Brain Shift and Pneumocephalus Assessment During Frame-Based Deep Brain Stimulation Implantation With Intraoperative Magnetic Resonance Imaging

Brain Shift and Pneumocephalus Assessment During Frame-Based Deep Brain Stimulation Implantation... Abstract BACKGROUND Brain shift and pneumocephalus are major concerns regarding deep brain stimulation (DBS). OBJECTIVE To report the extent of brain shift in deep structures and pneumocephalus in intraoperative magnetic resonance imaging (MRI). METHODS Twenty patients underwent bilateral DBS implantation in an MRI suite. Volume of pneumocephalus, duration of procedure, and 6 anatomic landmarks (anterior commissure, posterior commissure, right fornix [RF], left fornix [LF], right putaminal point, and left putaminal point) were measured. RESULTS Pneumocephalus varied from 0 to 32 mL (median = 0.6 mL). Duration of the procedure was on average 195.5 min (118-268 min) and was not correlated with the amount of pneumocephalus. There was a significant posterior displacement of the anterior commissure (mean = −1.1 mm, P < .001), RF (mean = −0.6 mm, P < .001), LF (mean = −0.7 mm, P < .001), right putaminal point (mean = −0.9 mm, P = .001), and left putaminal point (mean = −1.0 mm, P = .001), but not of the posterior commissure (mean = 0.0 mm, P = .85). Both RF (mean = −.7 mm, P < .001) and LF (mean = −0.5 mm, P < .001) were posteriorly displaced after a right-sided burr hole. There was a correlation between anatomic landmarks displacement and pneumocephalus after 2 burr holes (rho = 0.61, P = .007), but not after 1 burr hole (rho = 0.16, P = .60). CONCLUSION Better understanding of how pneumocephalus displaces subcortical structures can significantly enhance our intraoperative decision making and overall targeting strategy. Deep brain stimulation, Brain shift, Pneumocephalus, Interventional magnetic resonance imaging ABBREVIATIONS ABBREVIATIONS AC anterior commissure CSF cerebral spinal fluid CT computed tomography DBS deep brain stimulation ED Euclidian distance ICC intraclass correlation coefficient LF left fornix LPP left putaminal point MRI magnetic resonance imaging PC posterior commissure RF right fornix RPP right putaminal point SD standard deviation Suboptimal deep brain stimulation (DBS) electrode position may produce undesirable side effects limiting the benefits of this therapy.1,2 Advances in magnetic resonance imaging (MRI) allowed better visualization of brain structures and improved direct and indirect targeting.3 However, cerebral spinal fluid (CSF) loss (and consequently pneumocephalus) during the surgical procedure may cause the brain to shift from its original position.4 Intraoperative neurophysiological mapping is performed during awake procedures to refine preoperative planning and correct for stereotactic error and brain shift, but some patients do not tolerate or cannot undergo awake procedures. Intraoperative MRI has emerged as an important and useful alternative to awake stereotaxis with accuracy, outcomes, and complications comparable to DBS surgeries in a standard operative room.5-9 Intraoperative imaging can be utilized to better understand the dynamics of brain shift and pneumocephalus after unilateral or bilateral burr holes. Understanding how brain shift occurs during stereotactic procedures can help improve DBS-targeting strategies. In this study, we evaluate the extent of pneumocephalus and brain shift with frame-based stereotaxis in a series of patients who underwent bilateral DBS implantation. The frame-based stereotactic space provides a unique opportunity to study how pneumocephalus displaces different subcortical landmarks and targets of interest in functional neurosurgery. METHODS Patient Selection This study was approved by the local institutional review board and was exempted from obtaining individual patient informed consents due to its nature (retrospective review of medical records and images). We included in this study patients who underwent bilateral DBS implantation for movement disorders under general anesthesia with intraoperative MRI from February 2011 to May 2014. Frameless implantations were excluded and a total of 20 patients implanted with frame-based technique were selected. Right hemisphere was the first implanted side for most of the patients (n = 18). Two patients implanted on the left side first were excluded from the final analysis in order to better standardize the evaluation of how medial-lateral displacement of subcortical structures occurs with pneumocephalus. Surgical Procedure and Imaging All procedures were performed using a G model Leksell frame (Elekta, Stockholm, Sweden). After frame fixation, volumetric computed tomography (CT) scans were acquired and then were fused with preoperative gadolinium-enhanced axial T1-weighted MRI, coronal T2-weighted images, and axial proton density images. The globus pallidus pars interna was the target for 16 patients, and subthalamic nucleus was the target for 2 patients. Target and trajectory were determined using a stereotactic surgical planning software (iPlan 3.0, BrainLab AG, Munich, Germany) as previously described,10 except for microelectrode recording, which was not used for these patients. All patients were in supine position, with the head flexed approximately 30° from the ground. In all patients, a burr hole was made for the first (right) side and the lead implanted with the standard frame-based techniques. Then, the burr hole was made for the second side and the second lead was implanted. Gel foam and fibrin glue were applied in the burr hole to minimize CSF loss and air entry into the skull during the procedure. A T1-weighted MRI was acquired immediately after placement of the first lead for 13 patients, defined the interside MRI. Then, the contralateral electrode was implanted and a second T1-weighted MRI was acquired, defined as final MRI. All images were acquired according to labeling recommendations from the manufacturer.11 MRI safety testing studies had been conducted by our group, as previously reported.12,13 Anatomic Landmarks Six anatomic landmarks were used to evaluate displacement of deep brain structures: anterior commissure (AC), posterior commissure (PC), right fornix (RF), left fornix (LF), right and left putaminal points (RPP and LPP). RF and LF were determined as the center of the fornix at the level of the foramen of Monro. To find the putaminal point, axial and sagittal T1 images were analyzed slice by slice, with the window level allowing better contrast of the basal ganglia, until the most anterior point on both planes could be determined (Figure 1). The coordinates for all structures at each time points during the surgery were referenced to the same frame-based stereotactic space. Each MRI was coregistered to the preoperative stereo-CT using the iPlan 3.0 planning software (BrainLab AG). After analyzing the T1-weighted images, a virtual target was created for each landmark by two independent readers (C.M.M. and F.A). Coordinates in frame-based stereotactic space were obtained for each point. Then, the difference between post and preimplantation coordinates was calculated to determine the displacement of each anatomic landmark. The reference point (X = 0, Y = 0, Z = 0) for the Leksell frame coordinates system (Elekta) is the upper right posterior point of the fiducial box. Therefore, a positive difference means left displacement of the structure on the medial–lateral “X” axis, anterior displacement on the anteroposterior “Y” axis, and ventral (inferior) displacement on the dorsoventral “Z” axis. In addition, the Euclidian distance (ED) between the coordinates for each landmark in the preoperative, interside, and final MRI scans were calculated in order to evaluate total (ie, vector) displacement. FIGURE 1. View largeDownload slide Identification of the putaminal points (green dots) on axial (A) and sagital (B) T1-weighted images. FIGURE 1. View largeDownload slide Identification of the putaminal points (green dots) on axial (A) and sagital (B) T1-weighted images. Pneumocephalus Measurement Pneumocephalus was measured for volume and thickness. First, the contrast window of T1-weighted MRI was set for each patient individually in order to allow optimal visualization of the frontal sinus and the pneumocephalus. To measure the volume, the areas of pneumocephalus were shaded on all axial slices using a software tool, creating a 3-dimensional object which yielded the total volume. A volume of 0 (zero) mL was used for patients with no distinguishable pneumocephalus. A 2-dimensional evaluation of the pneumocephalus was also performed. The thickness of pneumocephalus was determined by the