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High-resolution QSM for functional and structural depiction of subthalamic nuclei in DBS presurgical mapping

Alexey V. Dimov, Ajay Gupta, Brian H. Kopell, and Yi Wang

OBJECTIVE

Faithful depiction of the subthalamic nucleus (STN) is critical for planning deep brain stimulation (DBS) surgery in patients with Parkinson’s disease (PD). Quantitative susceptibility mapping (QSM) has been shown to be superior to traditional T2-weighted spin echo imaging (T2w). The aim of the study was to describe submillimeter QSM for preoperative imaging of the STN in planning of DBS.

METHODS

Seven healthy volunteers were included in this study. T2w and QSM were obtained for all healthy volunteers, and images of different resolutions were reconstructed. Image quality and visibility of STN anatomical features were analyzed by a radiologist using a 5-point scale, and contrast properties of the STN and surrounding tissue were calculated. Additionally, data from 10 retrospectively and randomly selected PD patients who underwent 3-T MRI for DBS were analyzed for STN size and susceptibility gradient measurements.

RESULTS

Higher contrast-to-noise ratio (CNR) values were observed in both high-resolution and low-resolution QSM images. Inter-resolution comparison demonstrated improvement in CNR for QSM, but not for T2w images. QSM provided higher inter-quadrant contrast ratios (CR) within the STN, and depicted a gradient in the distribution of susceptibility sources not visible in T2w images.

CONCLUSIONS

For 3-T MRI, submillimeter QSM provides accurate delineation of the functional and anatomical STN features for DBS targeting.

In Journal of Neurosurgery Volume 131: Issue 2 (Aug 2019)

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Iron concentration linked to structural connectivity in the subthalamic nucleus: implications for deep brain stimulation

Alexey Dimov, Wahaj Patel, Yihao Yao, Yi Wang, Rafael O’Halloran, and Brian H. Kopell

OBJECTIVE

The objective of this study was to investigate the relationship between iron and white matter connectivity in the subthalamic nucleus (STN) in patients undergoing deep brain stimulation (DBS) of the STN for treatment of Parkinson’s disease.

METHODS

Nine Parkinson’s disease patients underwent preoperative 3T MRI imaging which included acquisition of T1-weighted anatomical images along with diffusion tensor imaging (DTI) and quantitative susceptibility mapping (QSM). MR tractography was performed for the seed voxels located within the STN, and the correlations between normalized QSM values and the STN’s connectivity to a set of a priori chosen regions of interest were assessed.

RESULTS

A strong negative correlation was found between STN connectivity and QSM intensity for the thalamus, premotor, motor, and sensory regions, while a strong positive correlation was found for frontal, putamen, and brain stem areas.

CONCLUSIONS

Quantitative susceptibility mapping not only accurately delineates the STN borders but is also able to provide functional information about the STN functional subdivisions. The observed iron-to-connectivity correlation patterns may aid in planning DBS surgery to avoid unwanted side effects associated with DBS.

In Journal of Neurosurgery Volume 132: Issue 1 (Jan 2020)

Free access

Deep brain stimulation of the ventralis intermedius nucleus for the treatment of essential tremor

Alexander G. Chartrain, Ahmed J. Awad, Jonathan J. Rasouli, Robert J. Rothrock, and Brian H. Kopell

A 59-year-old woman with a 30-year history of essential tremor refractory to medical therapy underwent staged deep brain stimulation of the ventralis intermedius nucleus of the thalamus (VIM). Left-sided lead placement was performed first. Once in the operating room, microelectrode recording (MER) was performed to confirm the appropriate trajectory and identify the VIM border with the ventralis caudalis nucleus. MER was repeated after repositioning 2 mm anteriorly to reduce the likelihood of stimulation-induced paresthesias. Physical examination prior to permanent lead placement demonstrated micro-lesion effect, suggesting optimal trajectory. After implantation of the permanent lead, physical examination showed excellent results.

The video can be found here: https://youtu.be/nn3KRdmRCZ4.

