Abstract
Repetitive transcranial magnetic stimulation (rTMS) play a important role for rehabilitation in stroke. But therapeutic schedule of rTMS in dysphagia after acute stroke is still controversial. The purpose of this study was to investigate the therapeutic effect of rTMS with different frequencies on dysphagia after acute stroke. From August 2019 to December 2020, 45 patients with post-stroke dysphagia were selected as research subjects, and randomly divided into 3 groups: the high frequency stimulation on bilateral hemisphere group (High group), bilateral high frequency stimulation on the affected hemisphere and low frequency stimulation on the unaffected hemisphere group (High-low group), and sham stimulation group (Sham group). On the basis of routine swallowing training (30 min) for all patients, the high group received 5 Hz rTMS in both hemispheres, the high- low group received 5 Hz rTMS in the unaffected hemisphere, 1 Hz rTMS in the affected hemisphere, and the sham stimulation group received sham stimulation in bilateral hemisphere. All participants were assessed with dysphagia handicap index (DHI), functional oral intake scale (FOIS) and videofluoroscopic swallowing study (VFSS) before the intervention (T1), immediately after intervention (T2) and 1 month after the intervention (T3). Meanwhile, according to the results of VFSS, Rosenbek penetration aspiration scale (PAS), the moving distance of hyoid bone towards the superior side (H), and pharyngeal response time (T) were analyzed and evaluated. After intervention, all three groups showed significant improvement in post-treatment scores from baseline (P = 0.000). The results of DHI, PAS and H showed that the improvement in high group and high-low group was significantly greater than sham group (P = 0.000). The results of FOIS and T showed that the improvement of bilateral high-frequency group was significantly greater than that of high-low group and sham group (P = 0.000), and the difference lasted until 1 month after the end of treatment. Therefore, bilateral pharyngeal cortex high frequency rTMS and affected side high frequency/unaffected side low frequency rTMS can effectively improve swallowing disorder after acute stroke. However, the effect of bilateral high frequency rTMS is significantly higher than high-low in improving oral feeding function and pharyngeal response time.
Similar content being viewed by others
Abbreviations
- rTMS:
-
Repetitive transcranial magnetic stimulation
- DHI:
-
Dysphagia handicap index
- FOIS:
-
Functional oral intake scale
- VFSS:
-
Videofluoroscopic swallowing study
- PAS:
-
Rosenbek penetration aspiration scale
References
Diéguez-Pérez I, Leirós-Rodríguez R. Effectiveness of different application parameters of neuromuscular electrical stimulation for the treatment of dysphagia after a stroke: a systematic review. J Clin Med. 2020;9(8):2618. https://doi.org/10.3390/jcm9082618.
Martino R, Foley N, Bhogal S, Diamant N, Speechley M, Teasell R. Dysphagia after stroke: incidence, diagnosis, and pulmonary complications. Stroke. 2005;36(12):2756–63. https://doi.org/10.1161/01.STR.0000190056.76543.eb.
Cohen DL, Roffe C, Beavan J, Blackett B, Fairfield CA, Hamdy S, Havard D, McFarlane M, McLauglin C, Randall M, Robson K, Scutt P, Smith C, Smithard D, Sprigg N, Warusevitane A, Watkins C, Woodhouse L, Bath PM. Post-stroke dysphagia: a review and design considerations for future trials. Int J Stroke. 2016;11(4):399–411. https://doi.org/10.1177/1747493016639057.
Cabib C, Ortega O, Kumru H, Palomeras E, Vilardell N, Alvarez-Berdugo D, Muriana D, Rofes L, Terré R, Mearin F, Clavé P. Neurorehabilitation strategies for poststroke oropharyngeal dysphagia: from compensation to the recovery of swallowing function. Ann N Y Acad Sci. 2016;1380(1):121–38. https://doi.org/10.1111/nyas.13135.
Takizawa C, Gemmell E, Kenworthy J, Speyer R. A systematic review of the prevalence of oropharyngeal dysphagia in stroke, Parkinson’s disease, Alzheimer’s disease, head injury, and pneumonia. Dysphagia. 2016;31(3):434–41. https://doi.org/10.1007/s00455-016-9695-9.