longest distance between the inner layer of frontal bone and the brain surface at the level of AC–PC line, which was chosen to minimize interreader variability. Statistical Analysis Statistical analysis was performed using IBM SPSS Statistics 20.0 (IBM Corp, Armonk, New York). Intraclass correlation coefficient (ICC) was used to determine agreement between readers. Paired t-test was used to analyze the displacement of each anatomic landmark. Pneumocephalus volume, thickness, the sum of the landmarks displacements, and duration of the procedure were analyzed using Spearman's rank correlation. RESULTS There was an excellent agreement between readers regarding anatomic landmark coordinates (mean = 0.7 mm, standard deviation [SD] = 1.4) and pneumocephalus (mean = 0.1 mL, SD = 0.2) with an ICC ranging between 0.87 and 0.99. Anatomic Landmark Displacement Following 1 Burr Hole Table 1 summarizes the 3-dimensional displacement of each anatomic landmark after 1 burr hole. When AC displacement was analyzed according to Cartesian axes, only displacement on the Y-axis was statistically significant (mean = −0.9 mm; SD = 0.5; min = −0.1 mm; max = −1.5 mm; P = .02; Table 2). PC displacement was not significant on any of the Cartesian axes (Table 2). For RF, displacement was statistically significant only on the Y-axis (mean = −0.7 mm; SD = 0.4; min = 0.2 mm; max = 1.3 mm; P <.001), as well as LF (mean = −0.5 mm; SD = 0.3; min = 0 mm; max = −0.9 mm; P <.001; Table 2). When RPP was analyzed according to the Cartesian axes, only displacement on the Y-axis exhibited statistical significance (mean = −0.7 mm; SD = 0.4; min = 0 mm; max = −1.3mm; P < .001; Table 2). However, for LPP displacement was not significant on any of the Cartesian axes (Table 2). TABLE 1. Anatomic Landmark 3-Dimensional Displacement (mm)   AC  PC  RF  LF  RPP  LPP  Preoperative MRI vs interside MRI     Mean  1.2  0.8  1.0  0.9  1.6  2.0   SD  0.4  0.3  0.4  0.4  1.0  0.8   Min  0.5  0.4  0.6  0.3  0.3  0.6   Max  1.9  1.3  1.9  1.4  3.6  3.3  Preoperative MRI vs final MRI     Mean  1.5  0.9  0.9  1.1  2.3  2.3   SD  0.6  0.4  0.4  0.3  1.6  1.3   Min  0.7  0.3  0.4  0.5  0.5  0.3   Max  2.9  1.8  1.8  1.6  6.6  5.6  Interside MRI vs final MRI     Mean  0.5  0.6  0.5  0.6  2.1  2.3   SD  0.2  0.3  0.4  0.3  1.9  1.4   Min  0.1  0.2  0.1  0.1  0.7  0.3   Max  1.0  1.1  1.2  1.3  5.7  5.2    AC  PC  RF  LF  RPP  LPP  Preoperative MRI vs interside MRI     Mean  1.2  0.8  1.0  0.9  1.6  2.0   SD  0.4  0.3  0.4  0.4  1.0  0.8   Min  0.5  0.4  0.6  0.3  0.3  0.6   Max  1.9  1.3  1.9  1.4  3.6  3.3  Preoperative MRI vs final MRI     Mean  1.5  0.9  0.9  1.1  2.3  2.3   SD  0.6  0.4  0.4  0.3  1.6  1.3   Min  0.7  0.3  0.4  0.5  0.5  0.3   Max  2.9  1.8  1.8  1.6  6.6  5.6  Interside MRI vs final MRI     Mean  0.5  0.6  0.5  0.6  2.1  2.3   SD  0.2  0.3  0.4  0.3  1.9  1.4   Min  0.1  0.2  0.1  0.1  0.7  0.3   Max  1.0  1.1  1.2  1.3  5.7  5.2  AC, anterior commissure; PC, posterior commissure; RF, right fornix; LF, left fornix; RPP, right putaminal point; LPP, left putaminal point; SD, standard deviation; Min, minimum; Max, maximum; MRI, magnetic resonance imaging; mm, millimeters. View Large TABLE 1. Anatomic Landmark 3-Dimensional Displacement (mm)   AC  PC  RF  LF  RPP  LPP  Preoperative MRI vs interside MRI     Mean  1.2  0.8  1.0  0.9  1.6  2.0   SD  0.4  0.3  0.4  0.4  1.0  0.8   Min  0.5  0.4  0.6  0.3  0.3  0.6   Max  1.9  1.3  1.9  1.4  3.6  3.3  Preoperative MRI vs final MRI     Mean  1.5  0.9  0.9  1.1  2.3  2.3   SD  0.6  0.4  0.4  0.3  1.6  1.3   Min  0.7  0.3  0.4  0.5  0.5  0.3   Max  2.9  1.8  1.8  1.6  6.6  5.6  Interside MRI vs final MRI     Mean  0.5  0.6  0.5  0.6  2.1  2.3   SD  0.2  0.3  0.4  0.3  1.9  1.4   Min  0.1  0.2  0.1  0.1  0.7  0.3   Max  1.0  1.1  1.2  1.3  5.7  5.2    AC  PC  RF  LF  RPP  LPP  Preoperative MRI vs interside MRI     Mean  1.2  0.8  1.0  0.9  1.6  2.0   SD  0.4  0.3  0.4  0.4  1.0  0.8   Min  0.5  0.4  0.6  0.3  0.3  0.6   Max  1.9  1.3  1.9  1.4  3.6  3.3  Preoperative MRI vs final MRI     Mean  1.5  0.9  0.9  1.1  2.3  2.3   SD  0.6  0.4  0.4  0.3  1.6  1.3   Min  0.7  0.3  0.4  0.5  0.5  0.3   Max  2.9  1.8  1.8  1.6  6.6  5.6  Interside MRI vs final MRI     Mean  0.5  0.6  0.5  0.6  2.1  2.3   SD  0.2  0.3  0.4  0.3  1.9  1.4   Min  0.1  0.2  0.1  0.1  0.7  0.3   Max  1.0  1.1  1.2  1.3  5.7  5.2  AC, anterior commissure; PC, posterior commissure; RF, right fornix; LF, left fornix; RPP, right putaminal point; LPP, left putaminal point; SD, standard deviation; Min, minimum; Max, maximum; MRI, magnetic resonance imaging; mm, millimeters. View Large TABLE 2. Anatomic Landmark Displacement After 1 Burr Hole   X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  0.1  0.4  .26  −0.9  0.5  .02  0.2  0.6  .31  PC  0.2  0.5  .18  0.1  0.5  .64  0.0  0.5  1.00  RF  0.0  0.3  .72  −0.7  0.4  <.001  −0.2  0.7  .25  LF  0.0  0.5  .81  −0.5  0.3  <.001  −0.2  0.6  .16  RPP  0.1  1.0  .68  −0.7  0.4  <.001  0.2  1.4  .62  LPP  −0.1  1.0  .80  −0.6  1.0  .055  0.1  1.6  .79    X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  0.1  0.4  .26  −0.9  0.5  .02  0.2  0.6  .31  PC  0.2  0.5  .18  0.1  0.5  .64  0.0  0.5  1.00  RF  0.0  0.3  .72  −0.7  0.4  <.001  −0.2  0.7  .25  LF  0.0  0.5  .81  −0.5  0.3  <.001  −0.2  0.6  .16  RPP  0.1  1.0  .68  −0.7  0.4  <.001  0.2  1.4  .62  LPP  −0.1  1.0  .80  −0.6  1.0  .055  0.1  1.6  .79  Anatomic displacement represents the difference between Leksell frame (Elekta) coordinates obtained from the final MRI and the preoperative MRI. AC, anterior commissure; PC, posterior commissure; RF, right fornix; LF, left fornix; RPP, right putaminal point; LPP, left putaminal point; SD, standard deviation. Positive values mean left displacement of the structure on the mediolateral “X” axis, anterior displacement on the anteroposterior “Y” axis, and ventral (inferior) displacement on the dorsoventral “Z” axis. View Large TABLE 2. Anatomic Landmark Displacement After 1 Burr Hole   X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  0.1  0.4  .26  −0.9  0.5  .02  0.2  0.6  .31  PC  0.2  0.5  .18  0.1  0.5  .64  0.0  0.5  1.00  RF  0.0  0.3  .72  −0.7  0.4  <.001  −0.2  0.7  .25  LF  0.0  0.5  .81  −0.5  0.3  <.001  −0.2  0.6  .16  RPP  0.1  1.0  .68  −0.7  0.4  <.001  0.2  1.4  .62  LPP  −0.1  1.0  .80  −0.6  1.0  .055  0.1  1.6  .79    X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  0.1  0.4  .26  −0.9  0.5  .02  0.2  0.6  .31  PC  0.2  0.5  .18  0.1  0.5  .64  0.0  0.5  1.00  RF  0.0  0.3  .72  −0.7  0.4  <.001  −0.2  0.7  .25  LF  0.0  0.5  .81  −0.5  0.3  <.001  −0.2  0.6  .16  RPP  0.1  1.0  .68  −0.7  0.4  <.001  0.2  1.4  .62  LPP  −0.1  1.0  .80  −0.6  1.0  .055  0.1  1.6  .79  Anatomic displacement represents the difference between Leksell frame (Elekta) coordinates obtained from the final MRI and the preoperative MRI. AC, anterior commissure; PC, posterior commissure; RF, right fornix; LF, left fornix; RPP, right putaminal point; LPP, left putaminal point; SD, standard deviation. Positive values mean left displacement of the structure on the mediolateral “X” axis, anterior displacement on the anteroposterior “Y” axis, and ventral (inferior) displacement on the dorsoventral “Z” axis. View Large Anatomic Landmark Displacement Following 2 Burr Holes Table 1 summarizes the 3-dimensional displacement of each anatomic landmark after 2 burr holes. According to Cartesian axes, AC displacement was statistically significant only on the Y-axis (mean = −1.1 mm; SD = 0.5; min = −0.1 mm; max = −2.5 mm; P < .001; Table 3). When PC was analyzed, displacement was not significant on any of the Cartesian axes (Table 3). For RF, displacement was statistically significant only on the Y-axis (Mean = −0.6 mm; SD = 0.5; min = 0 mm; max = −1.7 mm; P < .001; Table 3). For LF, again only displacement on the Y-axis was statistically significant (Mean = −0.7 mm; SD = 0.4; min = −0.1 mm; max = −1.3 mm; P <.001; Table 3). Statistical significance on the Y-axis was also found for RPP (Mean = −0.9 mm; SD = 0.9 mm; min = 0 mm; max = −3.2 mm; P = .001) and LPP (Mean = −1.0 mm; SD = 1.0; min = −0.2 mm; max = −3.4 mm; P = .001; Table 3). TABLE 3. Anatomic Landmark Displacement After 2 Burr Holes   X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  0.2  0.6  .19  −1.1  0.5  <.001  0.3  0.8  .17  PC  0.2  0.6  .11  0.0  0.6  .85  0.2  0.5  .19  RF  0.1  0.4  .52  −0.6  0.5  <.001  0.1  0.5  .53  LF  0.1  0.5  .27  −0.7  0.4  <.001  0.4  0.6  .84  RPP  0.0  1.4  .96  −0.9  0.9  .001  0.4  2.1  .42  LPP  0.0  1.2  .91  −1.0  1.0  .001  0.5  1.9  .29    X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  0.2  0.6  .19  −1.1  0.5  <.001  0.3  0.8  .17  