Department of Physical Medicine and Rehabilitation, Dong-A University College of Medicine, Busan; Regional Cardiocerebrovascular Center, Dong-A University Hospital, Busan, Korea.
Corresponding author: Jae Won Ri. Department of Physical Medicine and Rehabilitation, Dong-A University Hospital, 26 Daesingongwon-ro, Seo-gu, Busan 602-715, Korea. Tel: +82-51-240-5691, Fax: +82-51-253-8511, jun7432@naver.com
• Received: July 25, 2013 • Accepted: October 9, 2013
This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
To compare the outcome of an early application of neuromuscular electrical stimulation (NMES) combined with traditional dysphagia therapy (TDT) versus traditional dysphagia therapy only in acute/subacute ischemic stroke patients with moderate to severe dysphagia by videofluoroscopic swallowing study (VFSS).
Methods
Fifty-seven dysphagic stroke patients were enrolled in a VFSS within 10 days after stroke onset. Patients were randomly assigned into two treatment groups. Thirty-one patients received NMES combined with TDT (NMES/TDT group) and 26 patients received TDT only (TDT group). Electrical stimulation with a maximal tolerable intensity was applied on both suprahyoid muscles for 30 minutes, 5 days per week during 3 weeks. The swallowing function was evaluated at baseline and 3, 6, and 12 weeks after baseline. Outcomes of the VFSS were assessed using the Functional Oral Intake Scale (FOIS).
Results
The mean ages were 63.5±11.4 years in the NMES/TDT group and 66.7±9.5 years in the TDT group. Both groups showed a significant improvement on the FOIS after treatment. The FOIS score was significantly more improved at 3 and 6 weeks after baseline in the NMES/TDT group than in the TDT group (p<0.05).
Conclusion
An early application of NMES combined with TDT showed a positive effect in acute/subacute ischemic stroke patients with dysphagia. These results indicated that the early application of NMES could be used as a supplementary treatment of TDT to help rehabilitate acute/subacute dysphagic stroke patients by improving their swallowing coordination.
Dysphagia is extremely common following a stroke and affects 45%-65% of patients suffering from acute stroke. Its incidence is related to lesion size and location [1,2]. It is the most significant risk factor for the development of pneumonia and can delay the patient's functional recovery [2,3]. Most dysphagia patients recover within 3 weeks of stroke onset, but a recovery is not guaranteed. It may take a more protracted course and may lead to serious complications, such as pneumonia, malnutrition or even death [4,5,6].
A newer treatment modality, neuromuscular electrical stimulation (NMES), provides electrical stimulation on the skin over the throat area. NMES recruits more motor units than volitional contraction and may produce greater gains in muscle strength than exercise alone [7].
Recent studies reported significantly greater improvement for stroke patients in the NMES group compared with other therapeutic methods [8,9,10]. A previous case control study showed that NMES was a helpful treatment for the feeding of acute/subacute stroke patients with tube dependent dysphagia during inpatient rehabilitation. The previous study enrolled acute hemorrhagic or ischemic stroke patients with brain stem lesion and also severe dysphagic patients who had an initial Functional Oral Intake Scale (FOIS) score of 3 or less [11]. The purpose of this randomized study was to prospectively investigate whether combined NMES and traditional dysphagia therapy (TDT) can improve the swallowing function in acute/subacute supratentorial ischemic stroke patients with moderate to severe dysphagia by VFSS.
MATERIALS AND METHODS
Method
Between March 2011 and June 2012, patients were enrolled in this study with a diagnosis of dysphagia by VFSS within 10 days after stroke.
Inclusion criteria were: 1) age between 18 and 80 years; 2) supratentorial ischemic stroke; 3) primary diagnosis of stroke confirmed by computed tomography or magnetic resonance imaging; 4) FOIS score of 5 or less; 5) Korean Mini-Mental State Examination (K-MMSE) score of 21 or higher; and 6) stable underlying disease process.
Exclusion criteria for the trial were as follows: 1) presence of dysphagia before stroke; 2) previous stroke history; 3) unstable cardiopulmonary status, serious psychological disorder or epilepsy; 4) tumor or radiotherapy of the head and neck region; 5) underwent swallowing therapy before participation in the present study; and 6) unstable medical conditions that may interfere with VFSS.
Ninety-two patients were initially screened; 35 subjects who did not meet the inclusion criteria were excluded as study subjects. Fifty-seven patients met all eligibility criteria. The subjects were randomly assigned into two treatment groups. Thirty-one patients (male 22, female 9) were enrolled from the NMES/TDT group and 26 (male 20, female 6) from the TDT group (Fig. 1). Patients were randomly allocated by a computer generated block randomization sequence into two groups, assigning patients to NMES/TDT group or TDT group with a chance of 50% to be assigned to therapy.
