The current study retrospectively analyzed a series of one hundred thirty-two patients who underwent DBS surgery in Wuhan Union Hospital from December 2015 to April 2021. The 49 patients who underwent DBS surgery following the general procedure from December 2015 to October 2017 were included in the DI group (DI cohort), and the 83 patients who underwent DBS surgery following the modified procedure from March 2018 to April 2021 were included in the DP group (DP cohort). This study was approved by the local ethics committee of Tongji Medical College, Huazhong University of Science and Technology. All patients were provided informed consent for study inclusion before the DBS surgery.

All 132 surgeries were performed by one neurosurgical team (PF, WX, HYZ, XBJ, and JR). From October 2017 to March 2018, 16 patients underwent DBS surgery in our department, and the surgical procedure was modified gradually during this period, so they were excluded from the study.

For the DI cohort, the surgical procedure was as described previously, and T1- and T2-phase weighted brain MRI was obtained for the surgical plan to determine the target and paths before surgery by using the SurgiPlan Workstation (Elekta Instruments AB, Stockholm, Sweden). Gadolinium-containing contrast agents were used in patients who underwent MRI or magnetic resonance angiography (MRA) scans. Subsequently, CT scanning was performed after a Leksell head stereotactic frame was mounted under local anesthesia. The electrode implantation coordinates were determined by merging the initial target parameters on MRI and the frame coordinates on CT. The patients were kept in the supine position, and surgery was performed as follows: skin incision, drill burr hole, cross-cut the dura, expose the cortex, and implant the catheter under direct vision. With the guidance of electrophysiological recording, quadripolar DBS electrodes were bilaterally implanted into the initial targets, and then the implantable pulse generator (IPG) was connected to the electrodes.

For the DP cohort, some steps were added or modified. Additional enhanced T1-weighted brain MRI was performed using the same scanning parameters to build an image of the intracranial vessels, and then the planned puncture paths were kept away from the intracranial vessels to decrease the bleeding. After making the burr holes, dura and arachnoid membrane puncture was performed by adequate electrocoagulation of the puncture catheter with a monopole at 20 J. Water flushing was used to remove any blood, and then gel foam and fibrin glue were filled into the burr holes to block CSF loss and air inflow.

Data were collected and evaluated by two independent neurosurgeons (YXW and HT) who were involved in the surgery. Before the surgery, the clinical characteristics of all of the patients were recorded, and MRI/CT scans were taken routinely. During the surgery, relevant parameters, such as intraoperative electrophysiological signal length (IESL), stimulating electrode placement depth, the timing of the electrode adjustment, and implantation duration, were recorded. After the surgery, a postoperative 2 mm cranial CT scan was obtained within 8 h. Then, the postoperative pneumocephalus volume (PPV) and CSF loss volume were determined by volumetric segmentation using Osirix v.3.6.1 software. The PPV was calculated on air-present CT using the formula: volume = (A × B × C)/2, where A is the slice thickness of cranial air, B is the largest diameter of the air volume on a single slice, and C is the largest diameter of air measured orthogonally from the cortex to the skull. The magnitude of cortical brain shift (CBS), which equals C, was also examined.

At the same time, postoperative cranial CT and preoperative MR were fused to calculate the electrode fusion error (EFE), which is the maximum distance from the implanted electrode to the planned path, on the SurgiPlan Workstation. Before initiating the IPG programming, a 2 mm cranial CT was scanned again and imported to Lead-DBS software (www.lead-dbs.org) and reconstructed to show the three-dimensional electrode locations with preoperative MRI.

The following clinical characteristics were also collected for further analysis: age, sex, hospitalization time, DBS target, electrode implantation duration, perioperative cerebral haematoma, skin erosion, and epilepsy.

Metrology data were statistically analyzed to obtain mean and median values. Student's t-test was used to compare the means of continuous variables between two groups. Target precision and bias were compared between the two groups using the chi-square test. Probability values <0.05 were defined as statistically significant. All procedures were performed with GraphPad Prism 8.

The current study retrospectively analyzed one hundred thirty-two consecutive patients (60 women and 72 men) who underwent DBS surgery in Wuhan Union Hospital from December 2015 to February 2021. All 132 patients completed at least 3 months of follow-up. From October 2017 to March 2018, the surgical procedure was modified gradually with continuous improvement and innovation of the surgical experience, and 16 patients who underwent DBS surgery in our department were excluded from this study because they did not meet the inclusion criteria completely.