PC  0.2  0.6  .11  0.0  0.6  .85  0.2  0.5  .19  RF  0.1  0.4  .52  −0.6  0.5  <.001  0.1  0.5  .53  LF  0.1  0.5  .27  −0.7  0.4  <.001  0.4  0.6  .84  RPP  0.0  1.4  .96  −0.9  0.9  .001  0.4  2.1  .42  LPP  0.0  1.2  .91  −1.0  1.0  .001  0.5  1.9  .29  Anatomic displacement represents the difference between Leksell frame (Elekta) coordinates obtained from the final MRI and the preoperative MRI. AC, anterior commissure; PC, posterior commissure; RF, right fornix; LF, left fornix; RPP, right putaminal point; LPP, left putaminal point; SD, standard deviation. Positive values mean left displacement of the structure on the mediolateral “X” axis, anterior displacement on the anteroposterior “Y” axis, and ventral (inferior) displacement on the dorsoventral “Z” axis. View Large TABLE 3. Anatomic Landmark Displacement After 2 Burr Holes   X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  0.2  0.6  .19  −1.1  0.5  <.001  0.3  0.8  .17  PC  0.2  0.6  .11  0.0  0.6  .85  0.2  0.5  .19  RF  0.1  0.4  .52  −0.6  0.5  <.001  0.1  0.5  .53  LF  0.1  0.5  .27  −0.7  0.4  <.001  0.4  0.6  .84  RPP  0.0  1.4  .96  −0.9  0.9  .001  0.4  2.1  .42  LPP  0.0  1.2  .91  −1.0  1.0  .001  0.5  1.9  .29    X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  0.2  0.6  .19  −1.1  0.5  <.001  0.3  0.8  .17  PC  0.2  0.6  .11  0.0  0.6  .85  0.2  0.5  .19  RF  0.1  0.4  .52  −0.6  0.5  <.001  0.1  0.5  .53  LF  0.1  0.5  .27  −0.7  0.4  <.001  0.4  0.6  .84  RPP  0.0  1.4  .96  −0.9  0.9  .001  0.4  2.1  .42  LPP  0.0  1.2  .91  −1.0  1.0  .001  0.5  1.9  .29  Anatomic displacement represents the difference between Leksell frame (Elekta) coordinates obtained from the final MRI and the preoperative MRI. AC, anterior commissure; PC, posterior commissure; RF, right fornix; LF, left fornix; RPP, right putaminal point; LPP, left putaminal point; SD, standard deviation. Positive values mean left displacement of the structure on the mediolateral “X” axis, anterior displacement on the anteroposterior “Y” axis, and ventral (inferior) displacement on the dorsoventral “Z” axis. View Large Anatomic Landmark Displacement Between First and Second Burr Holes Table 1 summarizes the 3-dimensional displacement of each anatomic landmark between burr holes. Displacement according to Cartesian axes was not statistically significant for any of the three axes for AC and for PC, it was significant for the Y- and Z-axis only (P = .02; P = .03; Table 4). For both RF and LF, displacement on the Z-axis was statistically significant comparing both MRIs (P = .02, P = .004), whereas for both RPP and LPP, none of the Cartesian axes exhibited statistically significant displacements (Table 4). TABLE 4. Anatomic Landmark Displacement Between First and Second Burr Hole   X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  −0.1  0.3  .12  −0.2  0.3  .07  0.1  0.4  .45  PC  0.0  0.4  .73  −0.2  0.3  .02  0.2  0.3  .03  RF  0.0  0.3  .85  0.0  0.2  .81  0.3  0.4  .02  LF  0.1  0.3  .31  −0.2  0.4  .06  0.3  .3  .004  RPP  −0.2  1.4  .65  −0.2  0.9  .55  0.2  2.3  .81  LPP  −0.2  1.3  .66  −0.3  0.7  .23  0.4  2.3  .49    X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  −0.1  0.3  .12  −0.2  0.3  .07  0.1  0.4  .45  PC  0.0  0.4  .73  −0.2  0.3  .02  0.2  0.3  .03  RF  0.0  0.3  .85  0.0  0.2  .81  0.3  0.4  .02  LF  0.1  0.3  .31  −0.2  0.4  .06  0.3  .3  .004  RPP  −0.2  1.4  .65  −0.2  0.9  .55  0.2  2.3  .81  LPP  −0.2  1.3  .66  −0.3  0.7  .23  0.4  2.3  .49  Anatomic displacement represents the difference between Leksell frame (Elekta) coordinates obtained from the final MRI and the interside MRI. AC, anterior commissure; PC, posterior commissure; RF, right fornix; LF, left fornix; RPP, right putaminal point; LPP, left putaminal point; SD, standard deviation. Positive values mean left displacement of the structure on the mediolateral “X” axis, anterior displacement on the anteroposterior “Y” axis, and ventral (inferior) displacement on the dorsoventral “Z” axis. View Large TABLE 4. Anatomic Landmark Displacement Between First and Second Burr Hole   X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  −0.1  0.3  .12  −0.2  0.3  .07  0.1  0.4  .45  PC  0.0  0.4  .73  −0.2  0.3  .02  0.2  0.3  .03  RF  0.0  0.3  .85  0.0  0.2  .81  0.3  0.4  .02  LF  0.1  0.3  .31  −0.2  0.4  .06  0.3  .3  .004  RPP  −0.2  1.4  .65  −0.2  0.9  .55  0.2  2.3  .81  LPP  −0.2  1.3  .66  −0.3  0.7  .23  0.4  2.3  .49    X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  −0.1  0.3  .12  −0.2  0.3  .07  0.1  0.4  .45  PC  0.0  0.4  .73  −0.2  0.3  .02  0.2  0.3  .03  RF  0.0  0.3  .85  0.0  0.2  .81  0.3  0.4  .02  LF  0.1  0.3  .31  −0.2  0.4  .06  0.3  .3  .004  RPP  −0.2  1.4  .65  −0.2  0.9  .55  0.2  2.3  .81  LPP  −0.2  1.3  .66  −0.3  0.7  .23  0.4  2.3  .49  Anatomic displacement represents the difference between Leksell frame (Elekta) coordinates obtained from the final MRI and the interside MRI. AC, anterior commissure; PC, posterior commissure; RF, right fornix; LF, left fornix; RPP, right putaminal point; LPP, left putaminal point; SD, standard deviation. Positive values mean left displacement of the structure on the mediolateral “X” axis, anterior displacement on the anteroposterior “Y” axis, and ventral (inferior) displacement on the dorsoventral “Z” axis. View Large Pneumocephalus and Duration of the Procedure The median pneumocephalus volume for the patients with an interside MRI was 0.1 mL (min = 0.0 mL; max = 11.5 mL). Pneumocephalus thickness median was 0 mm (min = 0 mm; max = 9.3 mm). There was a strong correlation between volume and thickness (rho = 0.81; P < .001). Duration of implantation of the first lead (median = 78 min; min = 67 min; max = 109 min) was not correlated with the pneumocephalus volume (rho = −0.2; P = .50). The median pneumocephalus volume for the patients with a final MRI was 0.6 mL (min = 0.01 mL; max = 32 mL; Figure 2). After a second burr hole, pneumocephalus thickness median was 1.3 mm (min = 0 mm; max = 23.3 mm). There was a strong correlation between volume and thickness (rho = 0.77; P < .001). There was no correlation between duration of implantation of both leads (median = 195.5 min; min = 118 min; max = 268 min) and pneumocephalus volume (rho = −0.06; P = .80). FIGURE 2. View largeDownload slide Boxplot demonstrating the distribution of pneumocephalus volumes after 2 burr holes. mL, milliliters. FIGURE 2. View largeDownload slide Boxplot demonstrating the distribution of pneumocephalus volumes after 2 burr holes. mL, milliliters. Three-Dimensional Displacement and Number of Burr Holes After 1 burr hole, there was no correlation between the pneumocephalus volume and the sum of anatomic landmarks displacements (ED; rho = 0.16, P = .60). However, after 2 burr holes, there was a significant correlation between the pneumocephalus volume and the sum of anatomic landmarks displacements (ED; rho = 0.61, P = .007). DISCUSSION Traditionally, microelectrode recording has been used as the standard tool during awake implantation, for refining targeting based on intraoperative data.10,14 Recently, intraoperative MRI has gained greater attention as a tool for refining electrode placement and for compensating for target displacement.15,16 Evaluating the effect of pneumocephalus on target location during awake surgery has been difficult due to technical limitations. Most imaging techniques utilized (ie, fluoroscopy and “O-arm”) cannot adequately evaluate the volume of pneumocephalus or accurately visualize subcortical structures. Intraoperative MRI can often visualize subcortical structures; however, most of the systems used for implantation in the MRI suite are based on “frameless” technology, which does not provide a robust reference system for evaluating structural displacement. Of note, one cannot rely on utilizing internal landmarks such as the AC or midcommissural point to evaluate displacement of other cerebral structures because these landmarks are also subject to the same effects. Because we have been conducting frame-based DBS lead implantation in the intraoperative MRI suite, we developed a data set that allows for accurate assessment of how pneumocephalus influences the location of subcortical structures after single or bilateral burr holes. Different factors can be related to the amount of pneumocephalus after a burr hole (with opening of the dura mater and arachnoid) such as the volume of the brain,4 position of the patient's head, and the use of glue or bone wax to seal dural defect intraoperatively.17,18 In addition, the effect of gravity on brain structures, the amount of CSF lost, and the deformation of the brain during the introduction of the electrode