Personalizing Deep Brain Stimulation Using Advanced Imaging Sequences.


Journal

Annals of neurology
ISSN: 1531-8249
Titre abrégé: Ann Neurol
Pays: United States
ID NLM: 7707449

Informations de publication

Date de publication:
05 2022
Historique:
revised: 09 02 2022
received: 28 06 2021
accepted: 11 02 2022
pubmed: 16 2 2022
medline: 20 4 2022
entrez: 15 2 2022
Statut: ppublish

Résumé

With a growing appreciation for interindividual anatomical variability and patient-specific brain connectivity, advanced imaging sequences offer the opportunity to directly visualize anatomical targets for deep brain stimulation (DBS). The lack of quantitative evidence demonstrating their clinical utility, however, has hindered their broad implementation in clinical practice. Using fast gray matter acquisition T1 inversion recovery (FGATIR) sequences, the present study identified a thalamic hypointensity that holds promise as a visual marker in DBS. To validate the clinical utility of the identified hypointensity, we retrospectively analyzed 65 patients (26 female, mean age = 69.1 ± 12.7 years) who underwent DBS in the treatment of essential tremor. We characterized its neuroanatomical substrates and evaluated the hypointensity's ability to predict clinical outcome using stimulation volume modeling and voxelwise mapping. Finally, we determined whether the hypointensity marker could predict symptom improvement on a patient-specific level. Anatomical characterization suggested that the identified hypointensity constituted the terminal part of the dentatorubrothalamic tract. Overlap between DBS stimulation volumes and the hypointensity in standard space significantly correlated with tremor improvement (R Our findings introduce and validate a novel imaging-based marker attainable from FGATIR sequences that has the potential to personalize and inform targeting and programming in DBS for essential tremor. ANN NEUROL 2022;91:613-628.

Identifiants

pubmed: 35165921
doi: 10.1002/ana.26326
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

613-628

Subventions

Organisme : NIMH NIH HHS
ID : R01 MH113929
Pays : United States

Commentaires et corrections

Type : CommentIn
Type : CommentIn

Informations de copyright

© 2022 The Authors. Annals of Neurology published by Wiley Periodicals LLC on behalf of American Neurological Association.

