Movement disorders following mechanical thrombectomy resulting in ischemic lesions of the basal ganglia: An emerging clinical entity.

acute ischemic stroke basal ganglia mechanical thrombectomy post-stroke movement disorders

Journal

European journal of neurology
ISSN: 1468-1331
Titre abrégé: Eur J Neurol
Pays: England
ID NLM: 9506311

Informations de publication

Date de publication:
01 Feb 2024
Historique:
revised: 20 12 2023
received: 15 11 2023
accepted: 04 01 2024
medline: 1 2 2024
pubmed: 1 2 2024
entrez: 1 2 2024
Statut: aheadofprint

Résumé

Post-stroke movement disorders (PMDs) following ischemic lesions of the basal ganglia (BG) are a known entity, but data regarding their incidence are lacking. Ischemic strokes secondary to proximal middle cerebral artery (MCA) occlusion treated with thrombectomy represent a model of selective damage to the BG. The aim of this study was to assess the prevalence and features of movement disorders after selective BG ischemia in patients with successfully reperfused acute ischemic stroke (AIS). We enrolled 64 consecutive subjects with AIS due to proximal MCA occlusion treated with thrombectomy. Patients were clinically evaluated by a movement disorders specialist for PMDs onset at baseline, and after 6 and 12 months. None of the patients showed an identifiable movement disorder in the subacute phase of the stroke. At 6 and 12 months, respectively, 7/25 (28%) and 7/13 (53.8%) evaluated patients developed PMDs. The clinical spectrum of PMDs encompassed parkinsonism, dystonia and chorea, either isolated or combined. In most patients, symptoms were contralateral to the lesion, although a subset of patients presented with bilateral involvement and prominent axial signs. Post-stroke movement disorders are not uncommon in long-term follow-up of successfully reperfused AIS. Follow-up conducted by a multidisciplinary team is strongly advisable in patients with selective lesions of the BG after AIS, even if asymptomatic at discharge.

Sections du résumé

BACKGROUND AND PURPOSE OBJECTIVE
Post-stroke movement disorders (PMDs) following ischemic lesions of the basal ganglia (BG) are a known entity, but data regarding their incidence are lacking. Ischemic strokes secondary to proximal middle cerebral artery (MCA) occlusion treated with thrombectomy represent a model of selective damage to the BG. The aim of this study was to assess the prevalence and features of movement disorders after selective BG ischemia in patients with successfully reperfused acute ischemic stroke (AIS).
METHODS METHODS
We enrolled 64 consecutive subjects with AIS due to proximal MCA occlusion treated with thrombectomy. Patients were clinically evaluated by a movement disorders specialist for PMDs onset at baseline, and after 6 and 12 months.
RESULTS RESULTS
None of the patients showed an identifiable movement disorder in the subacute phase of the stroke. At 6 and 12 months, respectively, 7/25 (28%) and 7/13 (53.8%) evaluated patients developed PMDs. The clinical spectrum of PMDs encompassed parkinsonism, dystonia and chorea, either isolated or combined. In most patients, symptoms were contralateral to the lesion, although a subset of patients presented with bilateral involvement and prominent axial signs.
CONCLUSION CONCLUSIONS
Post-stroke movement disorders are not uncommon in long-term follow-up of successfully reperfused AIS. Follow-up conducted by a multidisciplinary team is strongly advisable in patients with selective lesions of the BG after AIS, even if asymptomatic at discharge.

Identifiants

pubmed: 38299441
doi: 10.1111/ene.16219
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e16219

Informations de copyright

© 2024 The Authors. European Journal of Neurology published by John Wiley & Sons Ltd on behalf of European Academy of Neurology.