can be causes of brain shift.17,19 In this study, we analyzed the displacement of different anatomic landmarks and the correlation between the amount of pneumocephalus following DBS leads implantation on 1 side or both. Pneumocephalus varies significantly across patients, from 0 to 32 mL. On average, pneumocephalus volume was smaller in our data (median = 0.6 mL) than Slotty et al18 (median = 2.1 mL), although both distributions were similar (Figure 2). Duration of the procedure was not associated with pneumocephalus volume, likely due to efficacious burr hole occlusion techniques such as use of fibrin glue that may have minimized CSF egress over time. Although Elias et al20 reported larger pneumocephali (mean = 4.3 mL) and longer duration of procedures (mean = 222 min), they also found no correlation between pneumocephalus volume and duration of procedure. Evaluation of landmark location according to the Cartesian axes showed that displacement was significant on the Y-axis for most of the structures after both interside and final MRIs. The finding corroborates the hypothesis that posterior displacement of intracranial structures occurs due to gravity and the supine position of the head during imaging acquisition. Our results show a significant AC displacement corroborating the findings of Halpern et al21. In that study, the authors found a significant correlation between AC–PC distance shortening and pneumocephalus, represented by the degree of frontal cortex displacement. Similar to Obuchi et al,22 we noted nonsignificant displacements on the X- and Z-axes after the first burr hole. However, significant displacements in the Z-axis were noted after the second burr hole. Interestingly, there was a minimal but superior displacement of PC, RF, and LF (mean = 0.2, 0.3, and 0.3, respectively) between the interside MRI and the final MRI. This finding may be related to changes in the patients’ head position during the lead implantation and the imaging acquisition. Another finding in our study was that PC position did not change as much as AC position following lead implantation on 1 or both sides. The finding is consistent with the work by Ivan et al16 reporting a greater displacement of the frontal lobe, followed by the temporal and the occipital poles following burr hole procedures. Likewise, our results indicate a significant displacement of the putaminal points, again suggesting that structures located more anteriorly are likely to show greater displacement than more posteriorly located landmarks. The analysis of anatomic landmark displacement after right (first)-sided burr holes demonstrates that both RF and LF were displaced posteriorly. This is an interesting finding, as one could intuitively expect that statistically significant displacements would only occur ipsilateral to the burr hole. The results indicate that structural displacement after a single burr hole can influence not only the targeting on the same side as the burr hole but also begin the process of displacement of the contralateral side, which can be further propagated after the second burr hole. Better understanding of these effects can inform neurosurgeons to attempt to adjust the targeting of the second DBS lead after accounting for the volume of pneumocephalus resulting from implantation on 1 side. Our findings contradict findings from prior studies. Miyagi et al23 suggested that contralateral brain shift that occurs following a unilateral burr hole is performed and that this shift resets to the midline after a second burr hole. However, we found no significant lateral displacement after a unilateral burr hole in our series. It is uncertain whether this discrepancy results from patient characteristics, measurement methods, or nuances in surgical technique. Limitations While this data set is unique for the use of frame-based DBS implantation techniques in the intraoperative MRI suite, a few limitations are inherent to the nature of the work and need to be taken into account. This study is a retrospective review with a limited number of patients and therefore potentially underpowered to assess significance of some effects. It is possible that as we continue to increase our case series of patients implanted with the same techniques that nonsignificant findings in the present study may prove to be, in fact, significant. In addition, we note that we acquired MRIs to evaluate lead location accuracy only after DBS leads were implanted on the first side or bilaterally. Therefore, we could not account for how much brain shift was the result of the burr hole or lead implantation. Additional studies may allow us to control for these questions. CONCLUSION Better understanding of how pneumocephalus displaces subcortical structures can significantly enhance our intraoperative decision making and overall targeting strategy. Disclosures Dr Machado is a consultant for Spinal Modulation, Functional Neuromodulation, and Deep Brain Innovation, has distribution rights for intellectual property with Enspire, ATI, and Cardionomics. The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. REFERENCES 1. Matias CM, Mehanna R, Cooper SE et al.   Correlation among anatomic landmarks, location of subthalamic deep brain stimulation electrodes, stimulation parameters, and side effects during programming monopolar review. Oper Neurosurg (Hagerstown) . 2015; 11( 1): 99- 109. 2. Pourfar MH, Mogilner AY. Lead angle matters: side effects of deep brain stimulation improved with adjustment of lead angle. Neuromodulation Technol Neural Interface . 2016. doi: 10.1111/ner.12476. 3. Foltynie T, Zrinzo L, Martinez-Torres I et al.   MRI-guided STN DBS in Parkinson's disease without microelectrode recording: efficacy and safety. J Neurol Neurosurg Psychiatry . 2011; 82( 4): 358- 363. Google Scholar CrossRef Search ADS PubMed  4. Azmi H, Machado A, Deogaonkar M, Rezai A. Intracranial air correlates with preoperative cerebral atrophy and stereotactic error during bilateral STN DBS surgery for Parkinson's disease. Stereotact Funct Neurosurg . 2011; 89( 4): 246- 252. Google Scholar CrossRef Search ADS PubMed  5. Sidiropoulos C, Rammo R, Merker B et al.   Intraoperative MRI for deep brain stimulation lead placement in Parkinson's disease: 1 year motor and neuropsychological outcomes. J Neurol . 2016; 263( 6): 1226- 1231. Google Scholar CrossRef Search ADS PubMed  6. Nakajima T, Zrinzo L, Foltynie T et al.   MRI-guided subthalamic nucleus deep brain stimulation without microelectrode recording: Can we dispense with surgery under local anaesthesia? Stereotact Funct Neurosurg . 2011; 89( 5): 318- 325. Google Scholar CrossRef Search ADS PubMed  7. Starr PA, Markun LC, Larson PS, Volz MM, Martin AJ, Ostrem JL. Interventional MRI-guided deep brain stimulation in pediatric dystonia: first experience with the ClearPoint system. J Neurosurg Pediatr . 2014; 14( 4): 400- 408. Google Scholar CrossRef Search ADS PubMed  8. Martin AJ, Larson PS, Ziman N et al.   Deep brain stimulator implantation in a diagnostic MRI suite: infection history over a 10-year period. J Neurosurg . 2017; 126( 1): 108- 113. Google Scholar CrossRef Search ADS PubMed  9. Chabardes S, Isnard S, Castrioto A et al.   Surgical implantation of STN-DBS leads using intraoperative MRI guidance: technique, accuracy, and clinical benefit at 1-year follow-up. Acta Neurochir (Wien) . 2015; 157( 4): 729- 737. Google Scholar CrossRef Search ADS PubMed  10. Machado A, Rezai AR, Kopell BH, Gross RE, Sharan AD, Benabid AL. Deep brain stimulation for Parkinson's disease: surgical technique and perioperative management. Mov Disord . 2006; 21( suppl 14): S247- S258. Google Scholar CrossRef Search ADS PubMed  11. Available at: http://manuals.medtronic.com/wcm/groups/mdtcom_sg/@emanuals/@era/@neuro/documents/documents/contrib_215455.pdf. Accessed December 2016. 12. Rezai AR, Baker KB, Tkach JA et al.   Is magnetic resonance imaging safe for patients with neurostimulation systems used for deep brain stimulation? Neurosurgery . 2005; 57( 5): 1056- 1062; discussion 1056–1062. Google Scholar CrossRef Search ADS PubMed  13. Baker KB, Tkach JA, Phillips MD, Rezai AR. Variability in RF-induced heating of a deep brain stimulation implant across MR systems. J Magn Reson Imaging . 2006; 24( 6): 1236- 1242. Google Scholar CrossRef Search ADS PubMed  14. Machado AG, Deogaonkar M, Cooper S. Deep brain stimulation for movement disorders: patient selection and technical options. Cleve Clin J Med . 2012; 79( suppl 2): S19- S24. Google Scholar CrossRef Search ADS PubMed  15. Starr PA, Martin AJ, Ostrem JL, Talke P, Levesque N, Larson PS. Subthalamic nucleus deep brain stimulator placement using high-field interventional magnetic resonance imaging and a skull-mounted aiming device: technique and application accuracy. J Neurosurg . 