Abstract
The study aimed to evaluate the effects of traditional dysphagia therapy (TDT) and neuromuscular electrical stimulation (NMES) combined with TDT on functionality of oral intake, dysphagia symptom severity, swallowing- and voice-related quality of life, leakage, penetration–aspiration, and residue levels in patients with post-stroke dysphagia (PSD). Thirty-four patients with PSD were included in our prospective, randomized, controlled, and single-blind study. The patients were divided into two groups: (1) TDT only (control group, n = 17) and (2) TDT with NMES (experimental group, n = 17). TDT was applied to both groups for three consecutive weeks, 5 days a week, 45 min a day. Sensory NMES was applied to the experimental group for 45 min per session. Patients were evaluated by the functional oral intake scale (FOIS), the eating assessment tool (EAT-10), the swallowing quality of life questionnaire (SWAL-QOL), and the voice-related quality of life questionnaire (VRQOL) at baseline, immediately post-intervention, and at the 3rd month post-intervention. Fiberoptic endoscopic evaluation of swallowing (FEES) with liquid and semi-solid food was performed pre- and post-intervention. A significant post-intervention improvement was observed on all scales in both groups, and these improvements were maintained 3 months post-intervention. Leakage and penetration–aspiration levels with semi-solid food declined only in the experimental group. In conclusion, TDT is a non-invasive and inexpensive method that leads to improvement in many swallowing-related features in stroke patients; however, NMES as an adjunct therapy is costly but can provide additional benefits for improving features, such as penetration–aspiration and residue levels.
Similar content being viewed by others
References
Ickenstein GW, Stein J, Ambrosi D, Goldstein R, Horn M, Bogdahn U. Predictors of survival after severe dysphagic stroke. J Neurol. 2005;252(12):1510–6. https://doi.org/10.1007/s00415-005-0906-9.
Cohen DL, Roffe C, Beavan J, Blackett B, Fairfield CA, Hamdy S, et al. 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.
Smithard DG. Dysphagia management and stroke units. Curr Phys Med Rehabil Rep. 2016;4(4):287–94. https://doi.org/10.1007/s40141-016-0137-2.
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.
Party ISW. National clinical guideline for stroke. 4th ed. London: Royal College of Physicians; 2012.
Dworzynski K, Ritchie G, Playford ED. Stroke rehabilitation: long-term rehabilitation after stroke. Clin Med. 2015;15(5):461. https://doi.org/10.7861/clinmedicine.15-5-461.
Umay E, Eyigor S, Ertekin C, Unlu Z, Selcuk B, Bahat G, et al. Best practice recommendations for stroke patients with dysphagia: a Delphi-based consensus study of experts in Turkey-Part II: rehabilitation. Dysphagia. 2021;36(5):800–20. https://doi.org/10.1007/s00455-020-10218-8.
Feed ML, Freed L, Chatburc RL, Christian M. Electrical stimulation for swallowing disorders caused by stroke. Respir Care. 2001;46(5):466–74.
Alamer A, Melese H, Nigussie F. Effectiveness of neuromuscular electrical stimulation on post-stroke dysphagia: a systematic review of randomized controlled trials. Clin Interv Aging. 2020;3(15):1521–31. https://doi.org/10.2147/CIA.S262596.
Desimone L, Lovis J, M.C.S.S. Candidates. Critical Review: Is Neuromuscular Electrical Stimulation (NMES) a beneficial supplement to existing dysphagia interventions for post-stroke patients? 2021. https://www.uwo.ca/fhs/lwm/teaching/EBP/2020_21/DesimoneLovis.pdf. Accessed 16 Feb 2022
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.
Poorjavad M, Talebian Moghadam S, Nakhostin Ansari N, Daemi M. Surface electrical stimulation for treating swallowing disorders after stroke: a review of the stimulation intensity levels and the electrode placements. Stroke Res Treat. 2014;2014: 918057. https://doi.org/10.1155/2014/918057.