All patients received TDT including thermal-tactile stimulation with any combination of lingual-strengthening exercises, laryngeal adduction-elevation exercises, effortful swallow maneuver, Mendelsohn maneuver, Masako maneuver, and Shaker exercises by one speech therapist every day. Thermal-tactile stimulation is a common method that involves stroking or rubbing the anterior faucial pillars with a cold probe prior to having the patient swallow. Both groups received 60 minutes of TDT within a day for 15 days. And NMES (VitalStim Dual Channel Unit and electrodes; Chattanooga Group, Hixson, TN, USA) therapy was applied simultaneously with TDT during the first 30 minutes in the NMES/TDT group. Two sets of electrodes were placed in the infrahyoid area targeting the sternohyoid muscles. NMES intensity was started at 3 mA and increased gradually by 1 mA. We defined the threshold sensibility when a patient continued to complain about discomfort or pain. Patients measured three times of threshold sensibility and swallowing therapist calculated the mean of the three values. The stimulation intensity was then set at 120% of the mean threshold value. A pulse rate of 80 Hz was used with 700 µs duration. Each NMES session was 30 minutes per day, 5 times a week for a total of 3 weeks.
The results were measured using FOIS (Appendix 1). The FOIS is a 7-point ordinal scale reflecting the dietary intake of patients with dysphagia. It has adequate reliability and validity and has been extensively used in clinical studies of dysphagia to measure the functional oral intake [7,12]. We assessed FOIS by VFSS at baseline, after 3, 6, and 12 weeks to compare the degree of improvement between the two groups. All patients were evaluated for dysphagia through VFSS within 10 days (baseline) after stroke and followed-up at 3, 6, and 12 weeks after baseline.
Statistical analysis
All statistical analyses were performed using the SPSS ver. 18.0K for Windows (SPSS Inc., Chicago, IL, USA). The Friedman test was used to determine changes in patients' swallowing function. The FOIS independent sample t-test validation was used to validate between the two groups. The level of statistical significance was set as p-value less than 0.05. The Bonferroni method was used as a post-hoc test. Each category was paired and a Wilcoxon signed-rank test was performed 6 times; at baseline, 3, 6, and 12 weeks after baseline. The level for statistical significance in the post-hoc test was 0.05/6=0.0083.
RESULTS
The mean ages of patients were 63.4±11.4 years for the NMES/TDT group and 66.7±9.5 years for the TDT group. The period from stroke onset to VFSS was 5.5±2.1 and 6.3±2.1 days. There was no significant difference between both groups. Age, sex distribution, stroke lesion, K-MMSE score, and baseline FOIS were similar in both groups and no significant differences were found (Table 1).
After 15 sessions of NMES with TDT, all patients were continuously applied with TDT. A change in feeding materials of both groups was described in Table 2. Overall, 52 of 57 patients (91.2%) improved enough to no longer require tubal feeding. However, 2 patients of the NMES/TDT group and 3 of the TDT group still required tubal feeding for long-term nutrition. The FOIS of the NMES/TDT group was statistically significant increased in all periods until 12 weeks after treatment (Table 3). The TDT group also improved until 12 weeks, but TDT appeared less effective compared with the NMES/TDT group (Fig. 2). The swallowing function of the NMES/TDT group was significantly improved compared with the TDT group in all periods.
Both groups did not show aspiration pneumonia and NMES groups did not show any adverse effects until 12 weeks after stroke.
DISCUSSION
This study demonstrated that early application of NMES and traditional swallowing rehabilitation showed the potential to improve the FOIS scores and the clinical degree of dysphagia for acute/subacute dysphagic stroke patients. Kushner et al. [11] reported NMES with TDT was a beneficial treatment for acute hemorrhage or ischemic stroke patients with tube dependent severe dysphagia. The measured FOIS score of the supratentorial ischemic stroke patients with moderate to severe dysphagia in our study were differently measured than in the previous study. Additionally, our study was not randomized controlled, but block randomized by a computer generated sequence. NMES is a new treatment for dysphagia, involving the application of electrical current across the skin to excite nerve or muscle tissue during a functional task. NMES can increase the suprahyoid muscle size and improve the range of motion, circulation and muscle endurance by increasing the aerobic capacity of the muscle [13]. Recent studies have reported benefits of NMES in the treatment of dysphagia compared with TDT, but most of the studies start dysphagia therapy after 3 weeks of stroke onset [13,14,15,16,17,18].
