Simultaneous dual-target magnetic resonance-guided focused ultrasound treatment for patients with tremor-dominant Parkinson’s disease

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Abstract

Introduction. Non-invasive magnetic resonance-guided focused ultrasound (MRgFUS) is a new neurosurgical treatment option for tremor-dominant Parkinson’s disease (TDPD). Outcomes of ablation with dual targeting of two subcortical nuclei to improve functional treatment results are yet to be explored.

Aim. This study aimed to evaluate the safety and efficacy of MRgFUS with simultaneous unilateral ablation of two cerebral targets in patients with TDPD.

Materials and methods. A total of 82 TDPD patients (20 women, 62 men; median age 65.0 [52.5; 70,0] years) received unilateral MRgFUS, i.e. ventrointermedial (VIM) nucleus thalamotomy and/or pallidothalamotractotomy (PTT). Motor symptoms, including tremor, were assessed using MDS-Unified Parkinson’s Disease Rating Scale Part III (MDS-UPDRS-III). VIM, PTT, and VIM + PTT ablation was received by 34, 12, and 36 patients, respectively.

Results. After surgery, MDS-UPDRS-III score improved by 40.1% (30.2; 51.7) without early or late-onset serious complications. Tremor returned in 18 patients (all after VIM thalamotomy); 9 of them successfully underwent re-treatment 9–12 months after the first procedure. Simultaneous dual-target (VIM + PPT) intervention was successfully received by 36 patients without any serious complications. A total of 89.3% and 69.7% of patients remained relapse-free in the dual-target and single-target groups, respectively (p = 0.039).

Conclusion. Simultaneous dual-target (VIM and PTT) MRgFUS showed favorable safety and efficacy profiles and can be considered a symptomatic treatment option for TDPD patients.

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Introduction

Parkinson’s disease (PD) is one of the most common progressive neurodegenerative disorders. The incidence of PD is 5 to 35 per 100,000 person-years [1–4]. In the next 20 years, the prevalence of PD is expected to double [5], and, without any new effective treatment options, this might lead to a significant increase in social and economic disease burden [6].

Medication therapy to manage symptoms of neurotransmitter imbalance in the brain is indicated to patients with tremor-dominant Parkinson disease (TDPD). If there no alternative medication treatment options, patients are usually administered functional neurosurgery with deep brain stimulation (DBS) or stereotactic ablation: radiofrequency ablation, gamma knife, or magnetic resonance guided focused ultrasound surgery (MRgFUS) [7–14]. Before widespread introduction of DBS, destructive surgery with an efficacy of 50–80% was the leading treatment option for PD symptoms [11, 15]. Since the end of the 20th century, DBS has become the leading neurosurgery option for PD [16–18]. Recently, ablative treatment methods have become popular again due to the introduction of MRgFUS, which allows managing movement disorders with high accuracy and avoiding any surgical incisions, anesthesia, long hospitalization, and pain [11, 19–21].

MRgFUS involves a combination of two procedures: high-intensity focused ultrasound and MRI, which are used to plan the target point and conduct thermometry in real time. Bond et al. in 2017 were one of the first to describe successful treatment of PD-associated tremor by MRgFUS in the ventral intermediate thalamic nucleus in 27 patients [22]. Among the authors who evaluated long-term results of MRgFUS in patients with PD, A. Sinai et al. reported the longest follow-up in 26 TDPD patients after VIM-ablation (median follow-up 36 months, range 12–60 months) [23]. Treatment resulted in 100% improvement in tremor in 23 patients and 90% improvement in 3 patients. In 2 patients tremor returned completely and in 8 patients there was partial return of tremor. This study demonstrated that unilateral MRgFUS VIM-thalamotomy in TDPD patients was effective and safe and provided long-term response. Heading to the premotor cortex, several important tracts (pallidothalamic, cerebellothalamic, and vestibulothalamic) converge in the VIM nucleus, and this makes it an optimal candidate for managing tremor and justifies intervention in this area [15, 24].