Speyer R, Sutt A-L, Bergström L, Hamdy S, Heijnen BJ, Remijn L, et al. Neurostimulation in people with oropharyngeal dysphagia: a systematic review and meta-analyses of randomised controlled trials—Part I: pharyngeal and neuromuscular electrical stimulation. J Clin Med. 2022;11(3):776. https://doi.org/10.3390/jcm11030776.
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.
Chen Y-W, Chang K-H, Chen H-C, Liang W-M, Wang Y-H, Lin Y-N. The effects of surface neuromuscular electrical stimulation on post-stroke dysphagia: a systemic review and meta-analysis. Clin Rehabil. 2016;30(1):24–35. https://doi.org/10.1177/0269215515571681.
Huang K-L, Liu T-Y, Huang Y-C, Leong C-P, Lin W-C, Pong Y-P. Functional outcome in acute stroke patients with oropharyngeal dysphagia after swallowing therapy. J Stroke Cerebrovasc Dis. 2014;23(10):2547–53. https://doi.org/10.1016/j.jstrokecerebrovasdis.2014.05.031.
Vasant DH, Michou E, O’Leary N, Vail A, Mistry S, Hamdy S, et al. Pharyngeal electrical stimulation in dysphagia poststroke: a prospective, randomized single-blinded interventional study. Neurorehabil Neural Repair. 2016;30(9):866–75. https://doi.org/10.1177/1545968316639129.
Chiang C-F, Lin M-T, Hsiao M-Y, Yeh Y-C, Liang Y-C, Wang T-G. Comparative efficacy of noninvasive neurostimulation therapies for acute and subacute poststroke dysphagia: a systematic review and network meta-analysis. Arch Phys Med Rehabil. 2019;100(4):739-750.e4. https://doi.org/10.1016/j.apmr.2018.09.117.
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.
Winstein CJ, Stein J, Arena R, Bates B, Cherney LR, Cramer SC, et al. Guidelines for adult stroke rehabilitation and recovery: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2016;47(6):e98–169. https://doi.org/10.1161/STR.0000000000000098.
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.
Park J-W, Kim Y, Oh J-C, Lee H-J. Effortful swallowing training combined with electrical stimulation in post-stroke dysphagia: a randomized controlled study. Dysphagia. 2012;27(4):521–7. https://doi.org/10.1007/s00455-012-9403-3.
Zeng Y, Yip J, Cui H, Guan L, Zhu H, Zhang W, et al. Efficacy of neuromuscular electrical stimulation in improving the negative psychological state in patients with cerebral infarction and dysphagia. Neurol Res. 2018;40(6):473–9. https://doi.org/10.1080/01616412.2018.1451015.
Lee KW, Kim SB, Lee JH, Lee SJ, Park JG, Jang KW. Effects of neuromuscular electrical stimulation for Masseter muscle on oral dysfunction after stroke. Ann Rehabil Med. 2019;43(1):11. https://doi.org/10.5535/arm.2019.43.1.11.
Lee KW, Kim SB, Lee JH, Lee SJ, Ri JW, Park JG. The effect of early neuromuscular electrical stimulation therapy in acute/subacute ischemic stroke patients with dysphagia. Ann Rehabil Med. 2014;38(2):153. https://doi.org/10.5535/arm.2014.38.2.153.
Lim K-B, Lee H-J, Yoo J, Kwon Y-G. Effect of low-frequency rTMS and NMES on subacute unilateral hemispheric stroke with dysphagia. Ann Rehabil Med. 2014;38(5):592. https://doi.org/10.5535/arm.2014.38.5.592.
Park JS, Oh DH, Hwang NK, Lee JH. Effects of neuromuscular electrical stimulation combined with effortful swallowing on post-stroke oropharyngeal dysphagia: a randomised controlled trial. J Oral Rehabil. 2016;43(6):426–34. https://doi.org/10.1111/joor.12390.