2010; 112( 3): 479- 490. Google Scholar CrossRef Search ADS PubMed  16. Ivan ME, Yarlagadda J, Saxena AP et al.   Brain shift during bur hole-based procedures using interventional MRI. J Neurosurg . 2014; 121( 1): 149- 160. Google Scholar CrossRef Search ADS PubMed  17. Petersen EA, Holl EM, Martinez-Torres I et al.   Minimizing brain shift in stereotactic functional neurosurgery. Neurosurgery . 2010; 67( 3 Suppl Operative): ons213- ons21; discussion ons221. Google Scholar PubMed  18. Slotty PJ, Kamp MA, Wille C, Kinfe TM, Steiger HJ, Vesper J. The impact of brain shift in deep brain stimulation surgery: observation and obviation. Acta Neurochir (Wien) . 2012; 154( 11): 2063- 2068. Google Scholar CrossRef Search ADS PubMed  19. Khan MF, Mewes K, Gross RE, Skrinjar O. Assessment of brain shift related to deep brain stimulation surgery. Stereotact Funct Neurosurg . 2008; 86( 1): 44- 53. Google Scholar CrossRef Search ADS PubMed  20. Elias WJ, Fu K-M, Frysinger RC. Cortical and subcortical brain shift during stereotactic procedures. J Neurosurg . 2007; 107( 5): 983- 988. Google Scholar CrossRef Search ADS PubMed  21. Halpern CH, Danish SF, Baltuch GH, Jaggi JL. Brain shift during deep brain stimulation surgery for Parkinson's disease. Stereotact Funct Neurosurg . 2008; 86( 1): 37- 43. Google Scholar CrossRef Search ADS PubMed  22. Obuchi T, Katayama Y, Kobayashi K, Oshima H, Fukaya C, Yamamoto T. Direction and predictive factors for the shift of brain structure during deep brain stimulation electrode implantation for advanced Parkinson's disease. Neuromodulation . 2008; 11( 4): 302- 310. Google Scholar CrossRef Search ADS PubMed  23. Miyagi Y, Shima F, Sasaki T. Brain shift: an error factor during implantation of deep brain stimulation electrodes. J Neurosurg . 2007; 107( 5): 989- 997. Google Scholar CrossRef Search ADS PubMed  Copyright © 2017 by the Congress of Neurological Surgeons This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Operative Neurosurgery Oxford University Press

Brain Shift and Pneumocephalus Assessment During Frame-Based Deep Brain Stimulation Implantation With Intraoperative Magnetic Resonance Imaging

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Congress of Neurological Surgeons
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Copyright © 2017 by the Congress of Neurological Surgeons
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2332-4252
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2332-4260
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10.1093/ons/opx170
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Abstract

Abstract BACKGROUND Brain shift and pneumocephalus are major concerns regarding deep brain stimulation (DBS). OBJECTIVE To report the extent of brain shift in deep structures and pneumocephalus in intraoperative magnetic resonance imaging (MRI). METHODS Twenty patients underwent bilateral DBS implantation in an MRI suite. Volume of pneumocephalus, duration of procedure, and 6 anatomic landmarks (anterior commissure, posterior commissure, right fornix [RF], left fornix [LF], right putaminal point, and left putaminal point) were measured. RESULTS Pneumocephalus varied from 0 to 32 mL (median = 0.6 mL). Duration of the procedure was on average 195.5 min (118-268 min) and was not correlated with the amount of pneumocephalus. There was a significant posterior displacement of the anterior commissure (mean = −1.1 mm, P < .001), RF (mean = −0.6 mm, P < .001), LF (mean = −0.7 mm, P < .001), right putaminal point (mean = −0.9 mm, P = .001), and left putaminal point (mean = −1.0 mm, P = .001), but not of the posterior commissure (mean = 0.0 mm, P = .85). Both RF (mean = −.7 mm, P < .001) and LF (mean = −0.5 mm, P < .001) were posteriorly displaced after a right-sided burr hole. There was a correlation between anatomic landmarks displacement and pneumocephalus after 2 burr holes (rho = 0.61, P = .007), but not after 1 burr hole (rho = 0.16, P = .60). CONCLUSION Better understanding of how pneumocephalus displaces subcortical structures can significantly enhance our intraoperative decision making and overall targeting strategy. Deep brain stimulation, Brain shift, Pneumocephalus, Interventional magnetic resonance imaging ABBREVIATIONS ABBREVIATIONS AC anterior commissure CSF cerebral spinal fluid CT computed tomography DBS deep brain stimulation ED Euclidian distance ICC intraclass correlation coefficient LF left fornix LPP left putaminal point MRI magnetic resonance imaging PC posterior commissure RF right fornix RPP right putaminal point SD standard deviation Suboptimal deep brain stimulation (DBS) electrode position may produce undesirable side effects limiting the benefits of this therapy.1,2 Advances in magnetic resonance imaging (MRI) allowed better visualization of brain structures and improved direct and indirect targeting.3 However, cerebral spinal fluid (CSF) loss (and consequently pneumocephalus) during the surgical procedure may cause the brain to shift from its original position.4 Intraoperative neurophysiological mapping is performed during awake procedures to refine preoperative planning and correct for stereotactic error and brain shift, but some patients do not tolerate or cannot undergo awake procedures. Intraoperative MRI has emerged as an important and useful alternative to awake stereotaxis with accuracy, outcomes, and complications comparable to DBS surgeries in a standard operative room.5-9 Intraoperative imaging can be utilized to better understand the dynamics of brain shift and pneumocephalus after unilateral or bilateral burr holes. Understanding how brain shift occurs during stereotactic procedures can help improve DBS-targeting strategies. In this study, we evaluate the extent of pneumocephalus and brain shift with frame-based stereotaxis in a series of patients who underwent bilateral DBS implantation. The frame-based stereotactic space provides a unique opportunity to study how pneumocephalus displaces different subcortical landmarks and targets of interest in functional neurosurgery. METHODS Patient Selection This study was approved by the local institutional review board and was exempted from obtaining individual patient informed consents due to its nature (retrospective review of medical records and images). We included in this study patients who underwent bilateral DBS implantation for movement disorders under general anesthesia with intraoperative MRI from February 2011 to May 2014. Frameless implantations were excluded and a total of 20 patients implanted with frame-based technique were selected. Right hemisphere was the first implanted side for most of the patients (n = 18). Two patients implanted on the left side first were excluded from the final analysis in order to better standardize the evaluation of how medial-lateral displacement of subcortical structures occurs with pneumocephalus. Surgical Procedure and Imaging All procedures were performed using a G model Leksell frame (Elekta, Stockholm, Sweden). After frame fixation, volumetric computed tomography (CT) scans were acquired and then were fused with preoperative gadolinium-enhanced axial T1-weighted MRI, coronal T2-weighted images, and axial proton density images. The globus pallidus pars interna was the target for 16 patients, and subthalamic nucleus was the target for 2 patients. Target and trajectory were determined using a stereotactic surgical planning software (iPlan 3.0, BrainLab AG, Munich, Germany) as previously described,10 except for microelectrode recording, which was not used for these patients. All patients were in supine position, with the head flexed approximately 30° from the ground. In all patients, a burr hole was made for the first (right) side and the lead implanted with the standard frame-based techniques. Then, the burr hole was made for the second side and the second lead was implanted. Gel foam and fibrin glue were applied in the burr hole to minimize CSF loss and air entry into the skull during the procedure. A T1-weighted MRI was acquired immediately after placement of the first lead for 13 patients, defined the interside MRI. Then, the contralateral electrode was implanted and a second T1-weighted MRI was acquired, defined as final MRI. All images were acquired according to labeling recommendations from the manufacturer.11 MRI safety testing studies had been conducted by our group, as previously reported.12,13 Anatomic Landmarks Six anatomic landmarks were used to evaluate displacement of deep brain structures: anterior commissure (AC), posterior