Attempts to perform MRgFUS ablation of the subthalamic nucleus (STN) were described by R. Martínez-Fernández et al. However, analysis of their results showed that this intervention, compared with other targets, was associated with a higher incidence of adverse effects (such as ballism, chorea, paresis, speech disturbances, and gait disturbances) with a similar efficacy [25]. With such adverse effects developing after subthalamotomy (with some of them persisting for up to one year or more), many medical centers prefer to target the VIM nucleus, which has become the key target for the treatment of essential tremor and the most common target for tremor in PD.

No effect on hypobradykinesia and muscle rigidity is a disadvantage of targeting the VIM nucleus [26]. Meanwhile, targeting the pallidothalamic tract (PTT) at the level where the Forel’s fields H1 and H2 converge was shown to reduce tremor, rigidity, and hypobradykinesia by an average of 70–93% while leaving the thalamus intact [20]. M.N. Gallay et al. assessed MRgFUS pallidothalamic tractotomy results in 51 patients with late-stage TDPD and complications of levodopa treatment (dyskinesia and fluctuations) [27]. They found percentage reductions of 84% for tremor, 70% for rigidity, and 73% for hypokinesia with almost complete suppression of levodopa-induced dyskinesia. This study showed that pallidothalamic tractotomy is very promising for the treatment of TDPD and complications of levodopa treatment.

Numerous studies have been conducted to evaluate MRgFUS with ablation of one target, while the feasibility, safety, and efficacy of simultaneous dual targeting are barely represented in available literature. A single study published in 2023 described 3 TDPD patients who received stepwise dual-target MRgFUS with VIM and PTT ablation [28]. All patients tolera- ted the two treatment steps adequately without any complications.

Aim. Our study aimed to evaluate the safety and efficacy of simultaneous unilateral dual-target MRgFUS in TDPD patients.

Materials and methods

Treatment with a MRgFUS system (ExAblate 4000, Insightec) was received by 82 patients (20 women and 62 men) with TDPD. Median patients’ age was 65.0 [52.5; 70] years. Mean age was 64.5 (55; 70.5) for men and 63.0 (61.0; 72.0) for women with no statistically significant gender differences (p = 0.95, Wilcoxon’s test). This prospective study included patients who received MRgFUS treatment at V.S. Buzaev International Medical Center from May 05, 2020 to July 29, 2023.

PD was diagnosed based on the PD diagnostic criteria of the International Parkinson and Movement Disorder Society [29]; the stage was determined using the Hoehn–Yahr functional scale [30]; and disease severity was assessed using the Movement Disorder Society Unified Parkinson’s Disease Ra-ting Scale (MDS-UPDRS), Part III (MDS-UPDRS-III) [31, 32]. A total of 37 and 28 patients had Hoehn and Yahr Rating Scale stage 2 and 3, respectively. Median MDS-UPDRS-III score before treatment was 54 (43; 65).

Eligibility criteria for the neurosurgical intervention:

  1. idiopathic PD lasting for 2 years or more;
  2. age over 30 years;
  3. persistence of tremor when using standard levodopa agents (at least 500 mg) or side effects with required doses of standard levodopa agents;
  4. on-medication fluctuations (on-off phenomenon) or dyskinesia;
  5. tremor intensity score at rest and/or hypokinesia score of ≥ 3–4;
  6. no significant cognitive impairment (i.e. total Montreal Cognitive Function Assessment Scale score of at least 20) and no psychotic disorders;
  7. bone ultrasound permeability factor of ≥ 0.35;
  8. no current treatment with anticoagulants and/or antiplatelet agents, no brain tumors or vascular malformations;
  9. no contraindications to MRI, such as claustrophobia or incompatible implants.

All patients were informed about DBS but did not consider it for several reasons (fear of a device in the brain; difficulties with access to medical centers that adjust DBS parameters due to remoteness of patients’ place of residence, etc.). During the screening period for MRgFUS, all patients also underwent brain MRI with the SWI/SWAN sequence, which has a certain diagnostic value in PD [33, 34].

We described MRgFUS in detail before [12]. In all cases, unilateral intervention was performed; the side of intervention was chosen as a joint decision with the patient and their relatives, considering severity of their symptoms or dominant limb. Median bone ultrasound permeability factor was 0.48 (0.41; 0.58); median treatment duration was 97.2 (73.6; 126.4) min; median number of sonications was 11 (9.5; 13.0).