Références

Boutet A, Loh A, Chow CT, et al. A literature review of magnetic resonance imaging sequence advancements in visualizing functional neurosurgery targets. J Neurosurg 2021:1-14. (Online ahead of print). doi: 10.3171/2020.8.JNS201125.
Dembek TA, Petry-Schmelzer JN, Reker P, et al. PSA and VIM DBS efficiency in essential tremor depends on distance to the dentatorubrothalamic tract. Neuroimage Clin 2020;26:102235.
Coenen VA, Sajonz B, Prokop T, et al. The dentato-rubro-thalamic tract as the potential common deep brain stimulation target for tremor of various origin: an observational case series. Acta Neurochir 2020;162:1053-1066.
Blomstedt P, Sandvik U, Tisch S. Deep brain stimulation in the posterior subthalamic area in the treatment of essential tremor. Mov Disord 2010;25:1350-1356.
Nowacki A, Debove I, Rossi F, et al. Targeting the posterior subthalamic area for essential tremor: proposal for MRI-based anatomical landmarks. J Neurosurg 2019;131:820-827.
Nölte IS, Gerigk L, Al-Zghloul M, et al. Visualization of the internal globus pallidus: sequence and orientation for deep brain stimulation using a standard installation protocol at 3.0 tesla. Acta Neurochir 2012;154:481-494.
Zrinzo L, Hariz M, Hyam JA, et al. Letter to the Editor: a paradigm shift toward MRI-guided and MRI-verified DBS surgery. J Neurosurg 2016;124:1135-1138.
Lozano AM, Lipsman N, Bergman H, et al. Deep brain stimulation: current challenges and future directions. Nat Rev Neurol 2019;15:148-160.
Horn A, Fox MD. Opportunities of connectomic neuromodulation. Neuroimage 2020;221:117180.
Li J, Li Y, Gutierrez L, et al. Imaging the centromedian thalamic nucleus using quantitative susceptibility mapping. Front Hum Neurosci 2020;13:447.
Vassal F, Coste J, Derost P, et al. Direct stereotactic targeting of the ventrointermediate nucleus of the thalamus based on anatomic 1.5-T MRI mapping with a white matter attenuated inversion recovery (WAIR) sequence. Brain Stimul 2012;5:625-633.
Lehman VT, Lee KH, Klassen BT, et al. MRI and tractography techniques to localize the ventral intermediate nucleus and dentatorubrothalamic tract for deep brain stimulation and MR-guided focused ultrasound: a narrative review and update. Neurosurg Focus 2020;49:E8.
Al-Fatly B, Ewert S, Kübler D, et al. Connectivity profile of thalamic deep brain stimulation to effectively treat essential tremor. Brain 2019;142:3086-3098.
Horn A, Li N, Dembek TA, et al. Lead-DBS v2: towards a comprehensive pipeline for deep brain stimulation imaging. Neuroimage 2019;184:293-316.
Avants BB, Tustison NJ, Song G, et al. A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage 2011;54:2033-2044.
Vorwerk J, Oostenveld R, Piastra MC, et al. The FieldTrip-SimBio pipeline for EEG forward solutions. Biomed Eng Online 2018;17:37.
Elias GJB, Boutet A, Joel SE, et al. Probabilistic mapping of deep brain stimulation: insights from 15 years of therapy. Ann Neurol 2021;89:426-443.
Su JH, Thomas FT, Kasoff WS, et al. Thalamus Optimized Multi Atlas Segmentation (THOMAS): fast, fully automated segmentation of thalamic nuclei from structural MRI. Neuroimage 2019;194:272-282.
Ewert S, Plettig P, Li N, et al. Toward defining deep brain stimulation targets in MNI space: a subcortical atlas based on multimodal MRI, histology and structural connectivity. Neuroimage 2018;170:271-282.
Ilinsky I, Horn A, Paul-Gilloteaux P, et al. Human motor thalamus reconstructed in 3D from continuous sagittal sections with identified subcortical afferent territories. eNeuro 2018;5:ENEURO.0060-18.2018.
Akram H, Dayal V, Mahlknecht P, et al. Connectivity derived thalamic segmentation in deep brain stimulation for tremor. Neuroimage Clin 2018;18:130-142.
He X, Chaitanya G, Asma B, et al. Disrupted basal ganglia-thalamocortical loops in focal to bilateral tonic-clonic seizures. Brain 2020;143:175-190.
Lau JC, Xiao Y, Haast RAM, et al. Direct visualization and characterization of the human zona incerta and surrounding structures. Hum Brain Mapp 2020;41:4500-4517.
Petersen MV, Mlakar J, Haber SN, et al. Holographic reconstruction of axonal pathways in the human brain. Neuron 2019;104:1056-1064.
Middlebrooks EH, Domingo RA, Vivas-Buitrago T, et al. Neuroimaging advances in deep brain stimulation: review of indications, anatomy, and brain connectomics. Am J Neuroradiol 2020;41:1558-1568.
Horn A, Kühn AA, Merkl A, et al. Probabilistic conversion of neurosurgical DBS electrode coordinates into MNI space. Neuroimage 2017;150:395-404.
Schaltenbrand G, Wahren W, Hassler R. Atlas for stereotaxy of the human brain. 2nd ed. New York, NY: Thieme, 1977.