commissure (PC), right fornix (RF), left fornix (LF), right and left putaminal points (RPP and LPP). RF and LF were determined as the center of the fornix at the level of the foramen of Monro. To find the putaminal point, axial and sagittal T1 images were analyzed slice by slice, with the window level allowing better contrast of the basal ganglia, until the most anterior point on both planes could be determined (Figure 1). The coordinates for all structures at each time points during the surgery were referenced to the same frame-based stereotactic space. Each MRI was coregistered to the preoperative stereo-CT using the iPlan 3.0 planning software (BrainLab AG). After analyzing the T1-weighted images, a virtual target was created for each landmark by two independent readers (C.M.M. and F.A). Coordinates in frame-based stereotactic space were obtained for each point. Then, the difference between post and preimplantation coordinates was calculated to determine the displacement of each anatomic landmark. The reference point (X = 0, Y = 0, Z = 0) for the Leksell frame coordinates system (Elekta) is the upper right posterior point of the fiducial box. Therefore, a positive difference means left displacement of the structure on the medial–lateral “X” axis, anterior displacement on the anteroposterior “Y” axis, and ventral (inferior) displacement on the dorsoventral “Z” axis. In addition, the Euclidian distance (ED) between the coordinates for each landmark in the preoperative, interside, and final MRI scans were calculated in order to evaluate total (ie, vector) displacement. FIGURE 1. View largeDownload slide Identification of the putaminal points (green dots) on axial (A) and sagital (B) T1-weighted images. FIGURE 1. View largeDownload slide Identification of the putaminal points (green dots) on axial (A) and sagital (B) T1-weighted images. Pneumocephalus Measurement Pneumocephalus was measured for volume and thickness. First, the contrast window of T1-weighted MRI was set for each patient individually in order to allow optimal visualization of the frontal sinus and the pneumocephalus. To measure the volume, the areas of pneumocephalus were shaded on all axial slices using a software tool, creating a 3-dimensional object which yielded the total volume. A volume of 0 (zero) mL was used for patients with no distinguishable pneumocephalus. A 2-dimensional evaluation of the pneumocephalus was also performed. The thickness of pneumocephalus was determined by the longest distance between the inner layer of frontal bone and the brain surface at the level of AC–PC line, which was chosen to minimize interreader variability. Statistical Analysis Statistical analysis was performed using IBM SPSS Statistics 20.0 (IBM Corp, Armonk, New York). Intraclass correlation coefficient (ICC) was used to determine agreement between readers. Paired t-test was used to analyze the displacement of each anatomic landmark. Pneumocephalus volume, thickness, the sum of the landmarks displacements, and duration of the procedure were analyzed using Spearman's rank correlation. RESULTS There was an excellent agreement between readers regarding anatomic landmark coordinates (mean = 0.7 mm, standard deviation [SD] = 1.4) and pneumocephalus (mean = 0.1 mL, SD = 0.2) with an ICC ranging between 0.87 and 0.99. Anatomic Landmark Displacement Following 1 Burr Hole Table 1 summarizes the 3-dimensional displacement of each anatomic landmark after 1 burr hole. When AC displacement was analyzed according to Cartesian axes, only displacement on the Y-axis was statistically significant (mean = −0.9 mm; SD = 0.5; min = −0.1 mm; max = −1.5 mm; P = .02; Table 2). PC displacement was not significant on any of the Cartesian axes (Table 2). For RF, displacement was statistically significant only on the Y-axis (mean = −0.7 mm; SD = 0.4; min = 0.2 mm; max = 1.3 mm; P <.001), as well as LF (mean = −0.5 mm; SD = 0.3; min = 0 mm; max = −0.9 mm; P <.001; Table 2). When RPP was analyzed according to the Cartesian axes, only displacement on the Y-axis exhibited statistical significance (mean = −0.7 mm; SD = 0.4; min = 0 mm; max = −1.3mm; P < .001; Table 2). However, for LPP displacement was not significant on any of the Cartesian axes (Table 2). TABLE 1. Anatomic Landmark 3-Dimensional Displacement (mm)   AC  PC  RF  LF  RPP  LPP  Preoperative MRI vs interside MRI     Mean  1.2  0.8  1.0  0.9  1.6  2.0   SD  0.4  0.3  0.4  0.4  1.0  0.8   Min  0.5  0.4  0.6  0.3  0.3  0.6   Max  1.9  1.3  1.9  1.4  3.6  3.3  Preoperative MRI vs final MRI     Mean  1.5  0.9  0.9  1.1  2.3  2.3   SD  0.6  0.4  0.4  0.3  1.6  1.3   Min  0.7  0.3  0.4  0.5  0.5  0.3   Max  2.9  1.8  1.8  1.6  6.6  5.6  Interside MRI vs final MRI     Mean  0.5  0.6  0.5  0.6  2.1  2.3   SD  0.2  0.3  0.4  0.3  1.9  1.4   Min  0.1  0.2  0.1  0.1  0.7  0.3   Max  1.0  1.1  1.2  1.3  5.7  5.2    AC  PC  RF  LF  RPP  LPP  Preoperative MRI vs interside MRI     Mean  1.2  0.8  1.0  0.9  1.6  2.0   SD  0.4  0.3  0.4  0.4  1.0  0.8   Min  0.5  0.4  0.6  0.3  0.3  0.6   Max  1.9  1.3  1.9  1.4  3.6  3.3  Preoperative MRI vs final MRI     Mean  1.5  0.9  0.9  1.1  2.3  2.3   SD  0.6  0.4  0.4  0.3  1.6  1.3   Min  0.7  0.3  0.4  0.5  0.5  0.3   Max  2.9  1.8  1.8  1.6  6.6  5.6  Interside MRI vs final MRI     Mean  0.5  0.6  0.5  0.6  2.1  2.3   SD  0.2  0.3  0.4  0.3  1.9  1.4   Min  0.1  0.2  0.1  0.1  0.7  0.3   Max  1.0  1.1  1.2  1.3  5.7  5.2  AC, anterior commissure; PC, posterior commissure; RF, right fornix; LF, left fornix; RPP, right putaminal point; LPP, left putaminal point; SD, standard deviation; Min, minimum; Max, maximum; MRI, magnetic resonance imaging; mm, millimeters. View Large TABLE 1. Anatomic Landmark 3-Dimensional Displacement (mm)   AC  PC  RF  LF  RPP  LPP  Preoperative MRI vs interside MRI     Mean  1.2  0.8  1.0  0.9  1.6  2.0   SD  0.4  0.3  0.4  0.4  1.0  0.8   Min  0.5  0.4  0.6  0.3  0.3  0.6   Max  1.9  1.3  1.9  1.4  3.6  3.3  Preoperative MRI vs final MRI     Mean  1.5  0.9  0.9  1.1  2.3  2.3   SD  0.6  0.4  0.4  0.3  1.6  1.3   Min  0.7  0.3  0.4  0.5  0.5  0.3   Max  2.9  1.8  1.8  1.6  6.6  5.6  Interside MRI vs final MRI     Mean  0.5  0.6  0.5  0.6  2.1  2.3   SD  0.2  0.3  0.4  0.3  1.9  1.4   Min  0.1  0.2  0.1  0.1  0.7  0.3   Max  1.0  1.1  1.2  1.3  5.7  5.2    AC  PC  RF  LF  RPP  LPP  Preoperative MRI vs interside MRI     Mean  1.2  0.8  1.0  0.9  1.6  2.0   SD  0.4  0.3  0.4  0.4  1.0  0.8   Min  0.5  0.4  0.6  0.3  0.3  0.6   Max  1.9  1.3  1.9  1.4  3.6  3.3  Preoperative MRI vs final MRI     Mean  1.5  0.9  0.9  1.1  2.3  2.3   SD  0.6  0.4  0.4  0.3  1.6  1.3   Min  0.7  0.3  0.4  0.5  0.5  0.3   Max  2.9  1.8  1.8  1.6  6.6  5.6  Interside MRI vs final MRI     Mean  0.5  0.6  0.5  0.6  2.1  2.3   SD  0.2  0.3  0.4  0.3  1.9  1.4   Min  0.1  0.2  0.1  0.1  0.7  0.3   Max  1.0  1.1  1.2  1.3  5.7  5.2  AC, anterior commissure; PC, posterior commissure; RF, right fornix; LF, left fornix; RPP, right putaminal point; LPP, left putaminal point; SD, standard deviation; Min, minimum; Max, maximum; MRI, magnetic resonance imaging; mm, millimeters. View Large TABLE 2. Anatomic Landmark Displacement After 1 Burr Hole   X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  0.1  0.4  .26  −0.9  0.5  .02  0.2  0.6  .31  PC  0.2  0.5  .18  0.1  0.5  .64  0.0  0.5  1.00  RF  0.0  0.3  .72  −0.7  0.4  <.001  −0.2  0.7  .25  LF  0.0  0.5  .81  −0.5  0.3  <.001  −0.2  0.6  .16  RPP  0.1  1.0  .68  −0.7  0.4  <.001  0.2  1.4  .62  LPP  −0.1  1.0  .80  −0.6  1.0  .055  0.1  1.6  .79    X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  0.1  0.4  .26  −0.9  0.5  .02  0.2  0.6  .31  PC  0.2  0.5  .18  0.1  0.5  .64  0.0  0.5  1.00  RF  0.0  0.3  .72  −0.7  0.4  <.001  −0.2  0.7  .25  LF  0.0  0.5  .81  −0.5  0.3  <.001  −0.2  0.6  .16  RPP  0.1  1.0  .68  −0.7  0.4  <.001  0.2  1.4  .62  LPP  −0.1  1.0  .80  −0.6  1.0  .055  0.1  1.6  .79  Anatomic displacement represents the difference between Leksell frame (Elekta) coordinates obtained from the final MRI and the preoperative MRI. AC, anterior commissure; PC, posterior commissure; RF, right fornix; LF, left fornix; RPP, right putaminal point; LPP, left putaminal point; SD, standard deviation. Positive values mean left displacement of the structure on the mediolateral “X” axis, anterior displacement on the anteroposterior “Y” axis, and ventral (inferior) displacement on the dorsoventral “Z” axis. View Large TABLE 2. Anatomic Landmark Displacement After 1 Burr Hole   X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  0.1  0.4  .26  −0.9  0.5  .02  0.2  0.6  .31  PC  0.2  0.5  .18  0.1  0.5  .64  0.0  0.5  1.00  RF  0.0  0.3  .72  −0.7  0.4  <.001  −0.2  0.7  .25  