Four-tract probabilistic tractography technique for target selection in essential tremor treatment with magnetic resonance-guided focused ultrasound.

Brain Essential tremor Four-tract tractography High-intensity focused ultrasound ablation Magnetic resonance imaging

Journal

European radiology
ISSN: 1432-1084
Titre abrégé: Eur Radiol
Pays: Germany
ID NLM: 9114774

Informations de publication

Date de publication:
11 Nov 2023
Historique:
received: 29 04 2023
accepted: 30 09 2023
revised: 20 09 2023
medline: 11 11 2023
pubmed: 11 11 2023
entrez: 10 11 2023
Statut: aheadofprint

Résumé

Magnetic resonance-guided focused ultrasound (MRgFUS) thalamotomy is a novel, minimally invasive ablative treatment for essential tremor (ET). The use of a four-tract probabilistic tractography technique, targeting the intersection between the dentato-rubro-thalamic tracts (both decussating and non-decussating), while evaluating the corticospinal tract and the medial lemniscus, may obtain immediate clinical results with reduced adverse events. Our aim is to present our experience with the four-tract technique for patients undergoing ET treatment with MRgFUS. Retrospective analysis of a prospective database of consecutive patients undergoing ET treatment in a single center from February 2022 to February 2023. Procedural parameters were collected, and tremor improvement was assessed with the Clinical Rating Scale for Tremor (CRST) at baseline and at 3 and 6 months. Adverse events were also reported. Forty-three patients (median age, 72 years [interquartile range, 66-76]; 22 females) were evaluated. Tremor improved significatively in all CRST subsections at 3 months, including the CRST part A + B treated hand tremor (22 [19-27] vs 4 [2-7], p < 0.001) and CRST part C (16 [13-19] vs 3 [1-4], p < 0.001). Differences persisted significant at 6 months. Adverse events were few (4.1% of paresthesias and 12.5% of objective gait disturbance at follow-up) and recorded as mild. The median number of sonications was 7 [6-8] and mean operative time 68.7 ± 24.2 min. Our data show support for the feasibility and benefits of systematic targeting approach with four-tract probabilistic tractography for treating ET using MRgFUS. An approach with four-tract probabilistic tractography for treating essential tremor (ET) patients with magnetic resonance-guided focused ultrasound decreases interindividual variability with good clinical outcomes, low number of sonications, few adverse effects, and short procedure times. • The optimal target for the treatment of essential tremor with MR-guided focused ultrasound remains unknown. • Four-tract probabilistic tractography is a feasible technique that reduces interindividual variability, with good clinical results, few side effects, and short operative time. • The four-tract tractography approach can be performed using different MRI scanners and post-processing software in comparison with the initial description of the technique.

Identifiants

pubmed: 37950079
doi: 10.1007/s00330-023-10431-7
pii: 10.1007/s00330-023-10431-7
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023. The Author(s), under exclusive licence to European Society of Radiology.

