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Comprehensive characterization of intracranial hemorrhage in deep brain stimulation: a systematic review of literature from 1987 to 2023

Cletus Cheyuo, Artur Vetkas, Can Sarica, Suneil K. Kalia, Mojgan Hodaie, and Andres M. Lozano

OBJECTIVE

Deep brain stimulation (DBS) is an effective treatment for medically refractory movement disorders and other neurological conditions. To comprehensively characterize the prevalence, locations, timing of detection, clinical effects, and risk factors of DBS-related intracranial hemorrhage (ICH), the authors performed a systematic review of the published literature.

METHODS

PubMed, EMBASE, and Web of Science were searched using 2 concepts: cerebral hemorrhage and brain stimulation, with filters for English, human studies, and publication dates 1980–2023. The inclusion criteria were the use of DBS intervention for any human neurological condition, with documentation of hemorrhagic complications by location and clinical effect. Studies with non-DBS interventions, no documentation of hemorrhage outcome, patient cohorts of ≤ 10, and pediatric patients were excluded. The risk of bias was assessed using Centre for Evidence-Based Medicine Levels of Evidence. The authors performed proportional meta-analysis for ICH prevalence.

RESULTS

A total of 63 studies, with 13,056 patients, met the inclusion criteria. The prevalence of ICH was 2.9% (fixed-effects model, 95% CI 2.62%–3.2%) per patient and 1.6% (random-effects model, 95% CI 1.34%–1.87%) per DBS lead, with 49.6% being symptomatic. The ICH rates did not change with time. ICH most commonly occurred around the DBS lead, with 16% at the entry point, 31% along the track, and 7% at the target. Microelectrode recording (MER) during DBS was associated with increased ICH rate compared to DBS without MER (3.5 ± 2.2 vs 2.1 ± 1.4; p[T ≤ t] 1-tail = 0.038). Other reported ICH risk factors include intraoperative systolic blood pressure > 140 mm Hg, sulcal DBS trajectories, and multiple microelectrode insertions. Sixty percent of ICH was detected at 24 hours postoperatively and 27% intraoperatively. The all-cause mortality rate of DBS was 0.4%, with ICH accounting for 22% of deaths. Single-surgeon DBS experience showed a weak inverse correlation (r = −0.27, p = 0.2189) between the rate of ICH per lead and the number of leads implanted per year.

CONCLUSIONS

This study provides level III evidence that MER during DBS is a risk factor for ICH. Other risk factors include intraoperative systolic blood pressure > 140 mm Hg, sulcal trajectories, and multiple microelectrode insertions. Avoidance of these risk factors may decrease the rate of ICH.

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Letter to the Editor. Clinical Rating Scale for Tremor: a needed clarification

Can Sarica, Anton Fomenko, Christian Iorio-Morin, Ajmal Zemmar, Kazuaki Yamamoto, Artur Vetkas, Andres M. Lozano, and Alfonso Fasano

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Idiopathic Parkinson’s disease and chronic pain in the era of deep brain stimulation: a systematic review and meta-analysis

Oliver Flouty, Kazuaki Yamamoto, Jurgen Germann, Irene E. Harmsen, Hyun Ho Jung, Cletus Cheyuo, Ajmal Zemmar, Vanessa Milano, Can Sarica, and Andres M. Lozano

OBJECTIVE

Pain is the most common nonmotor symptom of Parkinson’s disease (PD) and is often undertreated. Deep brain stimulation (DBS) effectively mitigates the motor symptoms of this multisystem neurodegenerative disease; however, its therapeutic effect on nonmotor symptoms, especially pain, remains inconclusive. While there is a critical need to help this large PD patient population, guidelines for managing this significant disease burden are absent. Herein, the authors systematically reviewed the literature and conducted a meta-analysis to study the influence of traditional (subthalamic nucleus [STN] and globus pallidus internus [GPi]) DBS on chronic pain in patients with PD.

METHODS

The authors performed a systematic review of the literature and a meta-analysis following PRISMA guidelines. Risk of bias was assessed using the levels of evidence established by the Oxford Centre for Evidence-Based Medicine. Inclusion criteria were articles written in English, published in a peer-reviewed scholarly journal, and about studies conducting an intervention for PD-related pain in no fewer than 5 subjects.

RESULTS

Twenty-six studies were identified and included in this meta-analysis. Significant interstudy heterogeneity was detected (Cochran’s Q test p < 0.05), supporting the use of the random-effects model. The random-effects model estimated the effect size of DBS for the treatment of idiopathic pain as 1.31 (95% CI 0.84–1.79). The DBS-on intervention improved pain scores by 40% as compared to the control state (preoperative baseline or DBS off).

