and outcomes data were collected. The relationship between these perioperative variables and discharge disposition as well as progression-free survival (PFS) was explored.
Results
A total of 26 patients with GBM (median age = 57 years) met inclusion criteria, comprising a total of 28 cases. Of these, 22 (79%) tumors were in eloquent regions, most commonly in the frontal lobe (14 cases, 50%). The median pre- and post-operative volumes were 24.0 cc and 1.3 cc, respectively. The median extent of resection for the cohort was 94.8%, with 86% achieving 6-month PFS. The most common neurological complication was a motor deficit followed by sensory loss, while 8 patients (29%) were symptom-free.
Conclusions
The robotic exoscope is safe and effective for patients undergoing GBM surgery, with a majority achieving large-volume resections. These patients experienced complication profiles similar to those undergoing treatment with the traditional microscope. Further studies are needed to assess direct comparisons between exoscope and microscope-assisted GBM resection.
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Introduction
Glioblastoma (GBM) is known to be one of the most aggressive brain tumors, with a median survival time of 12–15 months [1, 2]. Surgical resection remains the first-line treatment for GBM [3], followed by fractionated radiotherapy with concurrent and adjuvant temozolomide (TMZ) [1]. Despite first-line treatment, the median time to GBM tumor recurrence is approximately 8 months [4]. Prognostic factors include extent of tumor resection (EOR), age, Karnofsky performance status (KPS), and MGMT methylation [5]. While residual, infiltrating tumor cells nearly always remain, greater GBM EOR is one of the few modifiable variables, and has been associated with superior progression free survival (PFS) as well as other patient outcomes [6,7,8,9]. Recurrence rates have been shown to be decreased at EORs > 78%, with incremental improvements at larger values [10, 11]. Meanwhile, gross total resection (GTR) has demonstrated an increase in median overall survival (OS) by up to 5 months [6].The most common reasons for subtotal resection include large tumor size, eloquent location (involving or displacing motor, language, or visual pathways), and the inability to adequately differentiate tumor from normal brain parenchyma during surgery [10, 12,13,14].
Inadequate visualization of GBM lesions can result from homogenous texture and color under white light, along with extensive infiltration into the surrounding brain. In response to this, an array of novel technologies has been developed to improve the ability to delineate neoplastic tissue from surrounding brain [15,16,17,18,19]. While the conventional binocular microscope has proven invaluable in achieving intraoperative magnification during cranial surgery, the introduction of the digital surgical microscope, also known as an exoscope, may provide additional advantages. This device consists of a high-definition rigid rod lens telescope that rests suspended above the surgical field and has the potential to offer high magnification, illumination, and clarity of tissues [20,21,22], thus potentially enhancing GBM visualization during surgery [23, 24].
In comparison to the conventional microscope, the exoscope can provide up to double the magnification (×12.5 versus ×6 optical zoom). A panoramic, larger field of view that is also double the conventional microscope is possible with the exoscope. The exoscope utilizes light-emitting diode (LED) lighting which permits illumination of the surgical field at lower light intensity with less glare in comparison to the conventional microscope which relies on xenon lighting at higher intensities. Lower light intensity, a larger field of view, greater magnification, and greater clarity may permit better delineation of tumor tissue from surrounding brain tissue during tumor resections. In addition, this 2D exoscope is coupled with a robotically-controlled arm that tracks surgical instruments, allowing for hands-free camera movement during operations (Modus V™, Synaptive Medical, Toronto, Canada) [24]. The improved degrees of freedom of a robotically-controlled exoscope enables visualization of deeper resection cavities and angles that can be difficult to visualize using traditional methods. Utilizing the high definition heads-up display, the surgeon and operative team can all be engaged during the surgery. In addition to the exoscope visualization system, whole brain tractography (BrightMatter Servo™, Synaptive Medical, Toronto, Canada) integrated with neuronavigation can be utilized during resection in order to help navigate and preserve crucial eloquent pathways [25, 26].