Références

Louis ED, Ferreira JJ (2010) How common is the most common adult movement disorder? Update on the worldwide prevalence of essential tremor. Mov Disord 25(5):534–541. https://doi.org/10.1002/mds.22838
Thanvi B, Lo N, Robinson T (2006) Essential tremor—the most common movement disorder in older people. Age Ageing. https://doi.org/10.1093/ageing/afj072
doi: 10.1093/ageing/afj072 pubmed: 16982664
Louis ED, Rios E, Henchcliffe C (2010) How are we doing with the treatment of essential tremor (ET)? Eur J Neurol. https://doi.org/10.1111/j.1468-1331.2009.02926.x
doi: 10.1111/j.1468-1331.2009.02926.x pubmed: 20561042 pmcid: 2939209
Okun MS, Tagliati M, Pourfar M et al (2005) Management of referred deep brain stimulation failures. Arch Neurol. https://doi.org/10.1001/archneur.62.8.noc40425
doi: 10.1001/archneur.62.8.noc40425 pubmed: 15956104
Elias WJ, Lipsman N, Ondo WG et al (2016) A randomized trial of focused ultrasound thalamotomy for essential tremor. N Engl J Med. https://doi.org/10.1056/NEJMoa1600159
doi: 10.1056/NEJMoa1600159 pubmed: 27959759 pmcid: 5259561
Halpern CH, Santini V, Lipsman N et al (2019) Three-year follow-up of prospective trial of focused ultrasound thalamotomy for essential tremor. Neurology. https://doi.org/10.1212/WNL.0000000000008561
doi: 10.1212/WNL.0000000000008561 pubmed: 31748250
Burchiel KJ (1995) Thalamotomy for movement disorders. Neurosurg Clin N Am. https://doi.org/10.1016/S1042-3680(18)30477-7
doi: 10.1016/S1042-3680(18)30477-7 pubmed: 7696875
Jankovic J, Cardoso F, Grossman RG, Hamilton WJ (1995) Outcome after stereotactic thalamotomy for parkinsonian, essential, and other types of tremor. Neurosurgery. https://doi.org/10.1227/00006123-199510000-00011
doi: 10.1227/00006123-199510000-00011 pubmed: 8559296
Nowinski WL (1998) Anatomical targeting in functional neurosurgery by the simultaneous use of multiple Schaltenbrand-Wahren brain atlas microseries. Stereotact Funct Neurosurg. https://doi.org/10.1159/000029654
doi: 10.1159/000029654 pubmed: 10420144
Yamada K, Akazawa K, Yuen S et al (2010) MR imaging of ventral thalamic nuclei. AJNR Am J Neuroradiol. https://doi.org/10.3174/ajnr.A1870
doi: 10.3174/ajnr.A1870 pubmed: 20966051 pmcid: 7965479
Middlebrooks EH, Okromelidze L, Carter RE et al (2022) Directed stimulation of the dentato-rubro-thalamic tract for deep brain stimulation in essential tremor: a blinded clinical trial. Neuroradiol J. https://doi.org/10.1177/19714009211036689
doi: 10.1177/19714009211036689 pubmed: 36173305
Coenen VA, Sajonz B, Prokop T et al (2020) The dentato-rubro-thalamic tract as the potential common deep brain stimulation target for tremor of various origin: an observational case series. Acta Neurochir (Wien). https://doi.org/10.1007/s00701-020-04248-2
doi: 10.1007/s00701-020-04248-2 pubmed: 32337611
Coenen VA, Varkuti B, Parpaley Y et al (2017) Postoperative neuroimaging analysis of DRT deep brain stimulation revision surgery for complicated essential tremor. Acta Neurochir (Wien). https://doi.org/10.1007/s00701-017-3134-z
doi: 10.1007/s00701-017-3134-z pubmed: 28283867
Coenen VA, Allert N, Paus S et al (2014) Modulation of the cerebello-thalamo-cortical network in thalamic deep brain stimulation for tremor. Neurosurgery. https://doi.org/10.1227/NEU.0000000000000540
doi: 10.1227/NEU.0000000000000540 pubmed: 25161000
Coenen VA, Mädler B, Schiffbauer H et al (2011) Individual fiber anatomy of the subthalamic region revealed with diffusion tensor imaging: a concept to identify the deep brain stimulation target for tremor suppression. Neurosurgery. https://doi.org/10.1227/NEU.0b013e31820a1a20
doi: 10.1227/NEU.0b013e31820a1a20 pubmed: 21242831
Al-Fatly B, Ewert S, Kübler D et al (2019) Connectivity profile of thalamic deep brain stimulation to effectively treat essential tremor. Brain. https://doi.org/10.1093/brain/awz236
doi: 10.1093/brain/awz236 pubmed: 31377766
Akram H, Dayal V, Mahlknecht P et al (2018) Connectivity derived thalamic segmentation in deep brain stimulation for tremor. Neuroimage Clin. https://doi.org/10.1016/j.nicl.2018.01.008
doi: 10.1016/j.nicl.2018.01.008 pubmed: 29387530 pmcid: 5790021
Middlebrooks EH, Holanda VM, Tuna IS et al (2018) A method for pre-operative single-subject thalamic segmentation based on probabilistic tractography for essential tremor deep brain stimulation. Neuroradiology. https://doi.org/10.1007/s00234-017-1972-2
doi: 10.1007/s00234-017-1972-2 pubmed: 29307012
Fenoy AJ, Schiess MC (2017) Deep brain stimulation of the dentato-rubro-thalamic tract: outcomes of direct targeting for tremor. Neuromodulation. https://doi.org/10.1111/ner.12585
doi: 10.1111/ner.12585 pubmed: 28256785
Fenoy AJ, Schiess MC (2018) Comparison of tractography-assisted to atlas-based targeting for deep brain stimulation in essential tremor. Mov Disord. https://doi.org/10.1002/mds.27463
doi: 10.1002/mds.27463 pubmed: 30187527
Anthofer J, Steib K, Lange M et al (2017) Distance between active electrode contacts and dentatorubrothalamic tract in patients with habituation of stimulation effect of deep brain stimulation in essential tremor. J Neurol Surg Part A Cent Eur Neurosurg. https://doi.org/10.1055/s-0036-1597894
doi: 10.1055/s-0036-1597894