Terré R. Disfagia orofaríngea en el ictus: aspectos diagnósticos y terapéuticos [oropharyngeal dysphagia in stroke: diagnostic and therapeutic aspects]. Rev Neurol. 2020;70(12):444–52. https://doi.org/10.33588/rn.7012.2019447 (Spanish).
Wang Z, Song WQ, Wang L. Application of noninvasive brain stimulation for post-stroke dysphagia rehabilitation. Kaohsiung J Med Sci. 2017;33(2):55–61. https://doi.org/10.1016/j.kjms.2016.11.007.
Simons JA. Swallowing dysfunctions in Parkinson’s disease. Int Rev Neurobiol. 2017;134:1207–38. https://doi.org/10.1016/bs.irn.2017.05.026.
Fisicaro F, Lanza G, Grasso AA, Pennisi G, Bella R, Paulus W, Pennisi M. Repetitive transcranial magnetic stimulation in stroke rehabilitation: review of the current evidence and pitfalls. Ther Adv Neurol Disord. 2019;12:1756286419878317. https://doi.org/10.1177/1756286419878317.
Wang Q, Zhang D, Zhao YY, Hai H, Ma YW. Effects of high-frequency repetitive transcranial magnetic stimulation over the contralesional motor cortex on motor recovery in severe hemiplegic stroke: a randomized clinical trial. Brain Stimul. 2020;13(4):979–86. https://doi.org/10.1016/j.brs.2020.03.020.
Bonin Pinto C, Morales-Quezada L, de Toledo Piza PV, Zeng D, Saleh Vélez FG, Ferreira IS, Lucena PH, Duarte D, Lopes F, El-Hagrassy MM, Rizzo LV, Camargo EC, Lin DJ, Mazwi N, Wang QM, Black-Schaffer R, Fregni F. Combining fluoxetine and rTMS in poststroke motor recovery: a placebo-controlled double-blind randomized phase 2 clinical trial. Neurorehabil Neural Repair. 2019;33(8):643–55. https://doi.org/10.1177/1545968319860483.
Wang RY, Tseng HY, Liao KK, Wang CJ, Lai KL, Yang YR. rTMS combined with task-oriented training to improve symmetry of interhemispheric corticomotor excitability and gait performance after stroke: a randomized trial. Neurorehabil Neural Repair. 2012;26(3):222–30. https://doi.org/10.1177/1545968311423265.
Du J, Yang F, Liu L, Hu J, Cai B, Liu W, Xu G, Liu X. Repetitive transcranial magnetic stimulation for rehabilitation of poststroke dysphagia: a randomized, double-blind clinical trial. Clin Neurophysiol. 2016;127(3):1907–13. https://doi.org/10.1016/j.clinph.2015.11.045.
Cramer SC, Nelles G, Benson RR, Kaplan JD, Parker RA, Kwong KK, Kennedy DN, Finklestein SP, Rosen BR. A functional MRI study of subjects recovered from hemiparetic stroke. Stroke. 1997;28(12):2518–27. https://doi.org/10.1161/01.str.28.12.2518.
Bertolucci F, Chisari C, Fregni F. The potential dual role of transcallosal inhibition in post-stroke motor recovery. Restor Neurol Neurosci. 2018;36(1):83–97. https://doi.org/10.3233/RNN-170778.
Park E, Kim MS, Chang WH, Oh SM, Kim YK, Lee A, Kim YH. Effects of bilateral repetitive transcranial magnetic stimulation on post-stroke dysphagia. Brain Stimul. 2017;10(1):75–82. https://doi.org/10.1016/j.brs.2016.08.005.
Di Pino G, Pellegrino G, Assenza G, Capone F, Ferreri F, Formica D, Ranieri F, Tombini M, Ziemann U, Rothwell JC, Di Lazzaro V. Modulation of brain plasticity in stroke: a novel model for neurorehabilitation. Nat Rev Neurol. 2014;10(10):597–608. https://doi.org/10.1038/nrneurol.2014.162.