LF  0.0  0.5  .81  −0.5  0.3  <.001  −0.2  0.6  .16  RPP  0.1  1.0  .68  −0.7  0.4  <.001  0.2  1.4  .62  LPP  −0.1  1.0  .80  −0.6  1.0  .055  0.1  1.6  .79    X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  0.1  0.4  .26  −0.9  0.5  .02  0.2  0.6  .31  PC  0.2  0.5  .18  0.1  0.5  .64  0.0  0.5  1.00  RF  0.0  0.3  .72  −0.7  0.4  <.001  −0.2  0.7  .25  LF  0.0  0.5  .81  −0.5  0.3  <.001  −0.2  0.6  .16  RPP  0.1  1.0  .68  −0.7  0.4  <.001  0.2  1.4  .62  LPP  −0.1  1.0  .80  −0.6  1.0  .055  0.1  1.6  .79  Anatomic displacement represents the difference between Leksell frame (Elekta) coordinates obtained from the final MRI and the preoperative MRI. AC, anterior commissure; PC, posterior commissure; RF, right fornix; LF, left fornix; RPP, right putaminal point; LPP, left putaminal point; SD, standard deviation. Positive values mean left displacement of the structure on the mediolateral “X” axis, anterior displacement on the anteroposterior “Y” axis, and ventral (inferior) displacement on the dorsoventral “Z” axis. View Large Anatomic Landmark Displacement Following 2 Burr Holes Table 1 summarizes the 3-dimensional displacement of each anatomic landmark after 2 burr holes. According to Cartesian axes, AC displacement was statistically significant only on the Y-axis (mean = −1.1 mm; SD = 0.5; min = −0.1 mm; max = −2.5 mm; P < .001; Table 3). When PC was analyzed, displacement was not significant on any of the Cartesian axes (Table 3). For RF, displacement was statistically significant only on the Y-axis (Mean = −0.6 mm; SD = 0.5; min = 0 mm; max = −1.7 mm; P < .001; Table 3). For LF, again only displacement on the Y-axis was statistically significant (Mean = −0.7 mm; SD = 0.4; min = −0.1 mm; max = −1.3 mm; P <.001; Table 3). Statistical significance on the Y-axis was also found for RPP (Mean = −0.9 mm; SD = 0.9 mm; min = 0 mm; max = −3.2 mm; P = .001) and LPP (Mean = −1.0 mm; SD = 1.0; min = −0.2 mm; max = −3.4 mm; P = .001; Table 3). TABLE 3. Anatomic Landmark Displacement After 2 Burr Holes   X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  0.2  0.6  .19  −1.1  0.5  <.001  0.3  0.8  .17  PC  0.2  0.6  .11  0.0  0.6  .85  0.2  0.5  .19  RF  0.1  0.4  .52  −0.6  0.5  <.001  0.1  0.5  .53  LF  0.1  0.5  .27  −0.7  0.4  <.001  0.4  0.6  .84  RPP  0.0  1.4  .96  −0.9  0.9  .001  0.4  2.1  .42  LPP  0.0  1.2  .91  −1.0  1.0  .001  0.5  1.9  .29    X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  0.2  0.6  .19  −1.1  0.5  <.001  0.3  0.8  .17  PC  0.2  0.6  .11  0.0  0.6  .85  0.2  0.5  .19  RF  0.1  0.4  .52  −0.6  0.5  <.001  0.1  0.5  .53  LF  0.1  0.5  .27  −0.7  0.4  <.001  0.4  0.6  .84  RPP  0.0  1.4  .96  −0.9  0.9  .001  0.4  2.1  .42  LPP  0.0  1.2  .91  −1.0  1.0  .001  0.5  1.9  .29  Anatomic displacement represents the difference between Leksell frame (Elekta) coordinates obtained from the final MRI and the preoperative MRI. AC, anterior commissure; PC, posterior commissure; RF, right fornix; LF, left fornix; RPP, right putaminal point; LPP, left putaminal point; SD, standard deviation. Positive values mean left displacement of the structure on the mediolateral “X” axis, anterior displacement on the anteroposterior “Y” axis, and ventral (inferior) displacement on the dorsoventral “Z” axis. View Large TABLE 3. Anatomic Landmark Displacement After 2 Burr Holes   X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  0.2  0.6  .19  −1.1  0.5  <.001  0.3  0.8  .17  PC  0.2  0.6  .11  0.0  0.6  .85  0.2  0.5  .19  RF  0.1  0.4  .52  −0.6  0.5  <.001  0.1  0.5  .53  LF  0.1  0.5  .27  −0.7  0.4  <.001  0.4  0.6  .84  RPP  0.0  1.4  .96  −0.9  0.9  .001  0.4  2.1  .42  LPP  0.0  1.2  .91  −1.0  1.0  .001  0.5  1.9  .29    X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  0.2  0.6  .19  −1.1  0.5  <.001  0.3  0.8  .17  PC  0.2  0.6  .11  0.0  0.6  .85  0.2  0.5  .19  RF  0.1  0.4  .52  −0.6  0.5  <.001  0.1  0.5  .53  LF  0.1  0.5  .27  −0.7  0.4  <.001  0.4  0.6  .84  RPP  0.0  1.4  .96  −0.9  0.9  .001  0.4  2.1  .42  LPP  0.0  1.2  .91  −1.0  1.0  .001  0.5  1.9  .29  Anatomic displacement represents the difference between Leksell frame (Elekta) coordinates obtained from the final MRI and the preoperative MRI. AC, anterior commissure; PC, posterior commissure; RF, right fornix; LF, left fornix; RPP, right putaminal point; LPP, left putaminal point; SD, standard deviation. Positive values mean left displacement of the structure on the mediolateral “X” axis, anterior displacement on the anteroposterior “Y” axis, and ventral (inferior) displacement on the dorsoventral “Z” axis. View Large Anatomic Landmark Displacement Between First and Second Burr Holes Table 1 summarizes the 3-dimensional displacement of each anatomic landmark between burr holes. Displacement according to Cartesian axes was not statistically significant for any of the three axes for AC and for PC, it was significant for the Y- and Z-axis only (P = .02; P = .03; Table 4). For both RF and LF, displacement on the Z-axis was statistically significant comparing both MRIs (P = .02, P = .004), whereas for both RPP and LPP, none of the Cartesian axes exhibited statistically significant displacements (Table 4). TABLE 4. Anatomic Landmark Displacement Between First and Second Burr Hole   X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  −0.1  0.3  .12  −0.2  0.3  .07  0.1  0.4  .45  PC  0.0  0.4  .73  −0.2  0.3  .02  0.2  0.3  .03  RF  0.0  0.3  .85  0.0  0.2  .81  0.3  0.4  .02  LF  0.1  0.3  .31  −0.2  0.4  .06  0.3  .3  .004  RPP  −0.2  1.4  .65  −0.2  0.9  .55  0.2  2.3  .81  LPP  −0.2  1.3  .66  −0.3  0.7  .23  0.4  2.3  .49    X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  −0.1  0.3  .12  −0.2  0.3  .07  0.1  0.4  .45  PC  0.0  0.4  .73  −0.2  0.3  .02  0.2  0.3  .03  RF  0.0  0.3  .85  0.0  0.2  .81  0.3  0.4  .02  LF  0.1  0.3  .31  −0.2  0.4  .06  0.3  .3  .004  RPP  −0.2  1.4  .65  −0.2  0.9  .55  0.2  2.3  .81  LPP  −0.2  1.3  .66  −0.3  0.7  .23  0.4  2.3  .49  Anatomic displacement represents the difference between Leksell frame (Elekta) coordinates obtained from the final MRI and the interside MRI. AC, anterior commissure; PC, posterior commissure; RF, right fornix; LF, left fornix; RPP, right putaminal point; LPP, left putaminal point; SD, standard deviation. Positive values mean left displacement of the structure on the mediolateral “X” axis, anterior displacement on the anteroposterior “Y” axis, and ventral (inferior) displacement on the dorsoventral “Z” axis. View Large TABLE 4. Anatomic Landmark Displacement Between First and Second Burr Hole   X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  −0.1  0.3  .12  −0.2  0.3  .07  0.1  0.4  .45  PC  0.0  0.4  .73  −0.2  0.3  .02  0.2  0.3  .03  RF  0.0  0.3  .85  0.0  0.2  .81  0.3  0.4  .02  LF  0.1  0.3  .31  −0.2  0.4  .06  0.3  .3  .004  RPP  −0.2  1.4  .65  −0.2  0.9  .55  0.2  2.3  .81  LPP  −0.2  1.3  .66  −0.3  0.7  .23  0.4  2.3  .49    X  Y  Z    Mean  SD  P-value  Mean  SD  P-value  Mean  SD  P-value  AC  −0.1  0.3  .12  −0.2  0.3  .07  0.1  0.4  .45  PC  0.0  0.4  .73  −0.2  0.3  .02  0.2  0.3  .03  RF  0.0  0.3  .85  0.0  0.2  .81  0.3  0.4  .02  LF  0.1  0.3  .31  −0.2  0.4  .06  0.3  .3  .004  RPP  −0.2  1.4  .65  −0.2  0.9  .55  0.2  2.3  .81  LPP  −0.2  1.3  .66  −0.3  0.7  .23  0.4  2.3  .49  Anatomic displacement represents the difference between Leksell frame (Elekta) coordinates obtained from the final MRI and the interside MRI. AC, anterior commissure; PC, posterior commissure; RF, right fornix; LF, left fornix; RPP, right putaminal point; LPP, left putaminal point; SD, standard deviation. Positive values mean left displacement of the structure on the mediolateral “X” axis, anterior displacement on the anteroposterior “Y” axis, and ventral (inferior) displacement on the dorsoventral “Z” axis. View Large Pneumocephalus and Duration of the Procedure The median pneumocephalus volume for the patients with an interside MRI was 0.1 mL (min = 0.0 mL; max = 11.5 mL). Pneumocephalus thickness median was 0 mm (min = 0 mm; max = 9.3 mm). There was a strong correlation between volume and thickness (rho = 0.81; P < .001). Duration of implantation of the first lead (median = 78 min; min = 67 min; max = 109 min) was not correlated with the pneumocephalus volume (rho = −0.2; P = .50). The median pneumocephalus volume for the patients with a final MRI was 0.6 mL (min = 0.01 mL; max = 32 mL; Figure 2). After a second burr hole, pneumocephalus thickness median was 1.3 mm (min = 0 mm; max = 23.3 mm). There was a strong correlation between volume and thickness (rho = 0.77; P < .001). There was no correlation between duration of implantation of both leads (median = 195.5 