In Neurosurgical Focus Volume 42 (2017): Issue videosuppl2 (Apr 2017): Video Atlas - Deep Brain Stimulation

Free access

Motoric impairment versus iron deposition gradient in the subthalamic nucleus in Parkinson’s disease

Weiyuan Huang, Richard Ogbuji, Liangdong Zhou, Lingfei Guo, Yi Wang, and Brian H. Kopell

OBJECTIVE

The objective of this study was to investigate the correlation between the quantitative susceptibility mapping (QSM) signal gradient of the subthalamic nucleus (STN) and motor impairment in patients with Parkinson’s disease (PD).

METHODS

All PD patients who had undergone QSM MRI for presurgical deep brain stimulation (DBS) planning were eligible for inclusion in this study. The entire STN and its three functional subdivisions, as well as the adjacent white matter (WM), were segmented and measured. The QSM value difference between the entire STN and adjacent WM (STN-WM), between the limbic and associative regions of the STN (L-A), and between the associative and motor regions of the STN (A-M) were obtained as measures of gradient and were input into an unsupervised k-means clustering algorithm to automatically categorize the overall boundary distinctness between the STN and adjacent WM and between STN subdivisions (gradient blur [GB] and gradient sharp [GS] groups). Statistical tests were performed to compare clinical and image measurements for discrimination between GB and GS groups.

RESULTS

Of the 39 study patients, 19 were categorized into the GB group and 20 into the GS group, based on quantitative cluster analysis. The GB group had a significantly higher presurgical off-medication Unified Parkinson’s Disease Rating Scale Part III score (51.289 ± 20.741) than the GS group (38.5 ± 16.028; p = 0.037). The GB group had significantly higher QSM values for the STN and its three subdivisions and adjacent WM than those for the GS group (p < 0.01). The GB group also demonstrated a significantly higher STN-WM gradient in the right STN (p = 0.01). The GB group demonstrated a significantly lower L-A gradient in both the left and the right STN (p < 0.02).

CONCLUSIONS

Advancing PD with more severe motor impairment leads to more iron deposition in the STN and adjacent WM, as shown in the QSM signal. Loss of the STN inner QSM signal gradient should be considered as an image marker for more severe motor impairment in PD patients.

In Journal of Neurosurgery Volume 135: Issue 1 (Jul 2021)

Free access

Clinical profiles and outcomes of deep brain stimulation in G2019S LRRK2 Parkinson disease

Katherine Leaver, Aaron Viser, Brian H. Kopell, Roberto A. Ortega, Joan Miravite, Michael S. Okun, Sonya Elango, Deborah Raymond, Susan B. Bressman, Rachel Saunders-Pullman, and Marta San Luciano

OBJECTIVE

The objective of this study was to evaluate clinical features and response to deep brain stimulation (DBS) in G2019S LRRK2-Parkinson disease (LRRK2-PD) and idiopathic PD (IPD).

METHODS

The authors conducted a clinic-based cohort study of PD patients recruited from the Mount Sinai Beth Israel Genetics database of PD studies. The cohort included 87 participants with LRRK2-PD (13 who underwent DBS) and 14 DBS participants with IPD enrolled between 2009 and 2017. The baseline clinical features, including motor ratings and levodopa-equivalent daily dose (LEDD), were compared among LRRK2-PD patients with and without DBS, between LRRK2-PD with DBS and IPD with DBS, and between LRRK2-PD with subthalamic nucleus (STN) and internal segment of the globus pallidus (GPi) DBS. Longitudinal motor scores (Unified Parkinson’s Disease Rating Scale–part III) and medication usage were also assessed pre- and postoperatively.

