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Bilateral deep brain stimulation of the subthalamic nucleus in primary Meige syndrome

Shikun Zhan, Fafa Sun, Yixin Pan, Wei Liu, Peng Huang, Chunyan Cao, Jing Zhang, Dianyou Li, and Bomin Sun

OBJECTIVE

Subthalamic nucleus deep brain stimulation has been shown to be effective in reducing symptoms of primary Meige syndrome. However, assessments of its efficacy and safety have been limited to several case reports and small studies.

METHODS

The authors performed a retrospective study to assess the efficacy and safety of bilateral subthalamic nucleus stimulation in 15 patients with primary Meige syndrome who responded poorly to medical treatments or botulinum toxin injections. Using the movement and disability subscores of the Burke-Fahn-Marsden Dystonia Rating Scale, the authors evaluated the severity of patients’ dystonia and related before surgery and at final follow-up during neurostimulation. The movement scale was assessed based on preoperative and postoperative video documentation by an independent rater who was unaware of each patient’s neurostimulation status. Quality of life was assessed with the Medical Outcomes Study 36-Item Short-Form General Health Survey.

RESULTS

The dystonia movement subscores in 14 consecutive patients improved from 19.3 ± 7.6 (mean ± standard deviation) before surgery to 5.5 ± 4.5 at final follow-up (28.5 ± 16.5 months), with a mean improvement of 74% (p < 0.05). The disability subscore improved from 15.6 ± 4.9 before surgery to 6.1 ± 3.5 at final follow-up (p < 0.05). In addition, the postoperative SF-36 scores increased markedly over those at baseline. The authors also found that bilateral stimulation of the subthalamic nucleus immediately improved patient symptoms after stimulation and required lower stimulation parameters than those needed for pallidal deep brain stimulation for primary Meige syndrome. Four adverse events occurred in 3 patients; all of these events resolved without permanent sequelae.

CONCLUSIONS

These findings provide further evidence to support the long-term efficacy and safety of subthalamic nucleus stimulation as an alternative treatment for patients with medically intractable Meige syndrome.

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Deep brain stimulation telemedicine programming during the COVID-19 pandemic: treatment of patients with psychiatric disorders

Zhengyu Lin, Chencheng Zhang, Yingying Zhang, Lulin Dai, Valerie Voon, Dianyou Li, and Bomin Sun

OBJECTIVE

The ongoing coronavirus disease 2019 (COVID-19) pandemic has considerably affected the delivery of postoperative care to patients who have undergone deep brain stimulation (DBS) surgery. DBS teleprogramming technology was developed and deployed in China before the COVID-19 outbreak. In this report, the authors share their experiences with telemedical DBS treatment of patients with psychiatric disorders during the COVID-19 outbreak.

METHODS

Four patients (2 with obsessive-compulsive disorder, 1 with major depressive disorder, and 1 with anorexia nervosa) underwent DBS surgery at Ruijin Hospital and received continuous postoperative DBS telemedicine case management from January 2020 to July 2020. DBS teleprogramming, individualized psychological support, and medical consultations were provided via the authors’ DBS telemedicine platform, which also incorporated a synchronous real-time video communication system.

RESULTS

Forty-five DBS telemedicine sessions were conducted; there was no unexpected loss of network connection during the sessions. Of these, 28 sessions involved DBS teleprogramming. Adjustments were made to the stimulation voltage, frequency, pulse width, and contact site in 21, 12, 9, and 9 sessions, respectively. Psychological support and troubleshooting were provided during the remaining telemedicine sessions. Modest to substantial clinical improvements after DBS surgery were observed in some but not all patients, whereas stimulation-related side effects were reported by 2 patients and included reversible sleep and mood problems, headache, and a sensation of heat.

CONCLUSIONS

DBS telemedicine seems to offer a feasible, safe, and efficient strategy for maintaining the delivery of medical care to psychiatric patients during the COVID-19 outbreak. The authors propose that implementation of a comprehensive DBS telemedicine system, which combines DBS teleprogramming with psychological counseling, medical consultations, and medication prescriptions and delivery, could be an efficient and effective approach to manage the mental health and quality of life of patients with psychiatric disorders during future local or global public health crises.