We chose two targets for MRgFUS: VIM and PTT. The VIM nucleus was used in first patients because this target was approved earlier (in 2018) [12]. After PTT tractotomy was approved in November 2021, targets were selected for each patient in accordance with their clinical status (presence of severe muscle rigidity, hypokinesia, or disabling tremor) [35]. Of 82 treated patients, 34 received VIM, 12 PTT, and 36 VIM + PTT thalamotomy. A total of 51 and 31 patients received left-sided and right-sided interventions, respectively.

After treatment, all patients were followed up according to the approved protocol with clinical neurological examination and brain MRI at Months 1, 3, 6, and 12.

Statistical analysis was performed in x86_64-apple-darwin17.0 platform under macOS Monterey v. 12.0.1 in R v. 4.2.1 software package distributed under open license. Continuous numerical variables were tested for normal distribution using the Shapiro–Wilk test. Non-parametric methods were used in case of a relatively small number of observations and no normal distribution. Dependent groups were compared using the paired Wilcoxon test, and independent groups were compared using the Wilcoxon test. If there were more than two groups, the Kruskal–Wallis comparison method was used. Spearman correlation analysis was performed. Data were evaluated visually using graphs plotted using functions built into R. Time to return of symptoms was analyzed by Kaplan–Meier survival methods using survival v. 0.4.9 and survminer v. 0.4.9 packages.

Results

Positive MDS-UPDRS-III response to MRgFUS was achieved in all TDPD patients. Median score before and after surgery was 54 (43; 65) and 31 (24; 39), respectively, p < 0.00001 (Fig. 1). No statistically significant differences were found in treatment results between men and women (p = 0.68).

 

Fig. 1. MRgFUS treatment response (score, before and after) in TDPD patients.

*p < 0.00001, Wilcoxon’s test.

 

Evaluation of MRgFUS results by target (Fig. 2) showed greater improvement with PTT or VIM + PTT targets (p < 0.001, Kruskal–Wallis method). Improvement was 32.0% (24.5; 40.2) in the VIM group, 50.0% (40.3; 57.5) in the VIM + PTT group, and 40.1% (37.2; 58.7) in the PTT group; differences were statistically significant (p < 0.001, Kruskal–Wallis test). If tremor persisted after a sufficient PTT lesion, the patient received a second ablation intervention in another target. Fig. 3 shows a TDPD patient’s MRI scan after MRgFUS treatment in both PTT and VIM.

 

Fig. 2. Percentage improvement achieved in TDPD patients after MRgFUS (MDS-UPDRS, part III) vs. baseline by different targets.

*p < 0.001, Kruskal–Wallis method.

 

Fig. 3. Patient’s MRI scan 2 h after simultaneous right-sided PTT + VIM ablation (axial and coronary planes).

Ablation lesions are shown with arrows.

 

Statistically significant differences were found in percentage improvement (vs. baseline MDS-UPDRS-III score) between patients with isolated PTT and VIM ablation (p = 0.000024, Wilcoxon’s test). However, no statistically significant differences were found between PTT + VIM and PTT ablation groups (p = 0.9245). Median improvement in MDS-UPDRS-III score was 47.9% (38.8; 57.6) and 32% (24.2; 40.2) in patients with and without PTT thalamotomy, respectively. Median absolute improvement in MDS-UPDRS-III was 29 (21; 34) and 13.5 (10.2; 21) in patients with and without PTT ablation, respectively (p < 0.0001, Wilcoxon’s test).

A total of 73 patients received MRgFUS without any adverse effects. During the procedure, few patients developed complications related to the procedure itself: headache (n = 4), which resulted in procedure discontinuation in 1 case; increased blood pressure (n = 5); transitory obtundation (n = 1); arterial hypotension in response to medication administration during installation of the stereotactic frame (n = 2). No complications were observed after the end of treatment.