According to the surgical procedures and timetable, these 132 patients were classified into two cohorts (DI cohort and DP cohort). No significant difference in age, sex, or hospitalization time was observed between these two groups (p > 0.05). In the DI cohort, 39 patients with PD underwent subthalamic nucleus (STN)-DBS surgery under local anesthesia and 10 patients with dystonia underwent globus pallidus internus (Gpi)-DBS surgery under general anesthesia. In the DP cohort of 61 patients with PD and 22 patients with dystonia, 72 patients underwent STN-DBS surgery, 11 patients underwent Gpi-DBS surgery, 13 patients underwent local anesthesia surgery, and 70 patients underwent general anesthesia surgery. The clinical characteristics of all 132 patients in the two cohorts who underwent DBS surgery in Wuhan Union Hospital are shown in Table 1.

In the general procedure of DBS surgery, dural cross-incision could provide direct vision to expose the cortex and implant the puncture catheter, but CSF loss and air inflow could occur. In the modified procedure, we opened the dura and arachnoid membrane by adequate electrocoagulation with a monopole at 20 J. The puncture catheter could deliver energy from the monopole and penetrate through the dura and arachnoid membrane, as shown in Supplementary Video 1. Water flushing could rapidly remove any blood. Then, gel foam and fibrin glue are filled into the burr holes to block CSF loss and air inflow, as shown in Figure 1A. This modified step could prevent CSF loss and brain shift, so the electrodes could be implanted along the paths in accordance with the plan.

To decrease the rate of DP-induced hemorrhage, a similar method of stereotactic electroencephalography surgery was performed in the modified procedure of DBS surgery. Additional enhanced T1-weighted brain MRI with the same parameters was obtained to build an image of the intracranial vessels, and then the electrode trajectory was kept away from the intracranial vessels in the surgery plan, as shown in Figure 1B. This additional step could avoid perioperative cranial hemorrhage without direct vision to the maximum extent.

The selected cases present a comparison of brain shifts between the DI cohort and the DP cohort, as shown in Table 2. In the implantation period, the one-trajectory rate of MER was similar on the first side between these two cohorts (p = 0.1279), and it was lower in the DP cohort on the second side (p = 0.0018). Compared with the DP cohort, the DI cohort always took a long time to obtain satisfactory intraoperative MER signs or test stimulation effects (2.02 ± 0.77 h vs. 1.27 ± 0.56 h, p < 0.0001). The IESLs of the STN (5.16 ± 1.12 mm vs. 5.42 ± 0.82 mm) and Gpi (6.03 ± 2.76 mm vs. 6.86 ± 1.95 mm), which were used to identify the implanted location of electrodes, were not different between the two cohorts (p > 0.05).

A postoperative cranial CT was always taken within 8 h to check for the possibility of intracranial hemorrhage and pneumatosis. The PPV and CSF loss volume were much lower in the DP cohort (3.1 ± 3.7 ml) than in the DI cohort (12.5 ± 11.3 ml, p < 0.0001). The CBS was also lower in the DP cohort (4.5 ± 3.9 mm vs. 0.4 ± 1.9 mm, p < 0.0001), even though some cases showed no significant postoperative intracranial pneumatosis in the DP cohort. When the postoperative CT IS fused with perioperative MR to calculate the implantation error, as shown in Figure 2, the DP cohort implanted electrodes with a shorter EFE (0.86 ± 0.34 mm vs. 0.36 ± 0.36 mm, p < 0.0001). In brief, the modified procedure could reduce the brain shift in DBS surgery, as shown in Figure 3.

Intracranial hemorrhage is a concern in DBS surgery, especially when a puncture catheter is implanted without direct vision in the modified procedure (4). Electrode implantation-related hemorrhage occurs on only one side in a total of 166 sides in the DP cohort, while there is also one affected side in a total of 98 sides in the DI cohort, as shown in Table 1. These two patients did not require any further surgical intervention. All 132 patients finished the initial IPG programming, and at least 3 months of follow-up, there was no skin erosion or stimulation side effects (such as worsening of balance, motor function, and dysarthria in either cohort. Furthermore, arachnoid membrane puncture and cortex damage by electrocoagulation of the puncture catheter did not seem to increase the incidence of epilepsy in the DP cohort.