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Remote video-based outcome measures of patients with Parkinson’s disease after deep brain stimulation using smartphones: a pilot study

Xinmeng Xu, Zhitong Zeng, Yijia Qi, Kang Ren, Chencheng Zhang, Bomin Sun, and Dianyou Li

OBJECTIVE

To provide better postoperative healthcare for patients with Parkinson’s disease (PD) who received deep brain stimulation (DBS) surgery and to allow surgeons improved tracking of surgical outcomes, the authors sought to examine the applicability and feasibility of remote assessment using smartphones.

METHODS

A disease management mobile application specifically for PD was used to perform the remote assessment of patients with PD who underwent DBS. Connection with patients was first established via a phone call or a social application, and instructions for completing the remote assessment were delivered. During the video-based virtual meeting, three nonmotor assessment scales measuring the quality of life and mental state, and a modified version of the Movement Disorder Society–sponsored revision of the Unified Parkinson’s Disease Rating Scale, part III (MDS-UPDRS III) measuring motor abilities were evaluated. After the assessment, a report and the satisfaction questionnaire were sent to the patient.

RESULTS

Overall, 22 patients were recruited over a 4-week period. Among those, 18 patients completed the assessment on the mobile application. The mean duration was 41.3 minutes for video assessment and 17.5 minutes for nonmotor assessment via telephone. The mean estimated cost was 427.68 Chinese yuan (CNY) for an in-person visit and 20.91 CNY for a virtual visit (p < 0.001). The mean time estimate for an in-person visit was 5.51 hours and 0.68 hours for a virtual visit (p = 0.002). All patients reported satisfaction (77.78% very satisfied and 22.22% satisfied) with the virtual visit and were specifically impressed by the professionalism and great attitude of the physician assistant. The majority of patients agreed that the evaluation time was reasonable (50% totally agree, 44.44% agree, and 5.56% neither agree nor disagree) and all patients expressed interest in future virtual visits (61.11% very willingly and 38.89% willingly). No adverse events were observed during the virtual visit.

CONCLUSIONS

Innovation in remote assessment technologies was highly feasible for its transforming power in the clinical management of patients with PD who underwent DBS and research. Video-based remote assessment offered considerable time and resource reduction for both patients and doctors. It also increased safety and was a well-accepted, favored tool. Finally, the results of this study have shown there is potential to combine remote assessment tools with real-life clinical visits and other telemedical technologies to collectively benefit the postoperative healthcare of patients with PD undergoing DBS.

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Unilateral pallidotomy as a potential rescue therapy for cervical dystonia after unsatisfactory selective peripheral denervation

Yijie Lai, Peng Huang, Chencheng Zhang, Liangyun Hu, ME, Zhengdao Deng, Dianyou Li, Bomin Sun, Wei Liu, and Shikun Zhan

OBJECTIVE

Selective peripheral denervation (SPD) is a widely accepted surgery for medically refractory cervical dystonia (CD), but when SPD has failed, the available approaches are limited. The authors investigated the results from a cohort of CD patients treated with unilateral pallidotomy after unsatisfactory SPD.

METHODS

The authors retrospectively analyzed patients with primary CD who underwent unilateral pallidotomy after SPD between April 2007 and August 2019. The Toronto Western Spasmodic Torticollis Rating Scale (TWSTRS) was used to evaluate symptom severity before surgery, 7 days postsurgery, 3 months postsurgery, and at the last follow-up. TWSTRS subscores for disability and pain and the 24-item Craniocervical Dystonia Questionnaire (CDQ-24) were used to assess quality of life.

RESULTS

At a mean final follow-up of 5 years, TWSTRS severity subscores and total scores were significantly improved (n = 12, mean improvement 57.3% and 62.3%, respectively, p = 0.0022 and p = 0.0022), and 8 of 12 patients (66.7%) were characterized as responders (improvement ≥ 25%). Patients with rotation symptoms before pallidotomy showed greater improvement in TWSTRS severity subscores than those who did not (p = 0.049). The most common adverse event was mild upper-limb weakness (n = 3). Patients’ quality of life was also improved.

