Cortical somatosensory processing after botulinum toxin therapy in post-stroke spasticity.
Adult
Aged
Botulinum Toxins, Type A
/ administration & dosage
Evoked Potentials, Somatosensory
/ drug effects
Exercise Therapy
/ methods
Female
Follow-Up Studies
Humans
Male
Median Nerve
/ drug effects
Middle Aged
Muscle Spasticity
/ diagnosis
Neuromuscular Agents
/ administration & dosage
Somatosensory Cortex
/ drug effects
Stroke
/ complications
Stroke Rehabilitation
/ methods
Treatment Outcome
Upper Extremity
/ innervation
Young Adult
Journal
Medicine
ISSN: 1536-5964
Titre abrégé: Medicine (Baltimore)
Pays: United States
ID NLM: 2985248R
Informations de publication
Date de publication:
25 Jun 2021
25 Jun 2021
Historique:
received:
02
09
2020
accepted:
01
06
2021
entrez:
23
6
2021
pubmed:
24
6
2021
medline:
1
7
2021
Statut:
ppublish
Résumé
In dystonic and spastic movement disorders, abnormalities of motor control and somatosensory processing as well as cortical modulations associated with clinical improvement after botulinum toxin A (BoNT-A) treatment have been reported, but electrophysiological evidence remains controversial. In the present observational study, we aimed to uncover central correlates of post-stroke spasticity (PSS) and BoNT-A-related changes in the sensorimotor cortex by investigating the cortical components of somatosensory evoked potentials (SEPs). Thirty-one chronic stroke patients with PSS of the upper limb were treated with BoNT-A application into the affected muscles and physiotherapy. Clinical and electrophysiological evaluations were performed just before BoNT-A application (W0), then 4 weeks (W4) and 11 weeks (W11) later. PSS was evaluated with the modified Ashworth scale (MAS). Median nerve SEPs were examined in both upper limbs with subsequent statistical analysis of the peak-to-peak amplitudes of precentral P22/N30 and postcentral N20/P23 components. At baseline (W0), postcentral SEPs were significantly lower over the affected cortex. At follow up, cortical SEPs did not show any significant changes attributable to BoNT-A and/or physiotherapy, despite clear clinical improvement. Our results imply that conventional SEPs are of limited value in evaluating cortical changes after BoNT-A treatment and further studies are needed to elucidate its central actions.
Identifiants
pubmed: 34160405
doi: 10.1097/MD.0000000000026356
pii: 00005792-202106250-00028
pmc: PMC8238289
doi:
Substances chimiques
Neuromuscular Agents
0
Botulinum Toxins, Type A
EC 3.4.24.69
Types de publication
Journal Article
Observational Study
Langues
eng
Sous-ensembles de citation
IM
Pagination
e26356Subventions
Organisme : Ministerstvo zdravotnictví České republiky
ID : NV17-29452A
Informations de copyright
Copyright © 2021 the Author(s). Published by Wolters Kluwer Health, Inc.
Déclaration de conflit d'intérêts
The authors have no conflicts of interest to disclose.
Références
Zorowitz RD, Gillard PJ, Brainin M. Poststroke spasticity: sequelae and burden on stroke survivors and caregivers. Neurology 2013;80:45–52.
Sommerfeld DK, Eek EU-B, Svensson A-K, Holmqvist LW, von Arbin MH. Spasticity after stroke: its occurrence and association with motor impairments and activity limitations. Stroke 2004;35:134–9.
Hesse S, Werner C. Poststroke motor dysfunction and spasticity: novel pharmacological and physical treatment strategies. CNS Drugs 2003;17:1093–107.
Ward AB, Aguilar M, De Beyl Z, et al. Use of botulinum toxin type A in management of adult spasticity—a European consensus statement. J Rehabil Med 2003;35:98–9.
Wissel J, Ward AB, Erztgaard P, et al. European consensus table on the use of botulinum toxin type A in adult spasticity. J Rehabil Med 2009;41:13–25.