Références

Suri R, Rodriguez-Porcel F, Donohue K, et al. Post-stroke movement disorders: the clinical, neuroanatomic, and demographic portrait of 284 published cases. J Stroke Cerebrovasc Dis. 2018;27:2388-2397.
Bhatia KP, Marsden CD. The behavioural and motor consequences of focal lesions of the basal ganglia in man. Brain. 1994;117:859-876.
Mehanna R, Jankovic J. Movement disorders in cerebrovascular disease. Lancet Neurol. 2013;12:597-608.
Tater P, Pandey S. Post-stroke movement disorders: clinical spectrum, pathogenesis, and management. Neurol India. 2021;69(2):272-283. doi:10.4103/0028-3886.314574
Pandey S, Joutsa J, Mehanna R, Shukla AW, Rodriguez-Porcel F, Espay AJ. Gaps, controversies, and proposed roadmap for research in poststroke movement disorders. Mov Disord. 2022;37:1996-2007. doi:10.1002/mds.29218
Handley A, Medcalf P, Hellier K, Dutta D. Movement disorders after stroke. Age Ageing. 2009;38:260-266.
Alarcón F, Zijlmans JC, Dueñas G, Cevallos N. Post-stroke movement disorders: report of 56 patients. J Neurol Neurosurg Psychiatry. 2004;75(11):1568-1574. doi:10.1136/jnnp.2003.011874
D'Olhaberriague L, Arboix A, Martí-Vilalta JL, Moral A, Massons J. Movement disorders in ischemic stroke: clinical study of 22 patients. Eur J Neurol. 1995;2(6):553-557. doi:10.1111/j.1468-1331.1995.tb00173.x
Ghika-Schmid F, Ghika J, Regli F, Bogousslavsky J. Hyperkinetic movement disorders during and after acute stroke: the Lausanne stroke registry. J Neurol Sci. 1997;146:109-116.
Gupta N, Pandey S. Post-thalamic stroke movement disorders: a systematic review. Eur Neurol. 2018;79:303-314.
Park J. Movement disorders following cerebrovascular lesion in the basal ganglia circuit. J Mov Disord. 2016;9:71-79.
Yarbrough CK, Ong CJ, Beyer AB, Lipsey K, Derdeyn CP. Endovascular thrombectomy for anterior circulation stroke: systematic review and meta-analysis. Stroke. 2015;46:3177-3183.
Ghozy S, Kacimi SEO, Azzam AY, et al. Successful mechanical thrombectomy in acute ischemic stroke: revascularization grade and functional independence. J Neurointerv Surg. 2022;14:779-782.
Tambasco N, Romoli M, Calabresi P. Selective basal ganglia vulnerability to energy deprivation: experimental and clinical evidences. Prog Neurobiol. 2018;169:55-75.
Ghika JA, Bogousslavsky J, Regli F. Deep perforators from the carotid system: template of the vascular territories. Arch Neurol. 1990;47:1097-1100.
Kaesmacher J, Huber T, Lehm M, et al. Isolated striatocapsular infarcts after endovascular treatment of acute proximal middle cerebral artery occlusions: prevalence, enabling factors, and clinical outcome. Front Neurol. 2017;8:272. doi:10.3389/fneur.2017.00272
Kleine JF, Beller E, Zimmer C, Kaesmacher J. Lenticulostriate infarctions after successful mechanical thrombectomy in middle cerebral artery occlusion. J Neurointerv Surg. 2017;9:234-239.
Horie N, Morofuji Y, Iki Y, et al. Impact of basal ganglia damage after successful endovascular recanalization for acute ischemic stroke involving lenticulostriate arteries. J Neurosurg. 2020;132:1880-1888.
Kaesmacher J, Kaesmacher M, Berndt M, et al. Early thrombectomy protects the internal capsule in patients with proximal middle cerebral artery occlusion. Stroke. 2021;52:1570-1579. doi:10.1161/STROKEAHA.120.031977
Suh SH, Cloft HJ, Fugate JE, Rabinstein AA, Liebeskind DS, Kallmes DF. Clarifying differences among thrombolysis in cerebral infarction scale variants: is the artery half open or half closed? Stroke. 2013;44:1166-1168.
Von Kummer R, Allen KL, Holle R, et al. Acute stroke: usefulness of early CT findings before thrombolytic therapy. Radiology. 1997;205:327-333.
Pierot L, Jayaraman MV, Szikora I, et al. Standards of practice in acute ischemic stroke intervention: international recommendations. Interv Neuroradiol. 2019;25:31-37.
Powers WJ, Rabinstein AA, Ackerson T, et al. Guidelines for the early management of patients With acute ischemic stroke: 2019 update to the 2018 guidelines for the early management of acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2019;50(12):e344-e418. doi:10.1161/STR.0000000000000211