While the current literature provides qualitative case reports regarding the initial surgical experience using the robotic digital exoscope solely, no study to date has assessed the clinical, postoperative outcomes and complications for these patients [24, 25]. As such, the purpose of this study is to (a) perform high-fidelity volumetric analyses in order to quantify the EOR and (b) describe the post-operative complications, discharge disposition, and progression free survival (PFS) for a case series of patients undergoing GBM resection using the automated, robotic digital exoscope.
Methods
Participants
A single-center retrospective review was conducted at an academic, quaternary care center under Institutional Review Board (IRB) approval. Consent was waived and not feasible since patient records were reviewed following the date of surgery. Data were obtained from all adult patients (age > 18 years) diagnosed with glioblastoma (GBM) who underwent tumor resection using the robotic exoscope system between September 2017 and December 2019. Demographic, histologic, imaging, treatment, and outcomes data were extracted from Epic-based electronic medical records. All data were kept secure using Research Electronic Data Capture (REDCap, Vanderbilt University, Nashville, Tennessee) and subsequently exported for analysis.
Robot-assisted digital surgical exoscope
The Synaptive Modus V™ (Synaptive Medical, Toronto, Canada) is a fully automated, digital exoscope with a robotically-controlled arm that adjusts its angle relative to the movement of the operative instruments, whose position can be integrated into neuronavigation systems. Real-time images are displayed on a high-definition monitor. MRI-based neuronavigation that incorporated whole-brain 3D Diffusion Tensor Imaging (DTI) (BrightMatter Guide™) and fiber tractography was employed in the resection of each tumor. Figures 1 and 2 show the localization of the tumor using the navigation tools and how the trajectory relates to tracts as seen on the DTI heads-up display. The digital surgical exoscope was utilized for the entire surgical resection of tumors by the senior neurosurgeon for all cases in order to reduce intraoperative variability. The intraoperative experience using the microscope was noted by the senior neurosurgeon. The conventional binocular surgical microscope was not used for any portion of each surgery. Preparation time was defined as the duration between “ready time” after correct positioning and intubation, to the time of first incision. Patients undergoing fluorescence-guided surgery using 5-aminolevulinic acid (5-ALA) were excluded, as this occurs using the microscope following exoscope-assisted resection and is known to be associated with increased EOR and consequent PFS-6 [27].
Tumor Characteristics
An array of tumor characteristics, including anatomic location, proximity to key structures, and immunohistologic properties were examined. Lesions were deemed to be eloquent if the tumor location was directly adjacent to, or involving language, motor, visual, and somatosensory pathways. Cortical and subcortical motor mapping was performed in 15 cases using high frequency monopolar stimulation for the localization of eloquent cortical and subcortical structures. Immunohistochemistry analyses in the pathology reports were used to determine MGMT promoter methylation status, EGFR amplification, and mutations in isocitrate dehydrogenase (IDH1/2) and p53.
Volumetric analysis
MRI scans were obtained pre- and post-operatively (within 48 h of resection) for all patients. The Olea Sphere 3.0.18 segmenting software was used to compute tumor volumes. Gadolinium-enhancing tumor volume was visible as areas of increased signal intensity on T1-weighted MR images [10]. Segmentation was validated by a board-certified neuroradiologist. EOR was quantified using computer-assisted volumetric analysis where tumor-specific voxels are manually delineated on MRI slices [10, 28]. EOR was computed using the formula [(PTV-RTV/PTV)] × 100%, where PTV is preoperative tumor volume and RTV is residual tumor volume. A “large” EOR was defined as exceeding 78% of tumor volume removal, as this threshold has been demonstrated to be associated with prolonged survival following resection [11].
Postoperative complication profile
A chart review was conducted to calculate the follow-up time from resection to a neurooncological visit. Post-operative complications were ascertained by the neuro-oncology team within a month following resection and prior to the initiation of fractionated external beam radiotherapy and concurrent temozolomide (TMZ) treatment. These included neurologic complications, such as speech impairment, motor deficits, sensory loss, and visual defects. Other adverse events included fatigue, psychological symptoms of anxiety/depression, and headache. Discharge disposition, consisting of home discharge, medical/surgical rehabilitation, or a skilled nursing facility (SNF) was collected for each patient. Total hospital length of stay (LOS) and all postoperative therapies were recorded. Patients were reviewed for GBM recurrence on follow-up MRI in order to determine PFS at 6 months following resection.