Neudorfer C, Maarouf M. Neuroanatomical background and functional considerations for stereotactic interventions in the H fields of Forel. Brain Struct Funct 2018;223:17-30.
Sandvik U, Koskinen L-O, Lundquist A, Blomstedt P. Thalamic and subthalamic deep brain stimulation for essential tremor: where is the optimal target? Neurosurgery 2012;70:840-845; discussion 845-846.
García-Gomar MG, Soto-Abraham J, Velasco-Campos F, Concha L. Anatomic characterization of prelemniscal radiations by probabilistic tractography: implications in Parkinson's disease. Brain Struct Funct 2017;222:71-81.
Tsuboi T, Wong JK, Eisinger RS, et al. Comparative connectivity correlates of dystonic and essential tremor deep brain stimulation. Brain 2021;144:1774-1786.
Fytagoridis A, Åström M, Samuelsson J, Blomstedt P. Deep brain stimulation of the caudal zona incerta: tremor control in relation to the location of stimulation fields. Stereotact Funct Neurosurg 2016;94:363-370.
Philipson J, Blomstedt P, Hariz M, Jahanshahi M. Deep brain stimulation in the caudal zona incerta in patients with essential tremor: effects on cognition 1 year after surgery. J Neurosurg 2021;134:208-215.
Marsden JF, Ashby P, Limousin-Dowsey P, et al. Coherence between cerebellar thalamus, cortex and muscle in man: cerebellar thalamus interactions. Brain 2000;123:1459-1470.
Barbe MT, Reker P, Hamacher S, et al. DBS of the PSA and the VIM in essential tremor. Neurology 2018;91:e543-e550.
Hamel W, Herzog J, Kopper F, et al. Deep brain stimulation in the subthalamic area is more effective than nucleus ventralis intermedius stimulation for bilateral intention tremor. Acta Neurochir 2007;149:749-758.
Herzog J, Hamel W, Wenzelburger R, et al. Kinematic analysis of thalamic versus subthalamic neurostimulation in postural and intention tremor. Brain 2007;130:1608-1625.
Petry-Schmelzer JN, Dembek TA, Steffen JK, et al. Selecting the most effective DBS contact in essential tremor patients based on individual tractography. Brain Sci 2020;10:1015.
Sammartino F, Krishna V, King NKK, et al. Tractography-based ventral intermediate nucleus targeting: novel methodology and intraoperative validation. Mov Disord 2016;31:1217-1225.
Behrens TEJ, Berg HJ, Jbabdi S, et al. Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage 2007;34:144-155.
Sudhyadhom A, Haq IU, Foote KD, et al. A high resolution and high contrast MRI for differentiation of subcortical structures for DBS targeting: the fast gray matter acquisition T1 inversion recovery (FGATIR). Neuroimage 2009;47:44-52.
Petersen MV, Lund TE, Sunde N, et al. Probabilistic versus deterministic tractography for delineation of the cortico-subthalamic hyperdirect pathway in patients with Parkinson disease selected for deep brain stimulation. J Neurosurg 2017;126:1657-1668.
Petersen KJ, Reid JA, Chakravorti S, et al. Structural and functional connectivity of the nondecussating dentato-rubro-thalamic tract. Neuroimage 2018;176:364-371.
Edlow B, Mareyam A, Horn A, et al. 7 Tesla MRI of the ex vivo human brain at 100 micron resolution. Sci Data 2019;6:244.
Åström M, Diczfalusy E, Martens H, Wårdell K. Relationship between neural activation and electric field distribution during deep brain stimulation. IEEE Trans Biomed Eng 2015;62:664-672.
Duffley G, Anderson DN, Vorwerk J, et al. Evaluation of methodologies for computing the deep brain stimulation volume of tissue activated. J Neural Eng 2019;16:066024.
Papavassiliou E, Rau G, Heath S, et al. Thalamic deep brain stimulation for essential tremor: relation of lead location to outcome. Neurosurgery 2004;54:1120-1129; discussion 1129-1130.
Barbe MT, Liebhart L, Runge M, et al. Deep brain stimulation of the ventral intermediate nucleus in patients with essential tremor: stimulation below intercommissural line is more efficient but equally effective as stimulation above. Exp Neurol 2011;230:131-137.
Cury RG, Fraix V, Castrioto A, et al. Thalamic deep brain stimulation for tremor in Parkinson disease, essential tremor, and dystonia. Neurology 2017;89:1416-1423.
Fiechter M, Nowacki A, Oertel MF, et al. Deep brain stimulation for tremor: is there a common structure? Stereotact Funct Neurosurg 2017;95:243-250.
Nowacki A, Bogdanovic M, Sarangmat N, et al. Revisiting the rules for anatomical targeting of ventralis intermediate nucleus. J Clin Neurosci 2019;68:97-100.
Tsuboi T, Jabarkheel Z, Zeilman PR, et al. Longitudinal follow-up with VIM thalamic deep brain stimulation for dystonic or essential tremor. Neurology 2020;94:e1073-e1084.
Middlebrooks EH, Okromelidze L, Wong JK, et al. Connectivity correlates predicting deep brain stimulation outcome in essential tremor: evidence for a common treatment pathway. Neuroimage Clin 2021;32:102846.