Previous investigations have shown that signs of aspiration within the first 3 days of a stroke are associated with a delayed swallowing recovery [19,20,21,22]. Recovery from dysphagia after stroke might follow the reorganization of the unaffected motor cortex, but not all patients can recover from dysphagia [23]. Therefore, Odderson et al. [24] showed that an early application of dysphagia therapy for stroke patients was beneficial and cost effective.
Additionally, early NMES application was shown to have more beneficial effect in a dysphagia patient with stroke compared with traditional therapy. Most of the initial tube feeding patients (89.4%) improved enough to remove the nasogastric tube and maintained their oral feeding with no medical complications thereafter. About 40% of patients could return to a pre-stroke oral feeding pattern 3 months after the stroke. Our results suggest that early NMES for acute/subacute dysphagic stroke patients can contribute to a rapid and significant improvement in selected patients. However, five patients (NMES/TDT 2, TDT 3) still required tubal feeding for nutrition at 3-month follow-up. These patients had severe dysphagia at baseline VFSS and did not change at follow-up VFSS. Shaw et al. [25] showed that NMES therapy can improve mild to moderate dysphagia stroke patients, but the most severe dysphagic stroke patients did not gain independence from tubal feeding. Early NMES application with TDT as soon as possible and feeding control guided by VFSS substantially contributed to the improvement of the swallowing function and prevented medical complications, including aspiration pneumonia.
The action mechanisms of NMES have not been fully elucidated yet. NMES is postulated to improve the hyolaryngeal elevation, restore motor function of weak muscles, combat disuse atrophy, enhance sensory awareness and facilitate the muscle contractions [7].
This study has several limitations. First, the study was conducted with a small number of patients. Second, we only measured the functional improvement for a period of 3 to 12 weeks after the stroke. Third, some of the patients had spontaneous recovery, but couldn't be excluded.
In conclusion, we compared the functional swallowing outcomes in acute/subacute stroke patients with an early application of NMES combined with TDT and with TDT only. And as a result, early NMES applied patients showed a significant improvement in their swallowing function at 3, 6, and 12 weeks after onset of stroke compared with the TDT only group. This result suggests that the start of NMES combined with TDT as soon as possible after stroke is a more beneficial treatment for acute/subacute stroke patients with dysphagia.
CONFLICTS OF INTEREST
No potential conflict of interest relevant to this article was reported.
REFERENCES
1. Daniels SK, Brailey K, Priestly DH, Herrington LR, Weisberg LA, Foundas AL. Aspiration in patients with acute stroke. Arch Phys Med Rehabil 1998;79:14-19.
2. Roth EJ, Lovell L, Harvey RL, Heinemann AW, Semik P, Diaz S. Incidence of and risk factors for medical complications during stroke rehabilitation. Stroke 2001;32:523-529.
5. Dziewas R, Ritter M, Schilling M, Konrad C, Oelenberg S, Nabavi DG, et al. Pneumonia in acute stroke patients fed by nasogastric tube. J Neurol Neurosurg Psychiatry 2004;75:852-856.
7. Sun SF, Hsu CW, Lin HS, Sun HP, Chang PH, Hsieh WL, et al. Combined neuromuscular electrical stimulation (NMES) with fiberoptic endoscopic evaluation of swallowing (FEES) and traditional swallowing rehabilitation in the treatment of stroke-related dysphagia. Dysphagia 2013;28:557-566.
11. 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;92:486-495.
12. 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;86:1516-1520.
14. 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;22:1-10.
15. Kiger M, Brown CS, Watkins L. Dysphagia management: an analysis of patient outcomes using VitalStim therapy compared to traditional swallow therapy. Dysphagia 2006;21:243-253.
17. Blumenfeld L, Hahn Y, Lepage A, Leonard R, Belafsky PC. Transcutaneous electrical stimulation versus traditional dysphagia therapy: a nonconcurrent cohort study. Otolaryngol Head Neck Surg 2006;135:754-757.
18. Verin E, Maltete D, Ouahchi Y, Marie JP, Hannequin D, Massardier EG, et al. Submental sensitive transcutaneous electrical stimulation (SSTES) at home in neurogenic oropharyngeal dysphagia: a pilot study. Ann Phys Rehabil Med 2011;54:366-375.
20. Schroeder MF, Daniels SK, McClain M, Corey DM, Foundas AL. Clinical and cognitive predictors of swallowing recovery in stroke. J Rehabil Res Dev 2006;43:301-310.
21. Kumar S, Langmore S, Goddeau RP Jr, Alhazzani A, Selim M, Caplan LR, et al. Predictors of percutaneous endoscopic gastrostomy tube placement in patients with severe dysphagia from an acute-subacute hemispheric infarction. J Stroke Cerebrovasc Dis 2012;21:114-120.