CONCLUSIONS

Unilateral pallidotomy seems to offer an effective and safe option for patients with CD who have otherwise experienced limited benefits from SPD.

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Habenula deep brain stimulation for intractable schizophrenia: a pilot study

Yuhan Wang, Chencheng Zhang, Yingying Zhang, Hengfen Gong, Jun Li, Haiyan Jin, Dianyou Li, Dengtang Liu, and Bomin Sun

Schizophrenia is a psychiatric disorder associated with significant morbidity and mortality. Although antipsychotic medications and electroconvulsive therapy can be used to manage the clinical symptoms of schizophrenia, a substantial portion (10%–30%) of patients do not clinically respond to these treatments or cannot tolerate the side effects. Recently, deep brain stimulation (DBS) has emerged as a promising safe and effective therapeutic intervention for various psychiatric disorders. Here, the authors explore the utility of DBS of the habenula (HB) in the clinical management of 2 young adult male patients with severe, chronic, and treatment-resistant schizophrenia. After HB DBS surgery, both patients experienced improvements in clinical symptoms during the first 6 months of treatment. However, only 1 patient retained the clinical benefits and reached a favorable outcome at 12-month follow-up. The symptoms of the other patient subsequently worsened and became so profound that he needed to be hospitalized at 10-month follow-up and withdrawn from further study participation. It is tentatively concluded that HB DBS could ultimately be a relatively safe and effective surgical intervention for certain patients with treatment-resistant schizophrenia.

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BOLD frequency–dependent alterations in resting-state functional connectivity by pallidal deep brain stimulation in patients with Parkinson’s disease

Zhenghao Li, Yijie Lai, Jun Li, Naying He, Dianyou Li, Fuhua Yan, Yuyao Zhang, Chencheng Zhang, Bomin Sun, and Hongjiang Wei

OBJECTIVE

Functional MRI (fMRI) has been used to investigate the therapeutic mechanisms underlying deep brain stimulation (DBS) for Parkinson’s disease (PD). However, the alterations in stimulation site–seeded functional connectivity induced by DBS at the internal globus pallidus (GPi) remain unclear. Furthermore, whether DBS-modulated functional connectivity is differentially affected within particular frequency bands remains unknown. The present study aimed to reveal the alterations in stimulation site–seeded functional connectivity induced by GPi-DBS and to examine whether there exists a frequency band effect in blood oxygen level–dependent (BOLD) signals related to DBS.

METHODS

Patients with PD receiving GPi-DBS (n = 28) were recruited for resting-state fMRI with DBS on and DBS off under a 1.5-T MR scanner. Age- and sex-matched healthy controls (n = 16) and DBS-naïve PD patients (n = 24) also received fMRI scanning. The alterations in stimulation site–seeded functional connectivity in the stimulation-on state versus stimulation-off state, as well as the relationship between alterations in connectivity and improvement in motor function induced by GPi-DBS, were examined. Furthermore, the modulatory effect of GPi-DBS on the BOLD signals within the 4 frequency subbands (slow-2 to slow-5) was investigated. Finally, the functional connectivity of the motor-related network, consisting of multiple cortical and subcortical regions, was also examined among the groups. In this study, p < 0.05 with Gaussian random field correction indicates statistical significance.

RESULTS

Functional connectivity seeding from the stimulation site (i.e., the volume of tissue activated [VTA]) increased in the cortical sensorimotor areas and decreased in the prefrontal regions with GPi-DBS. Alterations in connectivity between the VTA and the cortical motor areas were correlated with motor improvement by pallidal stimulation. The alterations in connectivity were dissociable between the frequency subbands in the occipital and cerebellar areas. The motor network analysis indicated decreased connectivity among most cortical and subcortical regions but increased connectivity between the motor thalamus and the cortical motor area in patients with GPi-DBS compared with those in DBS-naïve patients. The DBS-induced decrease in several cortical-subcortical connectivities within the slow-5 band correlated with motor improvement with GPi-DBS.