Sheean G, Lannin NA, Turner-Stokes L, Rawicki B, Snow BJ. Cerebral Palsy Institute. Botulinum toxin assessment, intervention and after-care for upper limb hypertonicity in adults: international consensus statement. Eur J Neurol 2010;17:74–93.
Sunnerhagen KS, Olver J, Francisco GE. Assessing and treating functional impairment in poststroke spasticity. Neurology 2013;80:35–44.
Simpson LI. The binary toxin produced by Clostridium botulinum enters cells by receptor-mediated endocytosis to exert its pharmacologic effects. J Pharmacol Exp Ther 1989;251:1223–8.
Dressler D, Saberi FA, Barbosa ER. Botulinum toxin: mechanisms of action. Arq Neuropsiquiatr 2005;63:180–5.
Rosales RL, Dressler D. On muscle spindles, dystonia and botulinum toxin. Eur J Neurol 2010;17:71–80.
Giladi N. The mechanism of action of botulinum toxin type A in focal dystonia is most probably through its dual effect on efferent (motor) and afferent pathways at the injected site. J Neurol Sci 1997;152:132–5.
Currà A, Trompetto C, Abbruzzese G, Berardelli A. Central effects of botulinum toxin type A: evidence and supposition. Mov Disord 2004;19:60–4.
Veverka T, Nevrlý M, Otruba P, Hluštík P, Kaňovský P. How much evidence do we have on the central effects of botulinum toxin in spasticity and dystonia? IntechOpen 2016;doi: 10.5772/64763.
doi: 10.5772/64763
Palomar FJ, Mir P. Neurophysiological changes after intramuscular injection of botulinum toxin. Clin Neurophysiol 2012;123:54–60.
Kaňovský P, Streitová H, Dufek J, Znojil V, Daniel P, Rektor I. Change in lateralization of the P22/N30 cortical component of median nerve somatosensory evoked potentials in patients with cervical dystonia after successful treatment with botulinum toxin A. Mov Disord 1998;13:108–17.
Feys H, Van Hees J, Bruyninckx F, Mercelis R, De Weerdt W. Value of somatosensory and motor evoked potentials in predicting arm recovery after a stroke. J Neurol Neurosurg Psychiatry 2000;68:323–31.
Al-Rawi MAW, Hamdan FB, Abdul-Muttalib AK. Somatosensory evoked potentials as a predictor for functional recovery of the upper limb in patients with stroke. J Stroke Cerebrovasc Dis 2009;18:262–8.
Park ES, Park CI, Kim DY, Kim YR. The effect of spasticity on cortical somatosensory-evoked potentials: changes of cortical somatosensory-evoked potentials after botulinum toxin type A injection. Arch Phys Med Rehabil 2002;83:1592–6.
Frascarelli F, Di Rosa G, Bisozzi E, Castelli E, Santilli V. Neurophysiological changes induced by the botulinum toxin type A injection in children with cerebral palsy. Eur J Paediatr Neurol 2011;15:59–64.
Basaran A, Emre U, Karadavut KI, Bulmus N. Somatosensory evoked potentials of hand muscles in stroke and their modification by botulinum toxin: a preliminary study. J Rehabil Med 2012;44:541–6.
Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther 1987;67:206–7.
Paternostro-Sluga T, Grim-Stieger M, Posch M, et al. Reliability and validity of the Medical Research Council (MRC) scale and a modified scale for testing muscle strength in patients with radial palsy. J Rehabil Med 2008;40:665–71.
Mahoney FI, Barthel DW. Functional evaluation: the Barthel index. Md State Med J 1965;14:61–5.
Quinn TJ, Dawson J, Walters MR, Lees KR. Variability in modified ranking scoring across a large cohort of international observers. Stroke 2008;39:2975–9.
Krobot A, Schusterová B, Tomsová J, et al. Specific protocol of physiotherapy in stroke patients. Cesk Slov Neurol N 2008;71:74.
Veverka T, Hluštík P, Hok P, et al. Sensorimotor modulation by botulinum toxin A in post-stroke arm spasticity: passive hand movement. J Neurol Sci 2016;362:14–20.