22. Ickenstein GW, Hohlig C, Prosiegel M, Koch H, Dziewas R, Bodechtel U, et al. Prediction of outcome in neurogenic oropharyngeal dysphagia within 72 hours of acute stroke. J Stroke Cerebrovasc Dis 2012;21:569-576.
24. Odderson IR, Keaton JC, McKenna BS. Swallow management in patients on an acute stroke pathway: quality is cost effective. Arch Phys Med Rehabil 1995;76:1130-1133.
Flow chart of patient group assignment and treatment. NMES, neuromuscular electrical stimulation; TDT, traditional dysphagia therapy.
Fig. 2
The change of FOIS in both groups. FOIS significantly increased in NMES/TDT group compare with TDT group at 3 weeks, 6 weeks, and 12 weeks. FOIS, Functional Oral Intake Scale; NMES/TDT group: patients treated by neuromuscular electrical stimulation combined with traditional dysphagia therapy; TDT group, patients treated by traditional dysphagia therapy only. *p<0.05 (independent sample t-test).
Table 1
General characteristics of patients
Values are presented as mean±standard deviation or number (%).
NMES/TDT group, patients treated by neuromuscular electrical stimulation combined with traditional dysphagia therapy; TDT group, patients treated by traditional dysphagia therapy only; K-MMSE: Korean-Mini Mental State Examination; FOIS, Functional Oral Intake Scale.
Table 2
Comparison of changes in feeding materials after treatment
Values are presented as number (%).
NMES/TDT group, patients treated by neuromuscular electrical stimulation combined with traditional dysphagia therapy; TDT group, patients treated by traditional dysphagia therapy only.
Table 3
Comparison of mean changes in FOIS after treatment
Values are presented as number (%).
In all periods, NMES/TDT group showed significant improvement compared to TDT group. NMES/TDT group showed improvement of FOIS in all periods. TDT group did not show significant improvement of FOIS in period of 6 weeks to 12 weeks later.
FOIS, Functional Oral Intake Scale; NMES/TDT group, patients treated by neuromuscular electrical stimulation combined with traditional dysphagia therapy; TDT group, patients treated by traditional dysphagia therapy only.
p<0.0083 (independent sample t-test) significant difference a)between baseline and 3 weeks later in each group, b)between baseline and 6 weeks later in each group, c)between baseline and 12 weeks later in each group, d)between 3 weeks and 6 weeks after stroke in each group, e)between 3 weeks and 12 weeks after stroke in each group, f)between 6 weeks and 12 weeks after stroke in each group.
Figure & Data
References
Citations
Citations to this article as recorded by
Cortical and peripheral neurostimulation to improve swallowing function, aspiration, and dysphagia severity in dysphagia management: A network meta-analysis of randomized controlled trials Kondwani J. Banda, Hsin Chu, Chien-Mei Sung, Ruey Chen, Pi-Yu Su, Li-Fang Chang, Li-Chung Pien, Chu-Yi Wang, Kuei-Ru Chou Clinical Nutrition.2026; 57: 106567. CrossRef
Association Between the Intensity and Frequency of Swallowing Rehabilitation and Oral Intake at Discharge in Older Patients with Acute Post-stroke Dysphagia Kota Ishizuka, Hayato Yamana, Kojiro Morita, Hiroki Matsui, Hiroyuki Ohbe, Kiyohide Fushimi, Hideo Yasunaga Dysphagia.2025; 40(5): 1132. CrossRef
Effect of Multidirectional Chin Tuck Against Resistance Exercise on Oropharyngeal Muscles and Swallowing Function in Subacute Stroke Patients With Dysphagia: A Randomised Controlled Trial Ji‐Su Park, Young‐Seok Cho, Motoyoshi Morishita, Na‐Mi Han, Tae‐Hyung Yoon Journal of Oral Rehabilitation.2025; 52(7): 1050. CrossRef
Device-based solutions supporting patients with swallowing problems Ayodele Sasegbon, Ivy Cheng, Meng Dai, Wanqi Li, Shaheen Hamdy Expert Review of Medical Devices.2025; 22(7): 699. CrossRef
Dose-Response Meta-Analysis of Neuromuscular Electrical Stimulation for Post-Stroke Dysphagia Jong Mi Park, Seo Yeon Yoon, Sang Chul Lee, Yong Wook Kim Journal of the Korean Dysphagia Society.2025; 15(2): 125. CrossRef