Berge E, Whiteley W, Audebert H, et al. European stroke organisation (ESO) guidelines on intravenous thrombolysis for acute ischaemic stroke. Eur Stroke J. 2021;6:I-LXII.
Turc G, Bhogal P, Fischer U, et al. European Stroke Organisation (ESO) - European Society for Minimally Invasive Neurological Therapy (ESMINT) Guidelines on Mechanical Thrombectomy in Acute Ischaemic StrokeEndorsed by Stroke Alliance for Europe (SAFE). Eur Stroke J. 2019;4:6-12. doi:10.1177/2396987319832140
Yoo AJ, Simonsen CZ, Prabhakaran S, et al. Refining angiographic biomarkers of revascularization: improving outcome prediction after intra-arterial therapy. Stroke. 2013;44:2509-2512.
Brott T, Adams HP Jr, Olinger CP, et al. Measurements of acute cerebral infarction: a clinical examination scale. Stroke. 1989;20:864-870.
Banks JL, Marotta CA. Outcomes validity and reliability of the modified Rankin scale: implications for stroke clinical trials. Stroke. 2007;38:1091-1096.
Adams HP, Bendixen BH, Kapelle LJ, et al. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of org 10172 in acute stroke treatment. Stroke. 1993;24:35-41.
Movement Disorder Society Task Force on Rating Scales for Parkinson's Disease. The Unified Parkinson's Disease Rating Scale (UPDRS): status and recommendations. Mov Disord. 2003;18(7):738-750. doi:10.1002/mds.10473
Santangelo G, Siciliano M, Pedone R, et al. Normative data for the Montreal cognitive assessment in an Italian population sample. Neurol Sci. 2015;36:585-591.
Fahn S, Tolosa E, Marin C. Clinical rating scale for tremor. Parkinson's Dis Mov Disord. 1988;225-234.
Burke RE, Fahn S, Marsden CD, Bressman SB, Moskowitz C, Friedman J. Validity and reliability of a rating scale for the primary torsion dystonias. Neurology. 1985;35:73-77.
William Guy. 1976. ECDEU assessment manual for psychopharmacology. https://books.google.it/books?hl=it&lr=&id=B4mZEZQRZUEC&oi=fnd&pg=PA6&ots=Kp8ifkAq3G&sig=kTi6GOlQYu_3J1YE6p_2SBkRNRA&redir_esc=y#v=onepage&q=aims&f=false
Postuma RB, Berg D, Stern M, et al. MDS clinical diagnostic criteria for Parkinson's disease. Mov Disord. 2015;30:1591-1601.
Banks JL, Marotta CA. Outcomes validity and reliability of the modified rankin scale: implications for stroke clinical trials: a literature review and synthesis. Stroke. 2007;38(3):1091-1096. doi:10.1161/01.STR.0000258355.23810.c6
Saver JL, Chaisinanunkul N, Campbell BCV, et al. Standardized nomenclature for modified rankin scale global disability outcomes: consensus recommendations from stroke therapy academic industry roundtable XI. Stroke. 2021;52(9):3054-3062. doi:10.1161/STROKEAHA.121.034480
Pandey S, Sarma N, Jain S. Thumb tremor in acute cortical infarct. Mov Disord Clin Pract. 2016;3:515-517.
Pandey S, Sarma N, Jain S. Tongue tremor in acute cortical infarct. Mov Disord Clin Pract. 2016;3:214-215.
Fornito A, Zalesky A, Breakspear M. The connectomics of brain disorders. Nat Rev Neurosci. 2015;16:159-172.
Scott BL, Jankovic J. Delayed-onset progressive movement disorders after static brain lesions. Neurology. 1996;46:68-74.
Lanciego JL, Luquin N, Obeso JA. Functional neuroanatomy of the basal ganglia. Cold Spring Harb Perspect Med. 2012;2(12):a009621. doi:10.1101/cshperspect.a009621
Ottaviani D, Tiple D, Suppa A, et al. Mirror movements in patients with Parkinson's disease. Mov Disord. 2008;23:253-258.
Nürnberger L, Klein C, Baudrexel S, et al. Ultrasound-based motion analysis demonstrates bilateral arm hypokinesia during gait in heterozygous PINK1 mutation carriers. Mov Disord. 2015;30:386-392.
Mirelman A, Bernad-Elazari H, Thaler A, et al. Arm swing as a potential new prodromal marker of Parkinson's disease. Mov Disord. 2016;31:1527-1534.
Joutsa J, Horn A, Hsu J, Fox MD. Localizing parkinsonism based on focal brain lesions. Brain. 2018;141:2445-2456.
Guglielmi V, Quaranta D, Masone Iacobucci G, et al. Basal ganglia ischaemic infarction after thrombectomy: cognitive impairment at acute stage. Eur J Neurol. 2023;30:3772-3779.