Simpson DM, Hallett M, Ashman EJ, et al. Practice guideline update summary: botulinum neurotoxin for the treatment of blepharospasm, cervical dystonia, adult spasticity, and headache. Neurology 2016;86:1818–26.
Opavský R, Otruba P, Vysloužil M, et al. Post-stroke upper limb spasticity—modulation with botulinum toxin type a therapy and reflection in somatosensory cortical activation. Ceska a Slovenska Neurologie a Neurochirurgie 2011;74:54–9.
Donchin E, Callaway E, Cooper E, Desmedt R. Publication criteria for studies of evoked potentials (EP) in man. Report of the Methodology Committee. Progress in clinical neurophysiology: Vol 1 Attention, voluntary contraction and event-related cerebral potentials; Basel: Karger. Published online January 1, 1977:1-11.
Baker JA, Pereira G. The efficacy of Botulinum Toxin A for spasticity and pain in adults: a systematic review and meta-analysis using the grades of recommendation, assessment, development and evaluation approach. Clin Rehabil 2013;27:1084–96.
Veverka T, Hok P, Otruba P, et al. Botulinum toxin modulates posterior parietal cortex activation in post-stroke spasticity of the upper limb. Front Neurol 2019;10:495.
Hallett M. Mechanism of action of botulinum neurotoxin: unexpected consequences. Toxicon 2018;147:73–6.
Weise D, Weise CM, Naumann M. Central effects of botulinum neurotoxin evidence from human studies. Toxins 2019;11:21.
Trompetto C, Bove M, Avanzino L, Francavilla G, Berardelli A, Abbruzzese G. Intrafusal effects of botulinum toxin in post-stroke upper limb spasticity. Eur J Neurol 2008;15:367–70.
Gilio F, Currà A, Lorenzano C, Modugno N, Manfredi M, Berardelli A. Effects of botulinum toxin type A on intracortical inhibition in patients with dystonia. Ann Neurol 2000;48:20–6.
Kaňovský P, Bares M, Streitová H, Klajblová H, Daniel P, Rektor I. Abnormalities of cortical excitability and cortical inhibition in cervical dystonia evidence from somatosensory evoked potentials and paired transcranial magnetic stimulation recordings. J Neurol 2003;250:42–50.
Boroojerdi B, Cohen LG, Hallett M. Effects of botulinum toxin on motor system excitability in patients with writer's cramp. Neurology 2003;61:1546–50.
Allam N, Fonte-Boa PM, Tomaz CA, Brasil-Neto JP. Lack of effect of botulinum toxin on cortical excitability in patients with cranial dystonia. Clin Neuropharmacol 2005;28:01–5.
Contarino MF, Kruisdijk JJM, Koster L, et al. Sensory integration in writer's cramp: comparison with controls and evaluation of botulinum toxin effect. Clin Neurophysiol 2007;118:2195–206.
Münte TF, Jöbges EM, Wieringa BM, et al. Human evoked potentials to long duration vibratory stimuli: role of muscle afferents. Neurosci Lett 1996;216:163–6.
Kakigi R, Shibasaki H. Effects of age, gender, and stimulus side on scalp topography of somatosensory evoked potentials following median nerve stimulation. J Clin Neurophysiol 1991;8:320–30.
Jung P, Baumgärtner U, Bauermann T, et al. Asymmetry in the human primary somatosensory cortex and handedness. Neuroimage 2003;19:913–23.
Mas MF, Li S, Francisco GE. Centrally mediated late motor recovery after botulinum toxin injection: case reports and a review of current evidence. J Rehabil Med 2017;49:609–19.
Nevrlý M, Hluštík P, Hok P, Otruba P, Tüdös Z, Ka?ovský P. Changes in sensorimotor network activation after botulinum toxin type A injections in patients with cervical dystonia: a functional MRI study. Exp Brain Res 2018;236:2627–37.
Hämäläinen H, Kekoni J, Sams M, Reinikainen K, Näätänen R. Human somatosensory evoked potentials to mechanical pulses and vibration: contributions of SI and SII somatosensory cortices to P50 and P100 components. Electroencephalogr Clin Neurophysiol 1990;75:13–21.