Xia W, Zheng C, Lei Q, Tang Z, Hua Q, Zhang Y, et al. Treatment of post-stroke dysphagia by VitalStim therapy coupled with conventional swallowing training. J Huazhong Univ Sci Technol (Med Sci). 2011;31(1):73–6. https://doi.org/10.1007/s11596-011-0153-5.
Zhao J-W, Wang Z-Y, Cao W-Z, Zhang Y-W, Song S-C, Kang W-G, et al. Therapeutic efficacy of swallowing neuromuscular electrical stimulation combined with acupuncture for post-stroke dysphagia. World J Acupunct Moxibustion. 2015;25(1):19–23. https://doi.org/10.1016/S1003-5257(15)30004-0.
Guillén-Solà A, Messagi Sartor M, Bofill Soler N, Duarte E, Barrera MC, Marco E. Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial. Clin Rehabil. 2017;31(6):761–71. https://doi.org/10.1177/0269215516652446.
Bülow M, Speyer R, Baijens L, Woisard V, Ekberg O. Neuromuscular electrical stimulation (NMES) in stroke patients with oral and pharyngeal dysfunction. Dysphagia. 2008;23(3):302–9. https://doi.org/10.1007/s00455-007-9145-9.
Lim K-B, Lee H-J, Lim S-S, Choi Y-I. Neuromuscular electrical and thermal-tactile stimulation for dysphagia caused by stroke: a randomized controlled trial. J Rehabil Med. 2009;41(3):174–8. https://doi.org/10.2340/16501977-0317.
Permsirivanich W, Tipchatyotin S, Wongchai M, Leelamanit V, Setthawatcharawanich S, Sathirapanya P, et al. Comparing the effects of rehabilitation swallowing therapy vs. neuromuscular electrical stimulation therapy among stroke patients with persistent pharyngeal dysphagia: a randomized controlled study. Med J Med Assoc Thail. 2009;92(2):259.
Rofes L, Arreola V, López I, Martin A, Sebastian M, Ciurana A, et al. Effect of surface sensory and motor electrical stimulation on chronic poststroke oropharyngeal dysfunction. Neurogastroenterol Motil. 2013;25(11):888-e701. https://doi.org/10.1111/nmo.12211.
Park J, Oh D, Chang M, Kim K. Effects of expiratory muscle strength training on oropharyngeal dysphagia in subacute stroke patients: a randomised controlled trial. J Oral Rehabil. 2016;43(5):364–72. https://doi.org/10.1111/joor.12382.
Kushner DS, Peters K, Eroglu ST, Perless-Carroll M, Johnson-Greene D. Neuromuscular electrical stimulation efficacy in acute stroke feeding tube-dependent dysphagia during inpatient rehabilitation. Am J Phys Med Rehabil. 2013;92(6):486–95. https://doi.org/10.1097/PHM.0b013e31828762ec.
Simonelli M, Ruoppolo G, Iosa M, Morone G, Fusco A, Grasso MG, et al. A stimulus for eating. The use of neuromuscular transcutaneous electrical stimulation in patients affected by severe dysphagia after subacute stroke: a pilot randomized controlled trial. NeuroRehabilitation. 2019;44(1):103–10. https://doi.org/10.3233/NRE-182526.
Terré R, Mearin F. A randomized controlled study of neuromuscular electrical stimulation in oropharyngeal dysphagia secondary to acquired brain injury. Eur J Neurol. 2015;22(4):687-e44. https://doi.org/10.1111/ene.12631.
Zhang M, Tao T, Zhang Z-B, Zhu X, Fan W-G, Pu L-J, et al. Effectiveness of neuromuscular electrical stimulation on patients with dysphagia with medullary infarction. Arch Phys Med Rehabil. 2016;97(3):355–62. https://doi.org/10.1016/j.apmr.2015.10.104.