Shah BR, Lehman VT, Kaufmann TJ et al (2020) Advanced MRI techniques for transcranial high intensity focused ultrasound targeting. Brain. https://doi.org/10.1093/brain/awaa107
doi: 10.1093/brain/awaa107 pubmed: 32537631 pmcid: 7009471
Coenen VA, Sajonz BE, Reinacher PC et al (2021) A detailed analysis of anatomical plausibility of crossed and uncrossed streamline rendition of the dentato-rubro-thalamic tract (DRT(T)) in a commercial stereotactic planning system. Acta Neurochir (Wien). https://doi.org/10.1007/s00701-021-04890-4
doi: 10.1007/s00701-021-04890-4 pubmed: 34181083
Middlebrooks EH, Domingo RA, Vivas-Buitrago T et al (2020) Neuroimaging advances in deep brain stimulation: review of indications, anatomy, and brain connectomics. AJNR Am J Neuroradiol. https://doi.org/10.3174/ajnr.A6693
doi: 10.3174/ajnr.A6693 pubmed: 32816768 pmcid: 7583111
Feltrin FS, Chopra R, Pouratian N et al (2022) Focused ultrasound using a novel targeting method four-tract tractography for magnetic resonance–guided high-intensity focused ultrasound targeting. Brain Commun. https://doi.org/10.1093/braincomms/fcac273
doi: 10.1093/braincomms/fcac273 pubmed: 36751499 pmcid: 9897190
Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM (2012) FSL. Neuroimage 62(2):782–790. https://doi.org/10.1016/j.neuroimage.2011.09.015
Behrens TEJ, Woolrich MW, Jenkinson M et al (2003) Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med. https://doi.org/10.1002/mrm.10609
doi: 10.1002/mrm.10609 pubmed: 14587019
Behrens TEJ, Berg HJ, Jbabdi S et al (2007) Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage. https://doi.org/10.1016/j.neuroimage.2006.09.018
doi: 10.1016/j.neuroimage.2006.09.018 pubmed: 17543543
Hernández M, Guerrero GD, Cecilia JM et al (2013) Accelerating fibre orientation estimation from diffusion weighted magnetic resonance imaging using GPUs. PLoS One. https://doi.org/10.1371/journal.pone.0061892
doi: 10.1371/journal.pone.0061892 pubmed: 24386247 pmcid: 3875472
Patenaude B, Smith SM, Kennedy D, Jenkinson M (2011) A bayesian model of shape and appearance for subcortical brain segmentation. Neuroimage. https://doi.org/10.1016/j.neuroimage.2011.02.046
doi: 10.1016/j.neuroimage.2011.02.046 pubmed: 21352927
Tournier J-D, Smith R, Raffelt D et al (2019) MRtrix3: a fast, flexible and open software framework for medical image processing and visualisation. Neuroimage. https://doi.org/10.1016/j.neuroimage.2019.116137
doi: 10.1016/j.neuroimage.2019.116137 pubmed: 31843710 pmcid: 6889638
Elias WJ, Huss D, Voss T et al (2013) A pilot study of focused ultrasound thalamotomy for essential tremor. N Engl J Med. https://doi.org/10.1056/NEJMoa1300962
doi: 10.1056/NEJMoa1300962 pubmed: 23944301
Chang JW, Park CK, Lipsman N et al (2018) A prospective trial of magnetic resonance-guided focused ultrasound thalamotomy for essential tremor: results at the 2-year follow-up. Ann Neurol. https://doi.org/10.1002/ana.25126
doi: 10.1002/ana.25126 pubmed: 30255970
Sammartino F, Krishna V, King NKK et al (2016) Tractography-based ventral intermediate nucleus targeting: novel methodology and intraoperative validation. Mov Disord. https://doi.org/10.1002/mds.26633
doi: 10.1002/mds.26633 pubmed: 27214406 pmcid: 5089633
Agrawal M, Garg K, Samala R et al (2021) Outcome and complications of MR guided focused ultrasound for essential tremor: a systematic review and meta-analysis. Front Neurol. https://doi.org/10.3389/fneur.2021.654711
doi: 10.3389/fneur.2021.654711 pubmed: 34220698 pmcid: 8250852
Pineda-Pardo JA, Martínez-Fernández R, Rodríguez-Rojas R et al (2019) Microstructural changes of the dentato-rubro-thalamic tract after transcranial MR guided focused ultrasound ablation of the posteroventral VIM in essential tremor. Hum Brain Mapp. https://doi.org/10.1002/hbm.24569
doi: 10.1002/hbm.24569 pubmed: 30865338 pmcid: 6865586
Buch VP, McShane BJ, Beatson N et al (2020) Focused ultrasound thalamotomy with dentato-rubro-thalamic tractography in patients with spinal cord stimulators and cardiac pacemakers. Stereotact Funct Neurosurg. https://doi.org/10.1159/000507031
doi: 10.1159/000507031 pubmed: 32403106
Schreglmann SR, Bauer R, Hägele-Link S et al (2017) Unilateral cerebellothalamic tract ablation in essential tremor by MRI-guided focused ultrasound. Neurology. https://doi.org/10.1212/WNL.0000000000003795
doi: 10.1212/WNL.0000000000003795 pubmed: 28275083
Boutet A, Ranjan M, Zhong J et al (2018) Focused ultrasound thalamotomy location determines clinical benefits in patients with essential tremor. Brain. https://doi.org/10.1093/brain/awy278
doi: 10.1093/brain/awy278 pubmed: 30452554
Reich MM, Brumberg J, Pozzi NG et al (2016) Progressive gait ataxia following deep brain stimulation for essential tremor: adverse effect or lack of efficacy? Brain. https://doi.org/10.1093/brain/aww223
doi: 10.1093/brain/aww223 pubmed: 27658421
Kapadia AN, Elias GJB, Boutet A et al (2020) Multimodal MRI for MRgFUS in essential tremor: post-treatment radiological markers of clinical outcome. J Neurol Neurosurg Psychiatry. https://doi.org/10.1136/jnnp-2020-322745
doi: 10.1136/jnnp-2020-322745 pubmed: 32651242
Lak AM, Segar DJ, McDannold N, White JP, Cosgrove GR (2022) Magnetic resonance image guided focused ultrasound thalamotomy. A single center experience with 160 procedures. Front Neurol 13:743649. https://doi.org/10.3389/fneur.2022.743649