Several complications were observed in the early period after MRgFUS due to edema in the treatment target: apraxia within month 1 occurred in 6 out of 48 patients in the group with PTT ablation and 2 out of 34 in the group without PTT ablation (p = 0.32, χ2 method): 2 patients had dysarthria, 1 had decreased flow of speech, and 1 had numbness of the tip of the tongue. Most of these symptoms improved by follow-up month 6. One year after surgery, apraxia persisted in 2 and 2 patients with and without PTT ablation, respectively.

Median follow-up in TDPD patients after MRgFUS was 376 days (107.5; 612). Return of tremor (less pronounced compared with hyperkinesis before surgery) was recorded in 18 patients, including 5 and 13 patients with and without PTT ablation, respectively. Nine patients (2 women and 7 men; median age 63 (41; 69) years) of 18 received repeat treatment. All 9 patients did not receive PTT thalamotomy after specific targeting the VIM nucleus. During re-treatment, 5, 3, and 1 patient received PTT ablation, repeat VIM ablation, and PTT + VIM ablation, respectively. As a result, all patients achieved a satisfactory result without return of tremor throughout the entire follow-up period. In other 9 patients with tremor return, the symptoms were not significant enough to be an indication for re-treatment, and they remained being followed up.

We evaluated long-term treatment results after MRgFUS in men and women; no significant gender differences were found (p = 0.64; Kaplan–Meier method). However, when long-term treatment results were compared between single-target and dual-target treatment, long-term results were statistically significantly better in patients who received PTT + VIM (p = 0.039, Fig. 4).

 

Fig. 4. Kaplan–Meier curve for symptom return depending on PTT targeting.

 

Discussion

Treatment of TDPD patients is still a major challenge [1–3, 35]. The efficacy of conventional treatment with various groups of medications decreases over time, which is complicated by the development of persistent adverse effects [2, 8]. To date, DBS has been the best treatment option providing a significant reduction in tremor and other PD symptoms [10, 16–18]. However, DBS limitations include its invasive nature, complexity, implantation of the device into the body, insufficient availability, and the need for constant follow-up in large specialized medical centers in order to monitor the parameters of the generator.

In recent years, MRgFUS has been widely used to treat tre- mor-dominant Parkinson disease [12]. We reported our positive experience with MRgFUS in the treatment of 82 TDPD patients with a mean follow-up duration of 1 year or more, an improvement of MDS-UPDRS-III score of 40.1%, and no serious early or long-term complications. Here, we present a unique experience of dual-target MRgFUS in PTT and VIM. In 18 patients, tremor returned (all cases after VIM nucleus ablation); 9 of them successfully underwent re-treatment 6–9 months after the first procedure.

A thorough analysis of cases when tremor returned after MRgFUS and an assessment of treatment results in other centers allowed us to introduce MRgFUS РТТ ablation (after its approval in 2021) in this category of patients in our clinical practice. According to our data, PTT ultrasound ablation in TDPD patients resulted in a greater improvement in early and long-term results compared with conventional VIM nucleus ablation, which is consistent to results of other authors [27]. Simultaneous dual-target (i.e. VIM and PTT) MRgFUS, which is reported in our publication, is a global priority since we have not found any previous studies on this topic, except for 3 cases of stepwise treatment [28].

Overall, an analysis of the early and long-term treatment results with MRgFUS showed that our data were comparable with efficacy and safety data in other studies [19–23, 27, 28]. In our opinion, simultaneous unilateral MRgFUS treatment can be considered an effective treatment option for patients with medication-resistant TDPD. To make a final decision on whether to include this method in the list of recommended treatment options for PD, determine precise criteria for patient selection, understand outcome variability, and assess the possibility of conducting bila- teral interventions, multicenter studies in large cohorts of patients are needed.