Auteurs

Leonardo Rigon (L)

Dipartimento di Neuroscienze, Università Cattolica del Sacro Cuore, Rome, Italy.

Danilo Genovese (D)

Dipartimento di neuroscienze, Organi di Senso e Torace, Fondazione Policlinico Universitario A. Gemelli IRCCS - UOC Neurologia, Rome, Italy.
The Marlene and Paolo Fresco Institute for Parkinson's Disease and Movement Disorders, New York University Langone Health, New York, New York, USA.

Carla Piano (C)

Dipartimento di neuroscienze, Organi di Senso e Torace, Fondazione Policlinico Universitario A. Gemelli IRCCS - UOC Neurologia, Rome, Italy.

Valerio Brunetti (V)

Dipartimento di neuroscienze, Organi di Senso e Torace, Fondazione Policlinico Universitario A. Gemelli IRCCS - UOC Neurologia, Rome, Italy.

Valeria Guglielmi (V)

Dipartimento di neuroscienze, Organi di Senso e Torace, Fondazione Policlinico Universitario A. Gemelli IRCCS - UOC Neurologia, Rome, Italy.

Angelo Tiziano Cimmino (AT)

Dipartimento di Neuroscienze, Università Cattolica del Sacro Cuore, Rome, Italy.

Irene Scala (I)

Dipartimento di Neuroscienze, Università Cattolica del Sacro Cuore, Rome, Italy.

Salvatore Citro (S)

Dipartimento di Neuroscienze, Università Cattolica del Sacro Cuore, Rome, Italy.

Anna Rita Bentivoglio (AR)

Dipartimento di Neuroscienze, Università Cattolica del Sacro Cuore, Rome, Italy.
Dipartimento di neuroscienze, Organi di Senso e Torace, Fondazione Policlinico Universitario A. Gemelli IRCCS - UOC Neurologia, Rome, Italy.

Eleonora Rollo (E)

Dipartimento di Neuroscienze, Università Cattolica del Sacro Cuore, Rome, Italy.

Riccardo Di Iorio (R)

Dipartimento di neuroscienze, Organi di Senso e Torace, Fondazione Policlinico Universitario A. Gemelli IRCCS - UOC Neurologia, Rome, Italy.

Aldobrando Broccolini (A)

Dipartimento di Neuroscienze, Università Cattolica del Sacro Cuore, Rome, Italy.
Dipartimento di neuroscienze, Organi di Senso e Torace, Fondazione Policlinico Universitario A. Gemelli IRCCS - UOC Neurologia, Rome, Italy.

Roberta Morosetti (R)

Dipartimento di neuroscienze, Organi di Senso e Torace, Fondazione Policlinico Universitario A. Gemelli IRCCS - UOC Neurologia, Rome, Italy.

Mauro Monforte (M)

Dipartimento di neuroscienze, Organi di Senso e Torace, Fondazione Policlinico Universitario A. Gemelli IRCCS - UOC Neurologia, Rome, Italy.

Giovanni Frisullo (G)

Dipartimento di neuroscienze, Organi di Senso e Torace, Fondazione Policlinico Universitario A. Gemelli IRCCS - UOC Neurologia, Rome, Italy.

Pietro Caliandro (P)

Dipartimento di neuroscienze, Organi di Senso e Torace, Fondazione Policlinico Universitario A. Gemelli IRCCS - UOC Neurologia, Rome, Italy.

Alessandro Pedicelli (A)

UOC Radiologia e Neuroradiologia, Dipartimento di diagnostica per immagini, radioterapia oncologica ed ematologia, Fondazione Policlinico Universitario A. Gemelli IRCCS, Roma, Italy.

Anselmo Caricato (A)

Neuro Intensive Care Unit, Fondazione Policlinico Universitario Agostino Gemelli IRCCS, Università Cattolica del Sacro Cuore, Rome, Italy.

Giovanna Masone (G)

Dipartimento di neuroscienze, Organi di Senso e Torace, Fondazione Policlinico Universitario A. Gemelli IRCCS - UOC Neurologia, Rome, Italy.

Paolo Calabresi (P)

Dipartimento di Neuroscienze, Università Cattolica del Sacro Cuore, Rome, Italy.
Dipartimento di neuroscienze, Organi di Senso e Torace, Fondazione Policlinico Universitario A. Gemelli IRCCS - UOC Neurologia, Rome, Italy.

Giacomo Della Marca (GD)

Dipartimento di Neuroscienze, Università Cattolica del Sacro Cuore, Rome, Italy.
Dipartimento di neuroscienze, Organi di Senso e Torace, Fondazione Policlinico Universitario A. Gemelli IRCCS - UOC Neurologia, Rome, Italy.

Classifications MeSH