Auteurs

Carlos Pérez-García (C)

Department of Interventional Neuroradiology, Hospital Clínico Universitario San Carlos, 28040, Madrid, Spain. cperezgarcia.med@gmail.com.

Alfonso López-Frías (A)

Department of Interventional Neuroradiology, Hospital Clínico Universitario San Carlos, 28040, Madrid, Spain.

Juan Arrazola (J)

Department of Radiology, Hospital Clínico Universitario San Carlos, Madrid, Spain.

Lidia Gil (L)

Department of Radiology, Hospital Clínico Universitario San Carlos, Madrid, Spain.

Rocio García-Ramos (R)

Department of Neurology, Hospital Clínico Universitario San Carlos, Madrid, Spain.

Ana Fernández Revuelta (A)

Department of Neurology, Hospital Clínico Universitario San Carlos, Madrid, Spain.

Fernando Alonso-Frech (F)

Department of Neurology, Hospital Clínico Universitario San Carlos, Madrid, Spain.

Eva López Valdés (E)

Department of Neurology, Hospital Clínico Universitario San Carlos, Madrid, Spain.

Albert Trondin (A)

Department of Neurosurgery, Hospital Clínico Universitario San Carlos, Madrid, Spain.

Miguel Yus-Fuertes (M)

Department of Neuroradiology, Hospital Clínico Universitario San Carlos, Madrid, Spain.

Classifications MeSH