Sun Y, Chen X, Qiao J, Song G, Xu Y, Zhang Y, et al. Effects of transcutaneous neuromuscular electrical stimulation on swallowing disorders: a systematic review and meta-analysis. Am J Phys Med Rehabil. 2020;99(8):701. https://doi.org/10.1097/PHM.0000000000001397.
Crary MA, Mann GDC, 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.
Rofes L, Arreola V, Mukherjee R, Clavé P. Sensitivity and specificity of the Eating Assessment Tool and the Volume-Viscosity Swallow Test for clinical evaluation of oropharyngeal dysphagia. Neurogastroenterol Motil. 2014;26(9):1256–65. https://doi.org/10.1111/nmo.12382.
Belafsky PC, Mouadeb DA, Rees CJ, Pryor JC, Postma GN, Allen J, et al. Validity and reliability of the Eating Assessment Tool (EAT-10). Ann Otol Rhinol Laryngol. 2008;117(12):919–24. https://doi.org/10.1177/000348940811701210.
Cheney DM, Siddiqui MT, Litts JK, Kuhn MA, Belafsky PC. The ability of the 10-item eating assessment tool (EAT-10) to predict aspiration risk in persons with dysphagia. Ann Otol Rhinol Laryngol. 2015;124(5):351–4. https://doi.org/10.1177/0003489414558107.
Demir N, Arslan SS, İnal Ö, Ünlüer NÖ, Karaduman AA. Reliability and validity of the Turkish version of the swallow quality of life questionnaire. Fizyoterapi Rehabil. 2016;27(1):19–24. https://doi.org/10.21653/tfrd.271061.
Leow LP, Huckabee M-L, Anderson T, Beckert L. The impact of dysphagia on quality of life in ageing and Parkinson’s disease as measured by the swallowing quality of life (SWAL-QOL) questionnaire. Dysphagia. 2010;25(3):216–20. https://doi.org/10.1007/s00455-009-9245-9.
McHorney CA, Martin-Harris B, Robbins J, Rosenbek J. Clinical validity of the SWAL-QOL and SWAL-CARE outcome tools with respect to bolus flow measures. Dysphagia. 2006;21(3):141–8. https://doi.org/10.1007/s00455-005-0026-9.
Hogikyan ND, Sethuraman G. Validation of an instrument to measure voice-related quality of life (V-RQOL). J Voice. 1999;13(4):557–69. https://doi.org/10.1016/s0892-1997(99)80010-1.
Demir N, Arslan SS, İnal Ö, Karaduman AA. Reliability and validity of the Turkish eating assessment tool (T-EAT-10). Dysphagia. 2016;31(5):644–9. https://doi.org/10.1007/s00455-016-9723-9.
Tezcaner ZÇ, Aksoy S. Reliability and validity of the Turkish version of the voice-related quality of life measure. J Voice. 2017;31(2):262.e7-262.e11.
Langmore SE, Olney RK, Lomen-Hoerth C, Miller BL. Dysphagia in patients with frontotemporal lobar dementia. Arch Neurol. 2007;64(1):58–62. https://doi.org/10.1001/archneur.64.1.58.
Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration–aspiration scale. Dysphagia. 1996;11(2):93–8. https://doi.org/10.1007/BF00417897.
Neubauer PD, Hersey DP, Leder SB. Pharyngeal residue severity rating scales based on fiberoptic endoscopic evaluation of swallowing: a systematic review. Dysphagia. 2016;31(3):352–9. https://doi.org/10.1007/s00455-015-9682-6.
Frost J, Robinson HF, Hibberd J. A comparison of neuromuscular electrical stimulation and traditional therapy, versus traditional therapy in patients with longstanding dysphagia. Curr Opin Otolaryngol Head Neck Surg. 2018;26(3):167–73. https://doi.org/10.1097/MOO.0000000000000454.