Auteurs

Clemens Neudorfer (C)

Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité-Universitätsmedizin Berlin, corporate member of Free University of Berlin and Humboldt University of Berlin, Berlin, Germany.
MGH Neurosurgery & Center for Neurotechnology and Neurorecovery (CNTR), MGH Neurology Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.
Center for Brain Circuit Therapeutics Department of Neurology Brigham & Women's Hospital, Harvard Medical School, Boston, MA, USA.

Daniel Kroneberg (D)

Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité-Universitätsmedizin Berlin, corporate member of Free University of Berlin and Humboldt University of Berlin, Berlin, Germany.

Bassam Al-Fatly (B)

Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité-Universitätsmedizin Berlin, corporate member of Free University of Berlin and Humboldt University of Berlin, Berlin, Germany.

Lukas Goede (L)

Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité-Universitätsmedizin Berlin, corporate member of Free University of Berlin and Humboldt University of Berlin, Berlin, Germany.

Dorothee Kübler (D)

Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité-Universitätsmedizin Berlin, corporate member of Free University of Berlin and Humboldt University of Berlin, Berlin, Germany.

Katharina Faust (K)

Department of Neurosurgery, Charité-Universitätsmedizin Berlin, corporate member of Free University of Berlin and Humboldt University of Berlin, Berlin, Germany.

Ursula van Rienen (U)

Institute of General Electrical Engineering, University of Rostock, Rostock, Germany.
Department Life, Light, and Matter, University of Rostock, Rostock, Germany.
Department of Ageing of Individuals and Society, University of Rostock, Rostock, Germany.

Anna Tietze (A)

Institute of Neuroradiology, Charité-Universitätsmedizin Berlin, corporate member of Free University of Berlin and Humboldt University of Berlin, Berlin, Germany.

Thomas Picht (T)

Department of Neurosurgery, Charité-Universitätsmedizin Berlin, corporate member of Free University of Berlin and Humboldt University of Berlin, Berlin, Germany.

Todd M Herrington (TM)

Department of Neurology, Massachusetts General Hospital, Boston, MA.
Department of Neurology, Harvard Medical School, Boston, MA.

Erik H Middlebrooks (EH)

Department of Radiology, Mayo Clinic, Jacksonville, FL.
Department of Neurosurgery, Mayo Clinic, Jacksonville, FL.

Andrea Kühn (A)

Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité-Universitätsmedizin Berlin, corporate member of Free University of Berlin and Humboldt University of Berlin, Berlin, Germany.

Gerd-Helge Schneider (GH)

Department of Neurosurgery, Charité-Universitätsmedizin Berlin, corporate member of Free University of Berlin and Humboldt University of Berlin, Berlin, Germany.

Andreas Horn (A)

Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité-Universitätsmedizin Berlin, corporate member of Free University of Berlin and Humboldt University of Berlin, Berlin, Germany.
MGH Neurosurgery & Center for Neurotechnology and Neurorecovery (CNTR), MGH Neurology Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.
Center for Brain Circuit Therapeutics Department of Neurology Brigham & Women's Hospital, Harvard Medical School, Boston, MA, USA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH