Effectiveness of Neuromuscular Electrical Stimulation on Post-Stroke Dysphagia: A Systematic Review of Randomized Controlled Trials

Figures & data

Figure 1 Preferred reporting items for systematic reviews and meta-analyses (PRISMA) diagram.

Table 1 Summary of Included Randomized Controlled Trials

Authors (Year)	Participants Characteristics	Interventions	Outcome Measures	Results/Conclusions
Park et al (2016)^Citation30	Total of 50 participants: EG = 25 and CG = 25 Mean age (years): EG = 54 (11.9), CG = 55.8 (12.2) Time since onset (weeks): EG = 35.4 (5.6), CG = 36 (6)	EG = received NMES for 30 min per session, 5 times per week, for 6 weeks. CG = placebo/shame therapy for 30 min per session, 5 sessions per week, for 6 weeks.	VDS PAS VFSS	The experimental group revealed a significant increase in anterior and superior hyoid bone movement and the pharyngeal phase of the swallowing function.
Zeng et al (2018)^Citation31	Total of 112 participants: EG (n = 59); CG (n = 53) Mean age (years): EG = 67.9 (12.3); CG = 66.1 (13.0) Time since onset (days): not stated	EG = received conventional drug therapy, swallowing training and NMES performed once daily over a 20-minute period in intervals of three seconds for 12 days followed by a two-day break and then another 12-day course of treatment. CG = conventional drug therapy and swallowing training	Kubota water-drinking test	The rate of improvement in swallowing function was 88.1% in the treatment group while 69.8% in the control group. Patients with stroke and dysphagia could be minimized by neuromuscular electrical stimulation in conjunction with conventional therapy.
Li et al (2018)^Citation32	Total of 135 participants: EG1; (n = 45), and EG2 (n = 45), CG (n = 45) Mean age (years); EG1 = 65.8 (13.2), EG2 = 66.7 (14.6); CG = 66.1 (13) Duration (days): EG1 = 9.3 (3.9), EG2 = 8.4 (3.2); CG = 8.8 (3.7)	EG1 = received NMES for 1hr 5 times per week for 4 weeks duration. EG2 = received NMES plus TDT for 1 hour at a frequency of 5 per week for 4 week duration. CG = received TDT included basic training and direct food intake training for 1 hour at a frequency of 5 per week for 4 week duration.	SSA VFSS VAS	There were significant differences in SSA and VFSS scores in each group after the treatment (P<0.001). After 4-week treatment, SSA value, oral transit time, and pharyngeal transit time were significantly improved in the NMES and the traditional swallowing therapy group than in the other 2 groups (P< 0.001). NMES coupled with traditional swallowing therapy may be beneficial for post-stroke dysphagia.
Zhao et al (2015)^Citation33	120 total participants: EG = 62 CG = 58 Mean age (years): EG = 63.2 (9.7) CG = 60.2 (9.0) Duration (hours); EG = 15.7 (6.2) CG = 16.0 (5.9)	EG = received NMES combined with acupuncture for 30 minutes each time twice a day. CG = given normal acupuncture	Kubota water-swallow test	NMES combined with acupuncture for dysphagia after stroke shows better therapeutic effect than the ordinary acupuncture.
Lim et al (2014)^Citation34	47 total participants: EG1 = 18, EG2 = 14, CG = 15 Mean age (years): EG1 = 66.3 (15.4), EG2 = 59.8 (11.8), CG = 62.5 (8.2) Duration (days) EG1 = 37.3 (16.1), EG2 = 3 0.3 (14.8), CG = 34.4 (10.1)	EG1 = received NMES, to the anterior neck for 30 minutes per session (5 days per week for 2 weeks). EG2 = received rTMS at100% resting motor threshold with 1 Hz frequency for 20 minutes per session (5 days per week for 2 weeks). Both EG groups were given conventional dysphagia therapy for 4 weeks. CG = received CDT four 4 weeks	FDS PTT PAS ASHA NOMS	Mean changes in FDS and PAS for liquid during first 2 weeks in the rTMS and NMES groups were significantly higher than those in the CDT group, but no significant differences were found between the rTMS and NMES group. No significant difference in mean changes of FDS and PAS for semi-solid, PTT, and ASHA NOMS was observed among 3 groups
