Effects of Bilateral Repetitive Transcranial Magnetic Stimulation on Post-Stroke Dysphagia

BACKGROUND Optimal protocol of repetitive transcranial magnetic stimulation (rTMS) on post-stroke dysphagia remains uncertain with regard to its clinical efficacy. OBJECTIVE The aim of the present study is to investigate the effects of high-frequency rTMS at the bilateral motor cortices over the cortical representation of the mylohyoid muscles in the patients with post-stroke dysphagia. METHODS This study was a single-blind, randomized controlled study with a blinded observer. Thirty-five stroke patients were randomly divided into three intervention groups: the bilateral stimulation group, the unilateral stimulation group, and the sham stimulation group. For the bilateral stimulation group, 500 pulses of 10 Hz rTMS over the ipsilesional and 500 pulses of 10 Hz rTMS over the contralesional motor cortices over the cortical areas that project to the mylohyoid muscles were administered daily for 2 consecutive weeks. For the unilateral stimulation group, 500 pulses of 10 Hz rTMS over the ipsilesional motor cortex over the cortical representation of the mylohyoid muscle and the same amount of sham rTMS over the contralesional hemisphere were applied. For the sham stimulation group, sham rTMS was applied at the bilateral motor cortices. Clinical swallowing function and videofluoroscopic swallowing studies were assessed before the intervention (T0), immediately after the intervention (T1) and 3 weeks after the intervention (T2) using Clinical Dysphagia Scale (CDS), Dysphagia Outcome and Severity Scale (DOSS), Penetration Aspiration Scale (PAS), and Videofluoroscopic Dysphagia Scale (VDS). RESULTS There were significant time and intervention interaction effects in the CDS, DOSS, PAS, and VDS scores (p < 0.05). In the direct comparison of the changes in the swallowing parameters among the three groups, the change in CDS scores at T1 and T2 showed a significantly higher improvement in the bilateral simulation group than in two other groups (p < 0.05). There was a significantly larger change in the DOSS, PAS, and VDS scores at T1 in the bilateral stimulation group than in two other groups (p < 0.05). CONCLUSIONS The results of the present study provide substantial evidence that 10 Hz rTMS at the bilateral motor cortices over the cortical areas projecting to the mylohyoid muscles is effective as an additional treatment strategy to traditional dysphagia therapies.

[1]  Mark Speechley,et al.  Dysphagia After Stroke: Incidence, Diagnosis, and Pulmonary Complications , 2005, Stroke.

[2]  J. Rothwell,et al.  Treatment of post‐stroke dysphagia with repetitive transcranial magnetic stimulation , 2009, Acta neurologica Scandinavica.

[3]  W. Kakuda,et al.  Bilateral Repetitive Transcranial Magnetic Stimulation Combined with Intensive Swallowing Rehabilitation for Chronic Stroke Dysphagia: A Case Series Study , 2014, Case Reports in Neurology.

[4]  S. Hamdy,et al.  Characterizing the Mechanisms of Central and Peripheral Forms of Neurostimulation in Chronic Dysphagic Stroke Patients , 2014, Brain Stimulation.

[5]  K. Ryu,et al.  The effect of 5Hz high‐frequency rTMS over contralesional pharyngeal motor cortex in post‐stroke oropharyngeal dysphagia: a randomized controlled study , 2013, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[6]  C. Weiller,et al.  Dynamics of language reorganization after stroke. , 2006, Brain : a journal of neurology.

[7]  S. Pyun,et al.  Effectiveness of Non-invasive Brain Stimulation in Dysphagia Subsequent to Stroke: A Systemic Review and Meta-analysis , 2015, Dysphagia.

[8]  Jessica M. Pisegna,et al.  Effects of non-invasive brain stimulation on post-stroke dysphagia: A systematic review and meta-analysis of randomized controlled trials , 2016, Clinical Neurophysiology.

[9]  John C. Rothwell,et al.  The cortical topography of human swallowing musculature in health and disease , 1996, Nature Medicine.

[10]  Karen H. O'Neil,et al.  The Dysphagia Outcome and Severity Scale , 1999, Dysphagia.