Statistical analysis
An array of statistical tests were employed, including descriptive tests, bivariate analyses, and multivariable regression modeling. Continuous variables were represented as means and standard deviations if normally distributed and by median and interquartile range if non-parametric. Categorical variables were described using frequencies and proportions for descriptive purposes. Two binary multivariable regression models were constructed to explore the relationship between perioperative factors and the clinical outcomes of interest: PFS-6 and non-routine discharge disposition. Bivariate statistics, including Chi-squared or Fisher’s exact tests for categorical variables as well as univariable logistic regression for continuous ones, were employed to select potential predictors for inclusion into the regression models. Factors resulting in P < 0.2 with the outcome of interest were subsequently incorporated into the binary logistic regression. Post-regression diagnostics, including area under the curve (AUC) as well as the Homer–Lemeshow test were employed to assess the predictive capacity and goodness-of-fit of the models, respectively. All tests were two-tailed and P < 0.05 was selected a priori as the threshold for statistical significance. All analyses were conducted using R 3.5.2 (R Foundation for Statistical Computing, Vienna, Austria).
Results
Demographic and tumor-related characteristics
Patient demographics and tumor characteristics are presented in Table 1. A total of 26 patients (16 males and 10 females) with GBM and a median age of 57 years (range 28–74) met our inclusion criteria, comprising a total of 28 cases. Of these, 22 (79%) were in eloquent regions and the most common anatomic location was the frontal lobe in 14 cases (50%). A total of 26 patients underwent initial resection of their newly diagnosed GBM tumor. Two of these patients underwent re-resection of their tumor at recurrence. A majority of tumors (61%) were MGMT-unmethylated.
Tumor volumes and extent of resection
Tumor volumes, extent of resection data, and timing are reported in Table 2. The median pre- and post-operative volumes were 24.0 cc (range 0.6–61.2 cc) and 1.3 cc (range 0–11.3 cc), respectively. The median extent of resection was 94.8% (range: 61.8–100%). A large EOR was achieved in 86% of cases and the mean operative time was 221 (± 72) min.
Intraoperative experience
The use of whole brain tractography for motor pathway identification was reliably used during surgery in all cases where eloquent pathways were present. However, since DTI relies on neuronavigation, there is no question that brain shift during surgery could account for inaccuracies in localization of important motor pathways. The combination of whole brain tractography and intraoperative cortical/subcortical motor mapping permitted reliable identification of eloquent motor pathways during tumor resections with the exoscope. This combination approach ensured optimal localization of the surrounding motor pathways for preservation during surgery. High magnification (up to ×12.5) and tissue clarity was possible with the exoscope at low light intensity (15–30%) in all tumor resections and permitted visualization of the infiltrative tumor margin during surgery. The seamless motion of the robotic arm as it calibrated to the surgical instruments enabled a hands-free view of the surgical field at different angles. Figure 3 captures the intraoperative display of the tumor versus surrounding brain tissue, including a visualization of the infiltrative zone. As a final note, the heads-up display allowed for surgeon comfort with reduced neck strain during lengthy surgeries and engagement of the surgical team.
Hemostasis
In our series of patients where the exoscope was used for the entire surgical resection of GBM tumors, we had no reoperations for any postoperative hematomas. We strongly believe that the larger field of view, high magnification, and excellent clarity afforded from visualization of the resection cavity with the exoscope resulted in optimal tissue hemostasis. The mean estimated blood loss (EBL) reported for these cases was 219.6 (± 113.6) mL (Table 2).