Kushner DS, Johnson-Greene D, Cordero MK, Thomashaw SA, Rodriguez J. Swallowing outcomes and discharge destinations in acute-stroke tube-feeding-dependent dysphagia patients treated with neuromuscular-electrical-stimulation during inpatient rehabilitation. Am J Phys Med Rehabil. 2020;99(6):487–94. https://doi.org/10.1097/PHM.0000000000001353.
Güleç A, Albayrak I, Erdur Ö, Öztürk K, Levendoglu F. Effect of swallowing rehabilitation using traditional therapy, kinesiology taping and neuromuscular electrical stimulation on dysphagia in post-stroke patients: a randomized clinical trial. Clin Neurol Neurosurg. 2021;211: 107020. https://doi.org/10.1016/j.clineuro.2021.107020.
Byeon H. Combined effects of NMES and Mendelsohn maneuver on the swallowing function and swallowing-quality of life of patients with stroke-induced sub-acute swallowing disorders. Biomedicines. 2020;8(1):12. https://doi.org/10.3390/biomedicines8010012.
Ko KR, Park HJ, Hyun JK, Seo I-H, Kim TU. Effect of laryngopharyngeal neuromuscular electrical stimulation on dysphonia accompanied by dysphagia in post-stroke and traumatic brain injury patients: a pilot study. Ann Rehabil Med. 2016;40(4):600. https://doi.org/10.5535/arm.2016.40.4.600.
Altman KW, Schaefer SD, Yu G-P, Hertegard S, Lundy DS, Blumin JH. The voice and laryngeal dysfunction in stroke: a Report from the Neurolaryngology Subcommittee of the American Academy of Otolaryngology-Head and Neck Surgery. Otolaryngol Head Neck Surg. 2007;136(6):873–81. https://doi.org/10.1016/j.otohns.2007.02.032.
Giraldo-Cadavid LF, Leal-Leaño LR, Leon-Basantes GA, Bastidas AR, Garcia R, Ovalle S, et al. Accuracy of endoscopic and videofluoroscopic evaluations of swallowing for oropharyngeal dysphagia. Laryngoscope. 2017;127(9):2002–10. https://doi.org/10.1002/lary.26419.
González-Fernández M, Ottenstein L, Atanelov L, Christian AB. Dysphagia after stroke: an overview. Curr Phys Med Rehabil Rep. 2013;1(3):187–96. https://doi.org/10.1007/s40141-013-0017-y.
Ludlow CL, Humbert I, Saxon K, Poletto C, Sonies B, Crujido L. Effects of surface electrical stimulation both at rest and during swallowing in chronic pharyngeal dysphagia. Dysphagia. 2007;22(1):1–10. https://doi.org/10.1007/s00455-006-9029-4.
Cabib C, Ortega O, Kumru H, Palomeras E, Vilardell N, Alvarez-Berdugo D, et al. Neurorehabilitation strategies for poststroke oropharyngeal dysphagia: from compensation to the recovery of swallowing function. Ann NY Acad Sci. 2016;1380(1):121–38. https://doi.org/10.1111/nyas.13135.
Acknowledgements
The authors would like to thank clinical pharmacist Metin Sinan Elmalioglu for his assistance in editing the English version of this article and Rana Konyalioglu for her contributions in statistical evaluations. The authors are also grateful to Istanbul University Scientific Research Projects Coordination Unit for funding the study (Project Number 37068).
Funding
This study was funded by Istanbul University Scientific Research Projects Coordination Unit (Project Number 37068).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
None of the authors have a conflict of interest to report.
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
Tarihci Cakmak, E., Sen, E.I., Doruk, C. et al. The Effects of Neuromuscular Electrical Stimulation on Swallowing Functions in Post-stroke Dysphagia: A Randomized Controlled Trial. Dysphagia 38, 874–885 (2023). https://doi.org/10.1007/s00455-022-10512-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00455-022-10512-7