[11]  E. Khedr,et al.  Therapeutic role of rTMS on recovery of dysphagia in patients with lateral medullary syndrome and brainstem infarction , 2009, Journal of Neurology, Neurosurgery & Psychiatry.

[12]  T. Han,et al.  Validation of the Videofluoroscopic Dysphagia Scale in Various Etiologies , 2014, Dysphagia.

[13]  Karl J. Friston,et al.  Dynamic Diaschisis: Anatomically Remote and Context-Sensitive Human Brain Lesions , 2001, Journal of Cognitive Neuroscience.

[14]  P. Bath,et al.  Interventions for dysphagia and nutritional support in acute and subacute stroke. , 2012, The Cochrane database of systematic reviews.

[15]  Á. Pascual-Leone,et al.  Technology Insight: noninvasive brain stimulation in neurology—perspectives on the therapeutic potential of rTMS and tDCS , 2007, Nature Clinical Practice Neurology.

[16]  Gottfried Schlaug,et al.  Noninvasive Brain Stimulation May Improve Stroke-Related Dysphagia: A Pilot Study , 2011, Stroke.

[17]  Á. Pascual-Leone,et al.  BDNF Polymorphism and Differential rTMS Effects on Motor Recovery of Stroke Patients , 2014, Brain Stimulation.

[18]  K. Ohno,et al.  Transcranial Direct Current Stimulation Improves Swallowing Function in Stroke Patients , 2013, Neurorehabilitation and neural repair.

[19]  Bonnie Martin-Harris,et al.  Breathing and swallowing dynamics across the adult lifespan. , 2005, Archives of otolaryngology--head & neck surgery.

[20]  J. Rothwell,et al.  Explaining oropharyngeal dysphagia after unilateral hemispheric stroke , 1997, The Lancet.

[21]  A. Leroi,et al.  Poststroke Dysphagia Rehabilitation by Repetitive Transcranial Magnetic Stimulation: A Noncontrolled Pilot Study , 2009, Dysphagia.

[22]  J. Logemann,et al.  Manual for the videofluorographic study of swallowing , 1986 .

[23]  S. Rossi,et al.  Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research , 2009, Clinical Neurophysiology.

[24]  Kyeong-Woo Lee,et al.  Effect of Repetitive Transcranial Magnetic Stimulation According to the Stimulation Site in Stroke Patients With Dysphagia , 2015, Annals of rehabilitation medicine.

[25]  M. Chun,et al.  Annals of Rehabilitation Medicine Effect of Repetitive Transcranial Magnetic Stimulation on Patients with Brain Injury and , 2011 .

[26]  Olaf Steinsträter,et al.  Cortical swallowing processing in early subacute stroke , 2011, BMC neurology.

[27]  T. Han,et al.  Validation of Clinical Dysphagia Scale: Based on Videofluoroscopic Swallowing Study , 2005 .

[28]  Richard D. Jones,et al.  Journal of Neuroscience Methods the Effect of Swallowing Treatments on Corticobulbar Excitability: a Review of Transcranial Magnetic Stimulation Induced Motor Evoked Potentials , 2022 .

[29]  A. Vose,et al.  Dysphagia Management in Acute and Sub-acute Stroke , 2014, Current Physical Medicine and Rehabilitation Reports.

[30]  Tobi Frymark,et al.  Evidence-based systematic review: Oropharyngeal dysphagia behavioral treatments. Part III—Impact of dysphagia treatments on populations with neurological disorders , 2009 .

[31]  M. Escudero,et al.  Prognostic value of motor evoked potential obtained by transcranial magnetic brain stimulation in motor function recovery in patients with acute ischemic stroke. , 1998, Stroke.

[32]  W. Heindel,et al.  The impact of lesion location on dysphagia incidence, pattern and complications in acute stroke. Part 1: dysphagia incidence, severity and aspiration , 2015, European journal of neurology.

[33]  Nam-Jong Paik,et al.  Effects of transcranial direct current stimulation (tDCS) on post-stroke dysphagia. , 2012, Restorative neurology and neuroscience.