Exploration of treatment methods for patients with post-stroke dysphagia: a network meta-analysis Yueyang Zhuang, Xiaohua Wang, Xinbo Yin, Xiaoling Li, Weilin Liu Biotechnology and Genetic Engineering Reviews.2024; 40(1): 436. CrossRef
Neuromuscular Electrical Stimulation for Post-Stroke Dysphagia Treatment: A Systemic Evaluation and Meta-Analysis of Randomized Controlled Trials Zhenni Wang, Zihao Xiao, Qin Shen, Na Zhao, Weiming Zhang Dysphagia.2024; 39(3): 424. CrossRef
Therapeutic approach to dysphagia in post-COVID patients in a rehabilitation unit: a descriptive longitudinal study Anna GUILLEN-SOLA, Cindry RAMÍREZ, Sonia NIETO, Esther DUARTE, Marta TEJERO, Christian GRILLO, Helena BEL, Roser BOZA European Journal of Physical and Rehabilitation Medicine.2024;[Epub] CrossRef
Dysphagia Rehabilitation in Dysphagic Patients with Acute or Critical Illness: A Systematic Review and Meta-Analysis Akira Kuriyama, Shinichi Watanabe, Yukiko Katayama, Taisuke Yasaka, Akira Ouchi, Yuki Iida, Fumihito Kasai Dysphagia.2024; 39(6): 1171. CrossRef
Efficacy of Neuromuscular Electrical Stimulation in Patients with Dysphagia: A Randomized Controlled Trial Jasmine Rafique Sheikh, Leena Ajay Deshpande The Indian Journal of Occupational Therapy.2024; 56(4): 120. CrossRef
The Effects of Neuromuscular Electrical Stimulation on Swallowing Functions in Post-stroke Dysphagia: A Randomized Controlled Trial Elif Tarihci Cakmak, Ekin Ilke Sen, Can Doruk, Comert Sen, Selim Sezikli, Ayse Yaliman Dysphagia.2023; 38(3): 874. CrossRef
The Effect of Sensory Level Versus Motor Level Electrical Stimulation of Pharyngeal Muscles in Acute Stroke Patients with Dysphagia: A Randomized Trial Melissa M. Howard, Elliott S. Block, Demiana Mishreki, Tom Kim, Emily R. Rosario Dysphagia.2023; 38(3): 943. CrossRef
Effects of transcutaneous neuromuscular electrical stimulation on post-stroke dysphagia: a systematic review and meta-analysis Yuhan Wang, Lu Xu, Linjia Wang, Minjiao Jiang, Ling Zhao Frontiers in Neurology.2023;[Epub] CrossRef
Transcutaneous electrical stimulation for gastrointestinal motility disorders Gengqing Song, Sophie Trujillo, Yuhan Fu, Fahmi Shibi, Jiande Chen, Ronnie Fass Neurogastroenterology & Motility.2023;[Epub] CrossRef
Clinical Practice Guidelines for Oropharyngeal Dysphagia Seoyon Yang, Jin-Woo Park, Kyunghoon Min, Yoon Se Lee, Young-Jin Song, Seong Hee Choi, Doo Young Kim, Seung Hak Lee, Hee Seung Yang, Wonjae Cha, Ji Won Kim, Byung-Mo Oh, Han Gil Seo, Min-Wook Kim, Hee-Soon Woo, Sung-Jong Park, Sungju Jee, Ju Sun Oh, Ki De Annals of Rehabilitation Medicine.2023; 47(Suppl 1): S1. CrossRef
Clinical Practice Guidelines for Oropharyngeal Dysphagia Seoyon Yang, Jin-Woo Park, Kyunghoon Min, Yoon Se Lee, Young-Jin Song, Seong Hee Choi, Doo Young Kim, Seung Hak Lee, Hee Seung Yang, Wonjae Cha, Ji Won Kim, Byung-Mo Oh, Han Gil Seo, Min-Wook Kim, Hee-Soon Woo, Sung-Jong Park, Sungju Jee, Ju Sun Oh, Ki De Journal of the Korean Dysphagia Society.2023; 13(2): 77. CrossRef
Gastrointestinal Dysfunction in Stroke Heather Y.F. Yong, Aravind Ganesh, Carlos Camara-Lemarroy Seminars in Neurology.2023; 43(04): 609. CrossRef
Neurostimulation in People with Oropharyngeal Dysphagia: A Systematic Review and Meta-Analyses of Randomised Controlled Trials—Part I: Pharyngeal and Neuromuscular Electrical Stimulation Renée Speyer, Anna-Liisa Sutt, Liza Bergström, Shaheen Hamdy, Bas Joris Heijnen, Lianne Remijn, Sarah Wilkes-Gillan, Reinie Cordier Journal of Clinical Medicine.2022; 11(3): 776. CrossRef
Post-stroke Dysphagia: Prognosis and Treatment–A Systematic Review of RCT on Interventional Treatments for Dysphagia Following Subacute Stroke Philipp Balcerak, Sydney Corbiere, Richard Zubal, Georg Kägi Frontiers in Neurology.2022;[Epub] CrossRef
Therapeutic Effect and Optimal Electrode Placement of Transcutaneous Neuromuscular Electrical Stimulation in Patients with Post-Stroke Dysphagia: A Systematic Review and Meta-Analysis of Randomized Controlled Trials Thanh-Nhan Doan, Wen-Chao Ho, Liang-Hui Wang, Fei-Chun Chang, Trang Thi Quynh Tran, Li-Wei Chou Life.2022; 12(6): 875. CrossRef