Cheng IKY, Chan KMK, Wong CS, Li LSW, Chiu KMY, Cheung RTF, Yiu EML. Neuronavigated high-frequency repetitive transcranial magnetic stimulation for chronic post-stroke dysphagia: a randomized controlled study. J Rehabil Med. 2017;49(6):475–81. https://doi.org/10.2340/16501977-2235.
Noh JS, Lim JH, Choi TW, Jang SG, Pyun SB. Effects and safety of combined rTMS and action observation for recovery of function in the upper extremities in stroke patients: a randomized controlled trial. Restor Neurol Neurosci. 2019;37(3):219–30. https://doi.org/10.3233/RNN-180883.
Bath PM, Lee HS, Everton LF. Swallowing therapy for dysphagia in acute and subacute stroke. Cochrane Database Syst Rev. 2018;10(10):CD000323. https://doi.org/10.1002/14651858.CD000323.pub3.
Lefaucheur JP, Aleman A, Baeken C, Benninger DH, Brunelin J, Di Lazzaro V, Filipović SR, Grefkes C, Hasan A, Hummel FC, Jääskeläinen SK, Langguth B, Leocani L, Londero A, Nardone R, Nguyen JP, Nyffeler T, Oliveira-Maia AJ, Oliviero A, Padberg F, Palm U, Paulus W, Poulet E, Quartarone A, Rachid F, Rektorová I, Rossi S, Sahlsten H, Schecklmann M, Szekely D, Ziemann U. Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS): an update (2014–2018). Clin Neurophysiol. 2020;131(2):474–528. https://doi.org/10.1016/j.clinph.2019.11.002 (Erratum in: Clin Neurophysiol. 2020;131(5):1168–1169).
Khedr EM, Mohamed KO, Soliman RK, Hassan AMM, Rothwell JC. The effect of high-frequency repetitive transcranial magnetic stimulation on advancing Parkinson’s disease with dysphagia: double blind randomized clinical trial. Neurorehabil Neural Repair. 2019;33(6):442–52. https://doi.org/10.1177/1545968319847968.
Silbergleit AK, Schultz L, Jacobson BH, Beardsley T, Johnson AF. The dysphagia handicap index: development and validation. Dysphagia. 2012;27(1):46–52. https://doi.org/10.1007/s00455-011-9336-2.
Crary MA, Mann GD, Groher ME. Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients. Arch Phys Med Rehabil. 2005;86(8):1516–20. https://doi.org/10.1016/j.apmr.2004.11.049.
Alves TC, Cola PC, Jorge AG, Gatto AR, Da Silva RG. Relationship between pharyngeal response time and lateralized brain lesion in stroke. Top Stroke Rehabil. 2019;26(6):435–9. https://doi.org/10.1080/10749357.2019.1623519.
Martin-Harris B, Brodsky MB, Michel Y, Ford CL, Walters B, Heffner J. Breathing and swallowing dynamics across the adult lifespan. Arch Otolaryngol Head Neck Surg. 2005;131(9):762–70. https://doi.org/10.1001/archotol.131.9.762.
Momosaki R, Abo M, Kakuda W. Bilateral repetitive transcranial magnetic stimulation combined with intensive swallowing rehabilitation for chronic stroke dysphagia: a case series study. Case Rep Neurol. 2014;6(1):60–7. https://doi.org/10.1159/000360936.
Tarameshlu M, Ansari NN, Ghelichi L, Jalaei S. The effect of repetitive transcranial magnetic stimulation combined with traditional dysphagia therapy on poststroke dysphagia: a pilot double-blinded randomized-controlled trial. Int J Rehabil Res. 2019;42(2):133–8. https://doi.org/10.1097/MRR.0000000000000336.
Gao J, Zhang HJ. Effects of chin tuck against resistance exercise versus Shaker exercise on dysphagia and psychological state after cerebral infarction. Eur J Phys Rehabil Med. 2017;53(3):426–32. https://doi.org/10.23736/S1973-9087.16.04346-X.
Waddington H. Psychological and communication issues in feeding post-stroke patients with dysphagia. Nurs Times. 2009;105(32–33):25–6.