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About the authors

Rezida M. Galimova

Bashkir State Medical University; Intellectual Neurosurgery Clinic, V.S. Buzaev International Medical Center

Author for correspondence.
Email: rezida@galimova.com
ORCID iD: 0000-0003-2758-0351

Cand. Sci. (Med.), Department of neurosurgery, Bashkir State Medical University; chief, neurosurgeon, Intelligent Neurosurgery Clinic, International Medical Center V.S. Buzaev Memorial

Россия, Ufa; Ufa

Sergey N. Illarioshkin

Research Center of Neurology

Email: annaly-nevrologii@neurology.ru
ORCID iD: 0000-0002-2704-6282

D. Sci. (Med.), Prof., RAS Full Member, Director, Brain Institute, Deputy director, Research Center of Neurology

Россия, Moscow

Gulnara N. Akhmadeeva

Bashkir State Medical University; Intellectual Neurosurgery Clinic, V.S. Buzaev International Medical Center

Email: nevrolog.ufa@gmail.com
ORCID iD: 0000-0001-5516-0587

Cand. Sci. (Med.), Department of neurology, Bashkir State Medical University; neurologist, Intelligent Neurosurgery Clinic, International Medical Center V.S. Buzaev Memorial

Россия, Ufa; Ufa

Dinara I. Nabiullina

Intellectual Neurosurgery Clinic, V.S. Buzaev International Medical Center

Email: Nabiullina.Dinara@yandex.ru
ORCID iD: 0000-0003-2570-3709

neurologist, Intelligent Neurosurgery Clinic, International Medical Center V.S. Buzaev Memorial

Россия, Ufa

Felix F. Kashapov

Intellectual Neurosurgery Clinic, V.S. Buzaev International Medical Center

Email: felix.kashapov@mail.ru
ORCID iD: 0000-0003-3355-4096

neurologist, Intelligent Neurosurgery Clinic, International Medical Center V.S. Buzaev Memorial

Россия, Ufa

Shamil M. Safin

Bashkir State Medical University

Email: safinsh@mail.ru
ORCID iD: 0000-0002-0100-6100

D. Sci. (Med.), Prof., Head, Department of neurosurgery, Bashkir State Medical University

Россия, Ufa

Igor V. Buzaev

Bashkir State Medical University; Intellectual Neurosurgery Clinic, V.S. Buzaev International Medical Center

Email: igor@buzaev.com
ORCID iD: 0000-0003-0511-9345

D. Sci. (Med.), Prof., Surgery department, Bashkir State Medical University; cardiovascular surgeon, Intelligent Neurosurgery Clinic, International Medical Center V.S. Buzaev Memorial

Россия, Ufa; Ufa

Dinara R. Teregulova

Intellectual Neurosurgery Clinic, V.S. Buzaev International Medical Center

Email: dinamail@mail.ru
ORCID iD: 0000-0001-6283-3735

Cand. Sci. (Med.), neurologist, Intelligent Neurosurgery Clinic, International Medical Center V.S. Buzaev Memorial

Россия, Ufa

Yulia A. Sidorova

Intellectual Neurosurgery Clinic, V.S. Buzaev International Medical Center

Email: yuliasi.ufa@gmail.com
ORCID iD: 0000-0002-0992-0239

neurologist, Intelligent Neurosurgery Clinic, International Medical Center V.S. Buzaev Memorial

Россия, Ufa

Olga V. Kachemaeva

Bashkir State Medical University; Intellectual Neurosurgery Clinic, V.S. Buzaev International Medical Center

Email: olga.kachemaeva@gmail.com
ORCID iD: 0000-0001-9949-9582

Cand. Sci. (Med.), Associate Professor, Department of neurology, Bashkir State Medical University; neurologist, Intelligent Neurosurgery Clinic, International Medical Center V.S. Buzaev Memorial

Россия, Ufa; Ufa

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Supplementary files

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2. Fig. 1. MRgFUS treatment response (scores) in TDPD patients.

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3. Fig. 2. Percentage improvement achieved in TDPD patients after MRgFUS (MDS-UPDRS, part III) vs. baseline by different targets.

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4. Fig. 3. Patient’s MRI scan 2 h after simultaneous right-sided PTT + VIM ablation (axial and coronary planes).

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5. Fig. 4. Kaplan–Meier curve for symptom return depending on PTT targeting.

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Copyright (c) 2024 Galimova R.M., Illarioshkin S.N., Akhmadeeva G.N., Nabiullina D.I., Kashapov F.F., Safin S.M., Buzaev I.V., Teregulova D.R., Sidorova Y.A., Kachemaeva O.V.

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