CONCLUSIONS

These findings indicate that the alterations in functional connectivity from the stimulation site to the cortical motor areas, as well as multiple connectivities among the motor-related network, were associated with the efficacy of GPi-DBS for PD. Furthermore, the changing pattern of functional connectivity within the 4 BOLD frequency subbands is partially dissociable.

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Precise targeting of the globus pallidus internus with quantitative susceptibility mapping for deep brain stimulation surgery

Hongjiang Wei, Chencheng Zhang, Tao Wang, Naying He, Dianyou Li, Yuyao Zhang, Chunlei Liu, Fuhua Yan, and Bomin Sun

OBJECTIVE

The goal of this study was to demonstrate the use of quantitative susceptibility mapping (QSM)–based images to precisely localize the globus pallidus internus (GPi) for deep brain stimulation (DBS) planning and to enhance postsurgical visualization of the DBS lead positions.

METHODS

Presurgical T1-weighted (T1w), T2-weighted (T2w), and QSM images as well as postsurgical CT images were obtained in 29 patients with Parkinson’s disease. To enhance the contrast within the GP, a hybrid contrast was created by linearly combining T1w and QSM images. Contrast-to-noise ratios (CNRs) of the GPi on T1w, T2w, QSM, and hybrid images were compared. The CNR differences were tested using the 1-way ANOVA method. The visualization of the DBS lead position was demonstrated by merging the postsurgical CT with presurgical MR images.

RESULTS

The hybrid images yield the best CNRs for GPi depiction and the visualization of the postsurgical DBS lead position was significantly improved.

CONCLUSIONS

QSM-based images allow for confident localization of borders of the GPi that is superior to T1w and T2w images. High-contrast hybrid images can be used for precisely directed DBS targeting, e.g., GPi DBS for the treatment of advanced Parkinson’s disease.

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Parameter-based analysis of clinical efficacy of combined bed nucleus of the stria terminalis–nucleus accumbens deep brain stimulation for treatment-resistant depression

Tao Wang, Lulin Dai, Yijie Lai, Fengting Wang, Yingying Zhang, Yuhan Wang, Dianyou Li, Shikun Zhan, Liuguan Bian, and Bomin Sun

OBJECTIVE

Treatment-resistant depression (TRD) is a severely disabling psychiatric condition that responds poorly to conventional treatments. Deep brain stimulation (DBS) has been proposed for the treatment of patients with TRD in numerous studies. Several deep brain nuclei are considered as potential targets for TRD-DBS, but their clinical efficacy needs further validation. This study carried out dual-target combined stimulation of the bed nucleus of the stria terminalis (BNST) and nucleus accumbens (NAc) to investigate the effectiveness of the treatment for TRD patients.

METHODS

An 8-contact DBS electrode was used in the study with a surgical path that crossed the BNST and NAc targets. Stimulation parameters and the corresponding severity of symptoms evaluated by the 17-item Hamilton Depression Rating Scale (HAMD-17) and other scales were obtained at each follow-up. The accuracy of electrode positions, the effect of combined stimulation, and the corresponding stimulation parameters were evaluated. Sweet spot prediction models were used to assess the effective stimulation sites in the treatment.

RESULTS

The study included 23 TRD patients undergoing DBS at a single center from March 2021 to May 2023. At the last follow-up (range 4–24 months), 14 patients had responded to the treatment (HAMD-17 score improved ≥ 50%), 7 of whom had achieved clinical remission (HAMD-17 score ≤ 7). Electrode position analysis suggested that the BNST may be more important for the improvement of depressive symptoms than the NAc. Overlapped volumes of volume of tissue activated (VTA) and BNST were significantly correlated with absolute (ρleft = −0.377, p < 0.001; ρright = −0.251, p < 0.001) and percent (ρleft = −0.249, p < 0.001; ρright = −0.098, p = 0.102) changes in HAMD-17 score. The sweet spot model of HAMD-17 improvement also suggested that the VTA overlap with the dorsal side of BNST was associated with the impact on depressive symptoms (t = −4.10, p < 0.05).

CONCLUSIONS

Combined BNST-NAc stimulation of TRD can effectively improve depressive symptoms, in which the BNST seems to have a dominant therapeutic effect. The results of this study not only help to optimize the DBS programming parameters, but also offer an opportunity to further understand the differences between the two targets. In the future, larger prospective cohorts are needed to verify the results of combined BNST-NAc DBS.