Postoperative outcomes
Post-operative complications obtained at 1-month following resection are reported in Table 3. The median follow-up time with a neurooncologist following the resection was 19 days. The most common neurological complication was a temporary motor deficit followed by sensory loss, while eight patients (29%) were symptom-free and had no abnormal findings on neurologic exam. Almost all of the resections (27) were followed by a Stupp regimen that included adjuvant fractionated radiotherapy and adjuvant temozolomide (TMZ), with one patient refusing care. Three patients elected to use the Optune® (Novocure) device and five patients were placed on immunotherapies (Avelumab or Nivolumab). Three patients in this series had resections for tumor recurrence, two of which had GBM recurrence after their initial exoscope resection.
The mean hospital LOS was 6.7 days and the majority of patients (61%) were discharged home. Patients survived to 6 months without progression in 24 (86%) of cases. In the 4 cases that did progress at 6 months, the median time to disease progression was 3.5 months. None (0%) of the patients included in this study were deceased after 6 months (Table 3).
Predictors of postoperative outcomes
Two binary logistic regression models were constructed to explore the relationship between various perioperative variables and the primary outcomes of interest. Large (> 78%) EOR did not result in a statistically significant decrease in 6-month progression free survival (OR 0.04; 95% CI 0.001–1.93; P = 0.10). Prolonged hospital LOS trended towards a decreased rate of home discharge relative to other dispositions (OR 0.49; 95% CI 0.21–1.10; P = 0.09). All of the examined variables are presented in Table 4. The models demonstrated excellent predictive capacity, with AUCs of 0.875 and 0.938, respectively. Goodness-of-fit testing was non-significant, indicating that the selected models were appropriate to the data.
Discussion
The fundamental goal of operative brain tumor treatment is achieving the greatest EOR while preserving the maximum amount of function. Achieving this necessitates accurate differentiation between neoplastic tissue and surrounding brain parenchyma. The robotic-augmented exoscope was developed with the aim of providing superior resolution of anatomic structures, while improving surgeon comfort throughout the procedure. These data demonstrate that the use of this technology is both safe and effective in the surgical treatment of GBM, with complication profiles and outcomes similar to using the operative microscope.
Over the past century, there have been tremendous advances in the technologies used to visualize target tissue during surgery. In the 1950s, otolaryngologists were the first surgeons to utilize the operative microscope for middle ear surgery with the Littman, Zeiss OpMi 1 (Operating Microscope Number 1, ZEISS, Oberkochen, Germany). in 1953 [29]. Several years later, Theodore Kurze became the first neurosurgeon to employ the microscope in the operating room at the University of Southern California [30]. In the 1960s, Kurze would then go on to found the first microneurosurgical skull base laboratory, paving the field for the next generation of leaders including Drs. Drake, Donaghy and Yasargil [31].
During the ensuing three decades, multiple different operative microscopes have been introduced and modified resulting in augmented zoom/focus functions, creation of a rotary device, and the addition of an observer scope. Over the past 20 years, fluorescent-light emission at different wavelengths of light from the operative microscope have permitted neurosurgeons to visualize high-gliomas during FGS in patients who have been administered 5-ALA or fluorescein [18, 32,33,34]. These novel visualization methods have been incorporated into neurosurgical practice in order to increase the EOR of malignant brain tumors. Since its original inception, the operative microscope has been the sole option for microneurosurgery. However, this has recently changed with the introduction of the exoscope. Developed initially by Karl Storz (Tuttlingen, Germany), the high-definition exoscope permits long working distances and a wide visual perspective. Consisting of a telescope attached to a digital camera, the device produces high-quality, magnified images that are projected onto a screen in front of the surgeon. The new generation of this technology is represented by the Synaptive Modus V™ (Synaptive Medical, Toronto, Canada), which is comprised of an automated, digital microscope with a robotically-controlled arm that facilitates the use of neuronavigation with DTI.