Huang et al(2014)^Citation35	29 participants; CG = 11 EG1 = 8, and combined EG2 = 10 Median age (years): CG = 67, EG1 = 64.5, EG2 = 68.9	EG1 = received electrical stimulation 60 minutes per session for 3 times per week. EG-2 = received both TS and NMES for 3 times per week (60 minutes per session), and 10 sessions. CG received therapies included oral exercise, chin tuck, head tilt, and head rotation, faucial thermal–tactile stimulation and supraglottic swallowing, effortful swallowing and Mendelsohn maneuver.	FOIS PAS FDS	TS therapy and combined therapy both had significant swallowing improvement after therapy, with FOIS and PAS. Among groups they found significant improvements in patients eating cookies and thick liquid after combined NMES/TS therapy (P < 0.05) with VFS.
Vasant et al(2016)^Citation36	Total of 36 patients: EG = 18; CG = 18 Median age (years): EG=71 (56,79); CG = 71 (61, 78) Median Time post stroke (days): EG = 16 (9, 23) CG = 11 (7, 17)	EG = received 3 sessions of PES/NMES plus CDT for 10 minutes on 3 consecutive days. CG=received sham stimulation plus CDT (standard swallowing treatments) for the same period.	DSR PAS	Effects of EG versus sham for secondary outcomes: PAS ≥3 at 2 weeks, OR (95% CI) = 0.6 (0.2, 1.4); times to hospital discharge, 39 days versus 52 days, HR (95% CI) = 1.2 (0.5, 2.5); NGT removal 8 versus 14 days, HR (95% CI) = 2 (0.5, 7.9); and DSR <4 at 3 months, OR (95% CI) = 0.9 (0.1, 7). Although the direction of observed differences were consistent with PES accelerating swallowing recovery over the first 2 weeks post intervention, suboptimal recruitment prevents definitive conclusions.
Lee et al (2014)^Citation37	57 total participants: EG = 31, CG = 26 Mean age (years): EG = 63.4 (11.4), CG = 66.7 (9.5) duration since onset (Days) EG = 5.5 (2.1) CG = 6.3 (2.1)	EG = received NMES combined with TDT for 30 minutes5 days per week for 3 weeks. CG = received TDT (thermal-tactile stimulation with any combination of lingual-strengthening exercises, laryngeal adduction-elevation exercises, effortful swallow maneuver, Mendelsohn and Masako maneuver) for 60 minutes every day for 15 days.	FOIS	NMES group showed improvement of FOIS in all periods than the TDT group.
Lee et al (2019)^Citation38	Total 40 participants EG = 20, CG = 20 Mean age (years): EG = 66.2 (15.6), CG = 64.6 (12.8) Duration (days): EG = 16.3 (10.2), CG = 16.3 (10.2)	EG = received NMES plus CDT on masseter muscle and suprahyoid muscle simultaneously for 30 minutes each time, 2 times per day for a total of 20 sessions over 2 weeks. CG = received NMES plus CDT only on suprahyoid muscle for 30 minutes each time, 2 times per day for a total of 20 sessions over 2 weeks.	VFSS PAS FDS	After 2 weeks of NMES, both groups showed improvement in scores of total FDS and pharyngeal phase FDS. Additionally, the study group showed improvement in oral phase FDS.
Sola et al (2017)^Citation39	Total of 50 participants: EG1 = 21, EG2 = 20;CG = 21, Mean age (years): EG1 = 67.9 (10.6), EG2 = 70.3 (8.4) CG = 68.9 (7.0) Duration (days) = EG1 = 10.8 (8.7); EG2 =1 1.0 (5.5); CG = 9.3 (5.1),	EG1 = received SST +IEMT group’s muscle training consisted of 5 sets/10 repetitions, twice-daily, 5 days/week for 3 weeks duration. EG2 = received SST+ sham IEMT+ NMES; NMES consisted of 40-minute sessions, 5 days/week, at 80Hz for 3 weeks. CG = received sham IEMT required no effort 5 sets/10 repetitions, twice-daily, 5 days/week for 3 weeks duration.	PAS Maximal inspiratory and expiratory pressures	Combining IEMT to SST was effective, improved respiratory muscle strength. Both IEMT and NMES were associated with improvement in pharyngeal swallowing security signs at the end of the intervention, but the effect did not persist at 3-month follow-up and no differences in respiratory complications were detected between treatment groups and controls.
Konecny et al (2018)^Citation40	A total 108 post-stroke patients: EG = 54; CG = 54 Mean age (years): EG = 70 (7.3); CG = 69 (8.2) Time since onset (days): not stated	EG = received NMES of the suprahyoid muscles with a frequency of 60 Hz for 20 min a day, five days a week. CG = received standard OFR without ES	VFSS OTT PTT	The difference in duration of OTT after the therapy between the EG and CG was statistically significant (P=0.01). The difference in the duration of the PTT after the therapy between the EG and CG was also statistically significant (P = 0.01). The result is improved swallowing.