min; min = 118 min; max = 268 min) and pneumocephalus volume (rho = −0.06; P = .80). FIGURE 2. View largeDownload slide Boxplot demonstrating the distribution of pneumocephalus volumes after 2 burr holes. mL, milliliters. FIGURE 2. View largeDownload slide Boxplot demonstrating the distribution of pneumocephalus volumes after 2 burr holes. mL, milliliters. Three-Dimensional Displacement and Number of Burr Holes After 1 burr hole, there was no correlation between the pneumocephalus volume and the sum of anatomic landmarks displacements (ED; rho = 0.16, P = .60). However, after 2 burr holes, there was a significant correlation between the pneumocephalus volume and the sum of anatomic landmarks displacements (ED; rho = 0.61, P = .007). DISCUSSION Traditionally, microelectrode recording has been used as the standard tool during awake implantation, for refining targeting based on intraoperative data.10,14 Recently, intraoperative MRI has gained greater attention as a tool for refining electrode placement and for compensating for target displacement.15,16 Evaluating the effect of pneumocephalus on target location during awake surgery has been difficult due to technical limitations. Most imaging techniques utilized (ie, fluoroscopy and “O-arm”) cannot adequately evaluate the volume of pneumocephalus or accurately visualize subcortical structures. Intraoperative MRI can often visualize subcortical structures; however, most of the systems used for implantation in the MRI suite are based on “frameless” technology, which does not provide a robust reference system for evaluating structural displacement. Of note, one cannot rely on utilizing internal landmarks such as the AC or midcommissural point to evaluate displacement of other cerebral structures because these landmarks are also subject to the same effects. Because we have been conducting frame-based DBS lead implantation in the intraoperative MRI suite, we developed a data set that allows for accurate assessment of how pneumocephalus influences the location of subcortical structures after single or bilateral burr holes. Different factors can be related to the amount of pneumocephalus after a burr hole (with opening of the dura mater and arachnoid) such as the volume of the brain,4 position of the patient's head, and the use of glue or bone wax to seal dural defect intraoperatively.17,18 In addition, the effect of gravity on brain structures, the amount of CSF lost, and the deformation of the brain during the introduction of the electrode can be causes of brain shift.17,19 In this study, we analyzed the displacement of different anatomic landmarks and the correlation between the amount of pneumocephalus following DBS leads implantation on 1 side or both. Pneumocephalus varies significantly across patients, from 0 to 32 mL. On average, pneumocephalus volume was smaller in our data (median = 0.6 mL) than Slotty et al18 (median = 2.1 mL), although both distributions were similar (Figure 2). Duration of the procedure was not associated with pneumocephalus volume, likely due to efficacious burr hole occlusion techniques such as use of fibrin glue that may have minimized CSF egress over time. Although Elias et al20 reported larger pneumocephali (mean = 4.3 mL) and longer duration of procedures (mean = 222 min), they also found no correlation between pneumocephalus volume and duration of procedure. Evaluation of landmark location according to the Cartesian axes showed that displacement was significant on the Y-axis for most of the structures after both interside and final MRIs. The finding corroborates the hypothesis that posterior displacement of intracranial structures occurs due to gravity and the supine position of the head during imaging acquisition. Our results show a significant AC displacement corroborating the findings of Halpern et al21. In that study, the authors found a significant correlation between AC–PC distance shortening and pneumocephalus, represented by the degree of frontal cortex displacement. Similar to Obuchi et al,22 we noted nonsignificant displacements on the X- and Z-axes after the first burr hole. However, significant displacements in the Z-axis were noted after the second burr hole. Interestingly, there was a minimal but superior displacement of PC, RF, and LF (mean = 0.2, 0.3, and 0.3, respectively) between the interside MRI and the final MRI. This finding may be related to changes in the patients’ head position during the lead implantation and the imaging acquisition. Another finding in our study was that PC position did not change as much as AC position following lead implantation on 1 or both sides. The finding is consistent with the work by Ivan et al16 reporting a greater displacement of the frontal lobe, followed by the temporal and the occipital poles following burr hole procedures. Likewise, our results indicate a significant displacement of the putaminal points, again suggesting that structures located more anteriorly are likely to show greater displacement than more posteriorly located landmarks. The analysis of anatomic landmark displacement after right (first)-sided burr holes demonstrates that both RF and LF were displaced posteriorly. This is an interesting finding, as one could intuitively expect that statistically significant displacements would only occur ipsilateral to the burr hole. The results indicate that structural displacement after a single burr hole can influence not only the targeting on the same side as the burr hole but also begin the process of displacement of the contralateral side, which can be further propagated after the second burr hole. Better understanding of these effects can inform neurosurgeons to attempt to adjust the targeting of the second DBS lead after accounting for the volume of pneumocephalus resulting from implantation on 1 side. Our findings contradict findings from prior studies. Miyagi et al23 suggested that contralateral brain shift that occurs following a unilateral burr hole is performed and that this shift resets to the midline after a second burr hole. However, we found no significant lateral displacement after a unilateral burr hole in our series. It is uncertain whether this discrepancy results from patient characteristics, measurement methods, or nuances in surgical technique. Limitations While this data set is unique for the use of frame-based DBS implantation techniques in the intraoperative MRI suite, a few limitations are inherent to the nature of the work and need to be taken into account. This study is a retrospective review with a limited number of patients and therefore potentially underpowered to assess significance of some effects. It is possible that as we continue to increase our case series of patients implanted with the same techniques that nonsignificant findings in the present study may prove to be, in fact, significant. In addition, we note that we acquired MRIs to evaluate lead location accuracy only after DBS leads were implanted on the first side or bilaterally. Therefore, we could not account for how much brain shift was the result of the burr hole or lead implantation. Additional studies may allow us to control for these questions. CONCLUSION Better understanding of how pneumocephalus displaces subcortical structures can significantly enhance our intraoperative decision making and overall targeting strategy. Disclosures Dr Machado is a consultant for Spinal Modulation, Functional Neuromodulation, and Deep Brain Innovation, has distribution rights for intellectual property with Enspire, ATI, and Cardionomics. The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. REFERENCES 1. Matias CM, Mehanna R, Cooper SE et al.   Correlation among anatomic landmarks, location of subthalamic deep brain stimulation electrodes, stimulation parameters, and side effects during programming monopolar review. Oper Neurosurg (Hagerstown) . 2015; 11( 1): 99- 109. 2. Pourfar MH, Mogilner AY. Lead angle matters: side effects of deep brain stimulation improved with adjustment of lead angle. Neuromodulation Technol Neural Interface . 2016. doi: 10.1111/ner.12476. 3. Foltynie T, Zrinzo L, Martinez-Torres I et al.   MRI-guided STN DBS in Parkinson's disease without microelectrode recording: efficacy and safety. 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J Neurosurg . 2007; 107( 5): 989- 997. Google Scholar CrossRef Search ADS PubMed  Copyright © 2017 by the Congress of Neurological Surgeons This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

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Operative NeurosurgeryOxford University Press

Published: Aug 2, 2017

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