The data presented in this study highlights that using this exoscope in the operative treatment of GBM resulted in excellent short-term surgical results, with a median EOR of 95%. This is in line with the majority of studies reporting outcomes following resection using a traditional microscope. Li et al. analyzed data for one of the largest series of GBM patients in the literature, with 1229 microscopic resections. The authors reported that while GTR was achieved in 71% of patients, between 78 and 99% volume resection was achieved in 29% of patients [14]. Similarly, Laurent et al. described a series of 284 patients with supratentorial GBM lesions, highlighting a mean EOR of 95.7% [35]. Further, high magnification of the exoscope allowed for visualization of the tumor and surrounding blood vessels, thus improving tissue hemostasis. While tumor variables often affect EBL, the results of this paper show less intraoperative blood loss when compared to results published by Abecassis et al. [36].
The most common short-term postoperative complications in our series included neurologic deficits, such as impairments in motor (25%) or sensory (14%) function, while 11 patients (39%) had no functional neurologic deficits (Table 3). This favorable complication profile is consistent with the established literature on microscopic GBM resection. Karsy et al. analyzed the adverse events for 82 elderly patients following surgery, reporting an overall complication rate of 31.9% [37]. The common frequent adverse event was a neurologic deficit in 29.4%, followed by hemorrhage (11.8%), and uncontrolled pain or headache (8.8%). In addition, the mean LOS was 7 ± 6 days, compared to 6.7 days in our series. Similarly, Li et al. reported a 30-day complication rate of 227 (18%), with the most common deficit being motor dysfunction in 9%, followed by speech impairment (6%), and visual loss (3%) [14]. Overall, the postoperative complications following exoscope-guided resection are similar in incidence and distribution to those occurring after microscopic surgery.
In our series, large (> 78%) EOR trended towards a significantly decreased rate of disease progression at 6 months. The lack of statistical significance is likely due to inadequate power in this pilot study, where a small number of resections have been performed using this new technology. However, this relationship has been demonstrated throughout the literature on GBM surgery. Sanai et al. analyzed data for 500 consecutive, newly diagnosed GBM patients undergoing microscopic resection [11]. The authors reported a median EOR of 96% and OS of 12.2 months, highlighting that a significant survival advantage was achieved with as little as 78% EOR. Numerous other studies have described a significant relationship between increased EOR and subsequent PFS and OS [6, 13, 38]. In addition, prolonged hospital LOS trended towards a significantly decreased rate of home discharge for this cohort. This association has been described in a number of studies on brain tumor patients, highlighting a significant relationship between LOS and non-routine discharge disposition [39, 40].
Limitations
These results must be interpreted in the context of limitations in study design. Given that this analysis is retrospective in nature, it is subject to numerous sources of systematic error such as selection bias and residual confounding. As a single-institution study, these results may not be generalizable on a national level due to differences in patient characteristics and hospital resources. We also acknowledge that the limited number of participants in the study or the lack of a control group at this time, are limitations and further study is necessary to compare the Synaptive system to the conventional microscope during GBM resections. Due to the novelty of the robotic surgical exoscope device, only a small number of cases have been performed. As such, this represents a preliminary, pilot study describing the surgical outcomes and complications following its use in resection. However, the analyses are likely underpowered to detect a significant relationship between EOR and PFS.
Conclusions
We report the surgical and short-term postoperative outcomes following the use of a novel robotic exoscope in the resection of GBM. Overall, patients experienced large volumes of tumor removal and substantial rates of progression-free survival at 6 months. Complication profiles after resection were comparable in both incidence and distribution to microscopic GBM surgery. Increased EOR trended towards significance with PFS at 6 months. As such, use of the robotic exoscope is safe and effective for patients with GBM. However, further studies are needed to assess direct comparisons between exoscope and microscope-assisted tumor resection.
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Constantinos Hadjipanayis is a consultant for NX Development Corp. (NXDC) and Synaptive Medical Inc. He receives royalties from NXDC.
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Baron, R.B., Lakomkin, N., Schupper, A.J. et al. Postoperative outcomes following glioblastoma resection using a robot-assisted digital surgical exoscope: a case series. J Neurooncol 148, 519–527 (2020). https://doi.org/10.1007/s11060-020-03543-3
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DOI: https://doi.org/10.1007/s11060-020-03543-3