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Value of functional connectivity in outcome prediction for pallidal stimulation in Parkinson disease

Yijie Lai, Naying He, Hongjiang Wei, Lifu Deng, Haiyan Zhou, Jun Li, Marcus Kaiser, Chencheng Zhang, Dianyou Li, and Bomin Sun

OBJECTIVE

Functional connectivity shows the ability to predict the outcome of subthalamic nucleus deep brain stimulation (DBS) in Parkinson disease (PD). However, evidence supporting its value in predicting the outcome of globus pallidus internus (GPi) DBS remains scarce. In this study the authors investigated patient-specific functional connectivity related to GPi DBS outcome in PD and established connectivity models for outcome prediction.

METHODS

The authors reviewed the outcomes of 21 patients with PD who received bilateral GPi DBS and presurgical functional MRI at the Ruijin Hospital. The connectivity profiles within cortical areas identified as relevant to DBS outcome in the literature were calculated using the intersection of the volume of tissue activated (VTA) and the local structures as the seeds. Combined with the leave-one-out cross-validation strategy, models of the optimal connectivity profile were constructed to predict outcome.

RESULTS

Connectivity between the pallidal areas and primary motor area, supplementary motor area (SMA), and premotor cortex was identified through the literature as related to GPi DBS outcome. The similarity between the connectivity profile within the primary motor area, SMA, pre-SMA, and premotor cortex seeding from the VTA-GPi intersection from an out-of-sample patient and the constructed in-sample optimal connectivity profile predicts GPi DBS outcome (R = 0.58, p = 0.006). The predictions on average deviated by 13.1% ± 11.3% from actual improvements. On the contrary, connectivity profiles seeding from the GPi (R = −0.12, p = 0.603), the VTA (R = 0.23, p = 0.308), the VTA outside the GPi (R = 0.12, p = 0.617), or other local structures were found not to be predictive.

CONCLUSIONS

The results showed that patient-specific functional connectivity seeding from the VTA-GPi intersection could help in GPi DBS outcome prediction. Reproducibility remains to be determined across centers in larger cohorts stratified by PD motor subtype.

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Pallidal deep brain stimulation combined with capsulotomy for Tourette’s syndrome with psychiatric comorbidity

Chencheng Zhang, Zhengdao Deng, Yixin Pan, Jing Zhang, Kristina Zeljic, Haiyan Jin, Odin van der Stelt, Hengfen Gong, Shikun Zhan, Dianyou Li, and Bomin Sun

OBJECTIVE

A current challenge is finding an effective and safe treatment for severely disabled patients with Tourette’s syndrome (TS) and comorbid psychiatric disorders, in whom conventional treatments have failed. The authors aimed to evaluate the utility of globus pallidus internus deep brain stimulation (GPi-DBS) combined with bilateral anterior capsulotomy in treating these clinically challenging patients.

METHODS

The authors conducted a retrospective review of the clinical history and outcomes of 10 severely disabled patients with treatment-refractory TS and a psychiatric comorbidity, who had undergone GPi-DBS combined with bilateral anterior capsulotomy in their hospital. At the time of surgery, patients presented mainly with obsessive-compulsive disorder and affective disorders. Clinical outcome assessments of tic and psychiatric symptoms, as well as of general adaptive functioning and quality of life, were performed at the time of surgery and at 6, 12, and between 24 and 96 months postsurgery.

RESULTS

After surgery, all patients showed significant progressive improvements in tic and psychiatric symptoms, along with improvements in general adaptive functioning and quality of life. Tic alleviation reached 64% at 12 months and 77% at the last follow-up on the Yale Global Tic Severity Scale. At the final follow-up, patients had functionally recovered and displayed no or only mild tic and psychiatric symptoms. All patients tolerated treatment reasonably well, with no serious side effects.

CONCLUSIONS

GPi-DBS combined with bilateral anterior capsulotomy seems to offer major clinical benefits to severely disabled patients with otherwise treatment-refractory TS and psychiatric comorbidities.