RESULTS

Compared to LRRK2-PD without DBS (n = 74), the LRRK2-PD with DBS cohort (n = 13) had a significantly younger age of onset, longer disease duration, were more likely to have dyskinesia, and were less likely to experience hand tremor at disease onset. LRRK2-PD participants were also more likely to be referred for surgery because of severe dyskinesia (11/13 [85%] vs 6/14 [43%], p = 0.04) and were less likely to be referred for medically refractory tremor (0/13 [0%] vs 6/14 [43%], p = 0.02) than were IPD patients. Among LRRK2-PD patients, both STN-DBS and GPi-DBS targets were effective, although the sample size was small for both groups. There were no revisions or adverse effects reported in the GPi-DBS group, while 2 of the LRRK2-PD participants who underwent STN-DBS required revisions and a third reported depression as a stimulation-related side effect. Medication reduction favored the STN group.

CONCLUSIONS

The LRRK2-PD cohort referred for DBS had a slightly different profile, including earlier age of onset and dyskinesia. Both the STN and GPi DBS targets were effective in symptom suppression. Patients with G2019S LRRK2 PD were well-suited for DBS therapy and had favorable motor outcomes regardless of the DBS target. LRRK2-DBS patients had longer disease durations and tended to have more dyskinesia. Dyskinesia commonly served as the trigger for DBS surgical candidacy. Medication-refractory tremor was not a common indication for surgery in the LRRK2 cohort.

In Journal of Neurosurgery Volume 137: Issue 1 (Jul 2022)

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White matter connectivity of subthalamic nucleus and globus pallidus interna targets for deep brain stimulation

Aislyn C. DiRisio, Josue M. Avecillas-Chasin, Samantha Platt, Joohi Jimenez-Shahed, Martijn Figee, Helen S. Mayberg, Ki Sueng Choi, and Brian H. Kopell

OBJECTIVE

Deep brain stimulation (DBS) of the subthalamic nucleus (STN) and globus pallidus interna (GPi) have differential therapeutic effects for Parkinson’s disease (PD) that drive patient selection. For example, GPi DBS is preferred for dystonic features and dyskinesia, whereas STN DBS has shown faster tremor control and medication reduction. Connectivity studies comparing these two targets, using patient-specific data, are still lacking. The objective was to find STN and GPi structural connectivity patterns in order to better understand differences in DBS-activated brain circuits between these two stimulation targets and to guide optimal contact selection.

METHODS

The authors simulated DBS activation along the main axis of both the STN and GPi by using volume of activated tissue (VAT) modeling with known average stimulation parameters (2.8 V and 60 μsec for STN; 3.3 V and 90 μsec for GPi). The authors modeled VATs in the anterior, middle, and posterior STN and the anterior, midanterior, midposterior, and posterior GPi. The authors generated maps of the connections shared by the patients for each VAT by using probabilistic tractography of diffusion-weighted imaging data obtained in 46 PD patients who underwent DBS (26 with STN and 20 with GPi targeting), and differences between VATs for whole-brain and distal regions of interest (prefrontal cortex, supplementary motor area, primary motor cortex, primary sensory cortex, caudate, motor thalamus, and cerebellum) were generated from structural atlases. Differences between maps were quantified and compared.

RESULTS

VATs across the STN and GPi had different structural connectivity patterns. The authors found significant connectivity differences between VATs for all regions of interest. Posterior and middle STN showed stronger connectivity to the primary motor cortex and supplementary motor area (SMA) (p < 0.001). Posterior STN had the strongest connectivity to the primary sensory cortex and motor thalamus (p < 0.001). Posterior GPi showed stronger connectivity to the primary motor cortex (p < 0.001). Connectivity to the SMA was similar for the posterior and midposterior GPi (p > 0.05), which was greater than that for the anterior GPi (p < 0.001). When both nuclei were compared, posterior and middle STN had stronger connectivity to the SMA, cerebellum, and motor thalamus than GPi (all p < 0.001). Posterior GPi and STN had similar connectivity to the primary sensory cortex.

CONCLUSIONS

On patient-specific imaging, structural connectivity differences existed between GPi and STN DBS, as measured with standardized electrical field modeling of the DBS targets. These connectivity differences may correlate with the differential clinical benefits obtained by targeting each of the two nuclei with DBS for PD. Prospective work is needed to relate these differences to clinical outcomes and to inform targeting and programming.

In Journal of Neurosurgery Publish Before Print