Sproson L, Pownall S, Enderby P, Freeman J. Combined electrical stimulation and exercise for swallow rehabilitation post-stroke: a pilot randomized control trial. Int J Lang Commun Disord. 2018;53(2):405–17. https://doi.org/10.1111/1460-6984.12359.
Park JS, An DH, Oh DH, Chang MY. Effect of chin tuck against resistance exercise on patients with dysphagia following stroke: a randomized pilot study. NeuroRehabilitation. 2018;42(2):191–7. https://doi.org/10.3233/NRE-172250.
Konecny P, Elfmark M. Electrical stimulation of hyoid muscles in post-stroke dysphagia. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2018;162(1):40–2. https://doi.org/10.5507/bp.2017.043.
McCullough GH, Wertz RT, Rosenbek JC, Mills RH, Webb WG, Ross KB. Inter- and intrajudge reliability for videofluoroscopic swallowing evaluation measures. Dysphagia. 2001;16(2):110–8. https://doi.org/10.1007/PL00021291.
Cook IJ, Dodds WJ, Dantas RO, Kern MK, Massey BT, Shaker R, Hogan WJ. Timing of videofluoroscopic, manometric events, and bolus transit during the oral and pharyngeal phases of swallowing. Dysphagia. 1989;4(1):8–15. https://doi.org/10.1007/BF02407397.
Jefferson S, Mistry S, Michou E, Singh S, Rothwell JC, Hamdy S. Reversal of a virtual lesion in human pharyngeal motor cortex by high frequency contralesional brain stimulation. Gastroenterology. 2009;137(3):841–9. https://doi.org/10.1053/j.gastro.2009.04.056 (849.e1).
Hamdy S, Aziz Q, Rothwell JC, Power M, Singh KD, Nicholson DA, Tallis RC, Thompson DG. Recovery of swallowing after dysphagic stroke relates to functional reorganization in the intact motor cortex. Gastroenterology. 1998;115(5):1104–12. https://doi.org/10.1016/s0016-5085(98)70081-2.
Park JW, Oh JC, Lee JW, Yeo JS, Ryu KH. The effect of 5Hz high-frequency rTMS over contralesional pharyngeal motor cortex in post-stroke oropharyngeal dysphagia: a randomized controlled study. Neurogastroenterol Motil. 2013;25(4):324-e250. https://doi.org/10.1111/nmo.12063.
Yang SN, Pyun SB, Kim HJ, Ahn HS, Rhyu BJ. Effectiveness of non-invasive brain stimulation in dysphagia subsequent to stroke: a systemic review and meta-analysis. Dysphagia. 2015;30(4):383–91. https://doi.org/10.1007/s00455-015-9619-0.
Cheng I, Sasegbon A, Hamdy S. Effects of neurostimulation on poststroke dysphagia: a synthesis of current evidence from randomized controlled trials. Neuromodulation. 2021;24(8):1388–401. https://doi.org/10.1111/ner.13327.
Speyer R, Sutt AL, Bergström L, Hamdy S, Pommée T, Balaguer M, Kaale A, Cordier R. Neurostimulation in people with oropharyngeal dysphagia: a systematic review and meta-analysis of randomised controlled trials-part II: brain neurostimulation. J Clin Med. 2022;11(4):993. https://doi.org/10.3390/jcm11040993.
Funding
The experiment was funded by Chongqing medical scientific research project (Joint project of Chongqing Health Commission and Science and Technology Bureau) (No. 2019MSXM017), General project of Chongqing Natural Science Foundation (Chongqing Science and Technology Bureau) (cstc2021jcyj-msxmX0232).
Author information
Authors and Affiliations
Contributions
LN conceived of the study, and participated in its design and manuscript preparation. FZ and XC participated in manuscript preparation and dysphagia therapy. JC and JL participated in data collection and statistical analysis. CL and LT participated in swallowing function assessments. YW participated in rTMS treatment. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing Interests
The authors declare that they have no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zou, F., Chen, X., Niu, L. et al. Effect of Repetitive Transcranial Magnetic Stimulation on Post-stroke Dysphagia in Acute Stage. Dysphagia 38, 1117–1127 (2023). https://doi.org/10.1007/s00455-022-10533-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00455-022-10533-2