Abbreviations: EG, experimental group; CG, control group; TDT, traditional dysphagia therapy; CDT, conventional dysphagia treatment; rTMS, repetitive transcranial magnetic stimulation; FDS, functional dysphagia scale; PTT, pharyngeal transit time; PAS, penetration-aspiration scale; ASHA NOMS, American Speech Language Hearing Association National Outcomes Measurement System; OFR, swallowing scale; orofacial rehabilitation; IEMT, inspiratory/expiratory muscle training; NMES, neuromuscular electrical stimulation; SST, standard swallow therapy; VFSS, video fluoroscopic swallowing studies; VDS, videofluoroscopy dysphagia scale; VAS, visual analogue scale; SSA, Standardized Swallowing Assessment; DSR, Dysphagia Severity Rating Scale.

Table 2 Methodological Quality of Included Studies

PEDro Items	Parak et al, 2016^Citation30	Zeng et al, 2018^Citation31	Li et al 2018^Citation32	Zhao et al, 2015^Citation33	Lim et al, 2014^Citation34	Huang et al, 2014^Citation35	Vasant et al, 2016^Citation36	Lee et al, 2014^Citation37	Lee et al, 2019^Citation3,Citation8	Solà et al, 2017^Citation39	Konecny, 2018^Citation40
Eligibility	Yes	Yes	Yes	No	No	Yes	Yes	No	Yes	Yes	Yes
Random allocation	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes
Concealed allocation	Yes	No	Yes	No	No	Yes	No	Yes	No	Yes	No
Baseline comparability	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes
Blind participants	No	No	No	No	No	No	Yes	No	No	No	No
Blind therapists	No	No	No	No	No	No	No	No	No	Yes	No
Adequate follow-up	No	No	Yes	Yes	No	No	Yes	Yes	Yes	Yes	Yes
Blind assessor	No	No	Yes	No	Yes	No	Yes	No	No	Yes	No
Intention to treat analysis	Yes	Yes	Yes	No	Yes	No	No	No	Yes	Yes	Yes
Between group comparison	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes
Point estimate and variability	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes
Total score	6	5	8	5	6	5	7	6	6	9	6
GRADE Approach	Moderate	Moderate	High	Moderate	Moderate	Moderate	High	Moderate	Moderate	High	Moderate

Park JS, Oh D-H, Hwang N-K, et al. Effects of neuromuscular electrical stimulation combined with effortful swallowing on post‐stroke oropharyngeal dysphagia: a randomised controlled trial. J Oral Rehabil. 2016;43(6):426–434. doi:10.1111/joor.1239026969528

 PubMed Web of Science ®Google Scholar

Zeng Y, Yip J, Cui H, 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):473–479. doi:10.1080/01616412.2018.145101529726748

 PubMed Web of Science ®Google Scholar

Li L, Li Y, Wu X, et al. The value of adding transcutaneous neuromuscular electrical stimulation (VitalStim) to traditional therapy for poststroke dysphagia: a randomized controlled trial. Top Geriatr Rehabil. 2018;34(3):200–206. doi:10.1097/TGR.0000000000000195

 Web of Science ®Google Scholar

Zhao J-W, Wang Z-Y, Cao W-Z, 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. doi:10.1016/S1003-5257(15)30004-0

 Google Scholar

Lim K-B, Lee H-J, Yoo J, et al. Effect of low-frequency rTMS and NMES on subacute unilateral hemispheric stroke with dysphagia. Ann Rehabil Med. 2014;38(5):592. doi:10.5535/arm.2014.38.5.59225379488

 PubMedGoogle Scholar

Huang K-L, Liu T-Y, Huang Y-C, et al. Functional outcome in acute stroke patients with oropharyngeal dysphagia after swallowing therapy. J Stroke Cerebrovasc Dis. 2014;23(10):2547–2553. doi:10.1016/j.jstrokecerebrovasdis.2014.05.03125245482

 PubMed Web of Science ®Google Scholar

Vasant DH, Michou E, O’Leary N, et al. Pharyngeal electrical stimulation in dysphagia poststroke: a prospective, randomized single-blinded interventional study. Neurorehabil Neural Repair. 2016;30(9):866–875. doi:10.1177/154596831663912927053641

 PubMed Web of Science ®Google Scholar

Lee KW, Kim SB, Lee JH, et al. The effect of early neuromuscular electrical stimulation therapy in acute/subacute ischemic stroke patients with dysphagia. Ann Rehabil Med. 2014;38(2):153. doi:10.5535/arm.2014.38.2.15324855608

 PubMedGoogle Scholar

Lee KW, Kim SB, Lee JH, et al. Effects of neuromuscular electrical stimulation for masseter muscle on oral dysfunction after stroke. Ann Rehabil Med. 2019;43(1):11. doi:10.5535/arm.2019.43.1.1130852866

 PubMedGoogle Scholar

Guillén-Solà A, Messagi Sartor M, Bofill Soler N, et al. Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: a randomized controlled trial. Clin Rehabil. 2017;31(6):761–771. doi:10.1177/026921551665244627271373

 PubMed Web of Science ®Google Scholar

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):40–42. doi:10.5507/bp.2017.04329097820

 PubMed Web of Science ®Google Scholar

Falsetti P, Acciai C, Palilla R, et al. Oropharyngeal dysphagia after stroke: incidence, diagnosis, and clinical predictors in patients admitted to a neurorehabilitation unit. J Stroke Cerebrovasc Dis. 2009;18(5):329–335. doi:10.1016/j.jstrokecerebrovasdis.2009.01.00919717014

 PubMed Web of Science ®Google Scholar

Langmore SE. Efficacy of behavioral treatment for oropharyngeal dysphagia. Dysphagia. 1995;10(4):259–262. doi:10.1007/BF04314197493507

 PubMed Web of Science ®Google Scholar