Combined conventional speech therapy and functional electrical stimulation in acute stroke patients with dyphagia: a randomized controlled trial Klayne Cunha Matos, Vanessa Fernandes de Oliveira, Paula Luanna Carvalho de Oliveira, Fabíola Aureliano Carvalho, Maria Renata Matos de Mesquita, Camila Gabriella da Silva Queiroz, Levi Mota Marques, Débora Lilian Nascimento Lima, Fernanda Martins Maia Ca BMC Neurology.2022;[Epub] CrossRef
Advances in the Treatment of Dysphagia in Neurological Disorders: A Review of Current Evidence and Future Considerations Ivy Cheng, Adeel Hamad, Ayodele Sasegbon, Shaheen Hamdy Neuropsychiatric Disease and Treatment.2022; Volume 18: 2251. CrossRef
Cervical Interferential Current Transcutaneous Electrical Sensory Stimulation for Patients with Dysphagia and Dementia in Nursing Homes Yoshiko Hara, Ayako Nakane, Haruka Tohara, Kazumasa Kubota, Kazuharu Nakagawa, Koji Hara, Kohei Yamaguchi, Kanako Yoshimi, Shunsuke Minakuchi Clinical Interventions in Aging.2021; Volume 15: 2431. CrossRef
European Stroke Organisation and European Society for Swallowing Disorders guideline for the diagnosis and treatment of post-stroke dysphagia Rainer Dziewas, Emilia Michou, Michaela Trapl-Grundschober, Avtar Lal, Ethem Murat Arsava, Philip M Bath, Pere Clavé, Jörg Glahn, Shaheen Hamdy, Sue Pownall, Antonio Schindler, Margaret Walshe, Rainer Wirth, David Wright, Eric Verin European Stroke Journal.2021; 6(3): LXXXIX. CrossRef
Transcutaneous Electrical Neuromuscular Stimulation (TENS) Along with Traditional Dysphagia Therapy in Patients with Posterior Stroke: A Case Study Anindita A. Banik, Gayatri A. Hattiangadi Indian Journal of Otolaryngology and Head & Neck Surgery.2020; 72(3): 279. CrossRef
Transcutaneous Electrical Stimulation and Dysphagia Rehabilitation: A Narrative Review Ali Barikroo Rehabilitation Research and Practice.2020; 2020: 1. CrossRef
Effects of Transcutaneous Neuromuscular Electrical Stimulation on Swallowing Disorders Yuanyuan Sun, Xiaoyun Chen, Jianhong Qiao, Guixiang Song, Yuedong Xu, Yan Zhang, Dongmei Xu, Wei Gao, Yunfeng Li, Cuiping Xu American Journal of Physical Medicine & Rehabilitation.2020; 99(8): 701. CrossRef
Effectiveness of Neuromuscular Electrical Stimulation on Post-Stroke Dysphagia: A Systematic Review of Randomized Controlled Trials
Comparative Efficacy of Noninvasive Neurostimulation Therapies for Acute and Subacute Poststroke Dysphagia: A Systematic Review and Network Meta-analysis Ching-Fang Chiang, Meng-Ting Lin, Ming-Yen Hsiao, Yi-Chun Yeh, Yun-Chieh Liang, Tyng-Guey Wang Archives of Physical Medicine and Rehabilitation.2019; 100(4): 739. CrossRef
Effect of electro-acupuncture on regulating the swallowing by activating the interneuron in ventrolateral medulla (VLM) Qiuping Ye, Chunyan Liu, Junheng Shi, Hue You, Jiaying Zhao, Jianhua Liu, Nenggui Xu, Zhenhua Xu Brain Research Bulletin.2019; 144: 132. CrossRef
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 Marilia Simonelli, Giovanni Ruoppolo, Marco Iosa, Giovanni Morone, Augusto Fusco, Maria Grazia Grasso, Andrea Gallo, Stefano Paolucci NeuroRehabilitation.2019; 44(1): 103. CrossRef
Two Cases of Post-Stroke Dysphagia by Korean Medical Treatment with Electroacupuncture Yoon-jung Kim, Yu-ran Je, Koang-lok Kim The Journal of Internal Korean Medicine.2019; 40(2): 236. CrossRef
A Clinical Approach to Neuromuscular Electrical Stimulation for Speech and Swallow in an Acute Rehabilitation Facility Melissa M. Howard, Emily R. Rosario Perspectives of the ASHA Special Interest Groups.2019; 4(5): 1044. CrossRef
Effects of Sensory Neuromuscular Electrical Stimulation on Swallowing in the Elderly Affected by Stroke Cláudia Tiemi Mituuti, Marcela Maria Alves da Silva Arone, Raquel Rodrigues Rosa, Giédre Berretin-Felix Topics in Geriatric Rehabilitation.2018; 34(1): 71. CrossRef
The effect of surface neuromuscular electrical stimulation on patients with post-stroke dysphagia Pingping Meng, Shuchao Zhang, Qiang Wang, Peipei Wang, Chao Han, Jinghui Gao, Shouwei Yue Journal of Back and Musculoskeletal Rehabilitation.2018; 31(2): 363. CrossRef