CONCLUSIONS

The results indicated that traditional STN and GPi DBS can have a favorable impact on pain control and improve pain scores by 40% from baseline in PD patients experiencing chronic pain. Further trials are needed to identify the subtype of PD patients whose pain benefits from DBS and to identify the mechanisms by which DBS improves pain in PD patients.

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Clinical outcomes and complications of peripheral nerve field stimulation in the management of refractory trigeminal pain: a systematic review and meta-analysis

Can Sarica, Christian Iorio-Morin, David H. Aguirre-Padilla, Michelle Paff, Samuelle-Arianne Villeneuve, Artur Vetkas, Kazuaki Yamamoto, Nardin Samuel, Vanessa Milano, Aaron Loh, Brendan Santyr, Ajmal Zemmar, Andres M. Lozano, and Mojgan Hodaie

OBJECTIVE

Peripheral nerve field stimulation (PNFS) is a tool in the armamentarium of treatment options for trigeminal pain. The efficacy of this modality in mitigating trigeminal pain remains unclear. The aim of this study was to examine the existing literature on PNFS and elucidate pain score outcomes associated with its use in patients with trigeminal pain.

METHODS

A systematic review and meta-analysis was performed in accordance with the PRISMA framework. The PubMed, Web of Science, and Scopus databases were queried on June 10, 2020. Studies reporting pain outcomes in more than 5 adult patients treated with PNFS for facial pain were included. The primary outcome of the study was the mean difference in the visual analog scale (VAS) score from the last follow-up to baseline, and it was analyzed by an inverse-variance, random-effect model. The risk of bias was assessed using the Newcastle-Ottawa Scale and a funnel plot.

RESULTS

Of the 4597 studies screened for inclusion, 46 relevant full-text articles were assessed for eligibility. Eleven observational cohort studies from the 46 articles were found to be eligible, and reported on a total of 109 patients. In 86% (94/109) of cases, trial stimulation was successful and followed by a permanent system implantation. VAS scores improved by 75% (mean difference 6.32/10 points, 95% CI 5.38–7.27 points) compared to baseline. Seventy-six percent (42/55) of patients became medication free or required lower doses of medications. The complication rate necessitating surgical revision was estimated at 32% per procedure.

CONCLUSIONS

These findings support the belief that PNFS provides effective, long-term pain control for trigeminal pain. Statistical heterogeneity was considerable across all studies. Future work should be aimed at conducting double-blind randomized controlled trials to determine the utility of PNFS for treating various forms of trigeminal pain for which limited therapeutic options exist.

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Successful magnetic resonance–guided focused ultrasound treatment of tremor in patients with a skull density ratio of 0.4 or less

Artur Vetkas, Alexandre Boutet, Can Sarica, Jurgen Germann, Dave Gwun, Kazuaki Yamamoto, Hyun Ho Jung, Afnan Alkhotani, Nardin Samuel, Stefan Lang, Christopher R. Conner, Gavin J. B. Elias, Cletus Cheyuo, Clement Chow, Brendan Santyr, Christian Iorio-Morin, Andrew Z. Yang, Carolina Candeias da Silva, Alfonso Fasano, Suneil K. Kalia, and Andres M. Lozano

OBJECTIVE

The use of magnetic resonance–guided focused ultrasound (MRgFUS) for the treatment of tremor-related disorders and other novel indications has been limited by guidelines advocating treatment of patients with a skull density ratio (SDR) above 0.45 ± 0.05 despite reports of successful outcomes in patients with a low SDR (LSDR). The authors’ goal was to retrospectively analyze the sonication strategies, adverse effects, and clinical and imaging outcomes in patients with SDR ≤ 0.4 treated for tremor using MRgFUS.

METHODS

Clinical outcomes and adverse effects were assessed at 3 and 12 months after MRgFUS. Outcomes and lesion location, volume, and shape characteristics (elongation and eccentricity) were compared between the SDR groups.

RESULTS

A total of 102 consecutive patients were included in the analysis, of whom 39 had SDRs ≤ 0.4. No patient was excluded from treatment because of an LSDR, with the lowest being 0.22. Lesioning temperatures (> 52°C) and therapeutic ablations were achieved in all patients. There were no significant differences in clinical outcome, adverse effects, lesion location, and volume between the high SDR group and the LSDR group. SDR was significantly associated with total energy (rho = −0.459, p < 0.001), heating efficiency (rho = 0.605, p < 0.001), and peak temperature (rho = 0.222, p = 0.025).

CONCLUSIONS

The authors’ results show that treatment of tremor in patients with an LSDR using MRgFUS is technically possible, leading to a safe and lasting therapeutic effect. Limiting the number of sonications and adjusting the energy and duration to achieve the required temperature early during the treatment are suitable strategies in LSDR patients.