Efficacy of neuromuscular electrical stimulation in improving the negative psychological state in patients with cerebral infarction and dysphagia Yanfang Zeng, James Yip, Hongli Cui, Longfei Guan, Haomeng Zhu, Weidong Zhang, Huishan Du, Xiaokun Geng Neurological Research.2018; 40(6): 473. CrossRef
Combined electrical stimulation and exercise for swallow rehabilitation post‐stroke: a pilot randomized control trial Lise Sproson, Sue Pownall, Pam Enderby, Jenny Freeman International Journal of Language & Communication Disorders.2018; 53(2): 405. CrossRef
Clinical Effects and Differences in Neural Function Connectivity Revealed by MRI in Subacute Hemispheric and Brainstem Infarction Patients With Dysphagia After Swallowing Therapy Yu-Chi Huang, Tun-Wei Hsu, Chau-Peng Leong, Han-Chin Hsieh, Wei-Che Lin Frontiers in Neuroscience.2018;[Epub] CrossRef
Swallowing therapy for dysphagia in acute and subacute stroke Philip M Bath, Han Sean Lee, Lisa F Everton Cochrane Database of Systematic Reviews.2018;[Epub] CrossRef
Swallowing Function After Continuous Neuromuscular Electrical Stimulation of the Submandibular Region Evaluated by High-Resolution Manometry Michael Jungheim, Christoph Schubert, Simone Miller, Martin Ptok Dysphagia.2017; 32(4): 501. CrossRef
Early Rehabilitation After Stroke: a Narrative Review Elisheva R. Coleman, Rohitha Moudgal, Kathryn Lang, Hyacinth I. Hyacinth, Oluwole O. Awosika, Brett M. Kissela, Wuwei Feng Current Atherosclerosis Reports.2017;[Epub] CrossRef
Effect of head lift exercise on kinematic motion of the hyolaryngeal complex and aspiration in patients with dysphagic stroke J. S. Park, N. K. Hwang, D. H. Oh, M. Y. Chang Journal of Oral Rehabilitation.2017; 44(5): 385. CrossRef
Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial Anna Guillén-Solà, Monique Messagi Sartor, Neus Bofill Soler, Esther Duarte, Mª Camelia Barrera, Ester Marco Clinical Rehabilitation.2017; 31(6): 761. CrossRef
Does the addition of specific acupuncture to standard swallowing training improve outcomes in patients with dysphagia after stroke? a randomized controlled trial Wenguang Xia, Chanjuan Zheng, Suiqiang Zhu, Zhouping Tang Clinical Rehabilitation.2016; 30(3): 237. CrossRef
Effects of Tongue Strength and Accuracy Training on Tongue Strength, Swallowing Function, and Quality of Life in Chronic Stroke Patients with Dysphagia Jong-Hoon Moon, Hee-Jin Kim, Min-Kyu Kang, Young-Sik Won The Journal of the Korea Contents Association.2016; 16(11): 605. CrossRef
The effects of surface neuromuscular electrical stimulation on post-stroke dysphagia: a systemic review and meta-analysis Yi-Wen Chen, Kwang-Hwa Chang, Hung-Chou Chen, Wen-Miin Liang, Ya-Hui Wang, Yen-Nung Lin Clinical Rehabilitation.2016; 30(1): 24. CrossRef
Muscle Strengthening Approaches to Dysphagia Rehabilitation Nicole Rogus-Pulia, Nadine P. Connor Current Physical Medicine and Rehabilitation Reports.2016; 4(4): 277. CrossRef
Effectiveness of Neuromuscular Electrical Stimulation on Patients With Dysphagia With Medullary Infarction Ming Zhang, Tao Tao, Zhao-Bo Zhang, Xiao Zhu, Wen-Guo Fan, Li-Jun Pu, Lei Chu, Shou-Wei Yue Archives of Physical Medicine and Rehabilitation.2016; 97(3): 355. CrossRef
Management of oropharyngeal neurogenic dysphagia in adults Anna Miles, Jacqui E. Allen Current Opinion in Otolaryngology & Head and Neck Surgery.2015; 23(6): 433. CrossRef
Aktivierende Stromimpulse für denervierte Muskeln Daniela Kühn, Simone Miller, Michael Jungheim, Martin Ptok HNO Nachrichten.2015; 45(1): 30. CrossRef
Update on management options for dysphagia after acute stroke Jessica Beavan British Journal of Neuroscience Nursing.2015; 11(Sup2): 10. CrossRef
The Effect of Early Neuromuscular Electrical Stimulation Therapy in Acute/Subacute Ischemic Stroke Patients With Dysphagia
Fig. 1 Flow chart of patient group assignment and treatment. NMES, neuromuscular electrical stimulation; TDT, traditional dysphagia therapy.
Fig. 2 The change of FOIS in both groups. FOIS significantly increased in NMES/TDT group compare with TDT group at 3 weeks, 6 weeks, and 12 weeks. FOIS, Functional Oral Intake Scale; NMES/TDT group: patients treated by neuromuscular electrical stimulation combined with traditional dysphagia therapy; TDT group, patients treated by traditional dysphagia therapy only. *p<0.05 (independent sample t-test).
Fig. 1
Fig. 2
The Effect of Early Neuromuscular Electrical Stimulation Therapy in Acute/Subacute Ischemic Stroke Patients With Dysphagia
General characteristics of patients
Values are presented as mean±standard deviation or number (%).
NMES/TDT group, patients treated by neuromuscular electrical stimulation combined with traditional dysphagia therapy; TDT group, patients treated by traditional dysphagia therapy only; K-MMSE: Korean-Mini Mental State Examination; FOIS, Functional Oral Intake Scale.
Comparison of changes in feeding materials after treatment
Values are presented as number (%).
NMES/TDT group, patients treated by neuromuscular electrical stimulation combined with traditional dysphagia therapy; TDT group, patients treated by traditional dysphagia therapy only.
Comparison of mean changes in FOIS after treatment
Values are presented as number (%).
In all periods, NMES/TDT group showed significant improvement compared to TDT group. NMES/TDT group showed improvement of FOIS in all periods. TDT group did not show significant improvement of FOIS in period of 6 weeks to 12 weeks later.
FOIS, Functional Oral Intake Scale; NMES/TDT group, patients treated by neuromuscular electrical stimulation combined with traditional dysphagia therapy; TDT group, patients treated by traditional dysphagia therapy only.
p<0.0083 (independent sample t-test) significant difference a)between baseline and 3 weeks later in each group, b)between baseline and 6 weeks later in each group, c)between baseline and 12 weeks later in each group, d)between 3 weeks and 6 weeks after stroke in each group, e)between 3 weeks and 12 weeks after stroke in each group, f)between 6 weeks and 12 weeks after stroke in each group.
Table 1 General characteristics of patients
Values are presented as mean±standard deviation or number (%).
NMES/TDT group, patients treated by neuromuscular electrical stimulation combined with traditional dysphagia therapy; TDT group, patients treated by traditional dysphagia therapy only; K-MMSE: Korean-Mini Mental State Examination; FOIS, Functional Oral Intake Scale.
Table 2 Comparison of changes in feeding materials after treatment
Values are presented as number (%).
NMES/TDT group, patients treated by neuromuscular electrical stimulation combined with traditional dysphagia therapy; TDT group, patients treated by traditional dysphagia therapy only.
Table 3 Comparison of mean changes in FOIS after treatment
Values are presented as number (%).
In all periods, NMES/TDT group showed significant improvement compared to TDT group. NMES/TDT group showed improvement of FOIS in all periods. TDT group did not show significant improvement of FOIS in period of 6 weeks to 12 weeks later.
FOIS, Functional Oral Intake Scale; NMES/TDT group, patients treated by neuromuscular electrical stimulation combined with traditional dysphagia therapy; TDT group, patients treated by traditional dysphagia therapy only.
p<0.0083 (independent sample t-test) significant difference a)between baseline and 3 weeks later in each group, b)between baseline and 6 weeks later in each group, c)between baseline and 12 weeks later in each group, d)between 3 weeks and 6 weeks after stroke in each group, e)between 3 weeks and 12 weeks after stroke in each group, f)between 6 weeks and 12 weeks after stroke in each group.
