NeuroRehabilitation xx (20xx) x–xx 1

DOI:10.3233/NRE-172306
IOS Press

1 Effects of neuromuscular electrical

2 stimulation in patients with parkinson’s
disease and dysphagia: A randomized,

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3

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4 single-blind, placebo-controlled trial

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5 Ji-Su Parka , Dong-Hwan Ohb , Na-Kyoung Hwangc and Jung-Hoon Leed,∗
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a Department of Rehabilitation Science, Graduate School, Inje University, Gimhae, Republic of Korea
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b Department of Occupational Therapy, Kyung-dong University, Wonju, Republic of Korea
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c Department of Occupational Therapy, Seoul North Municipal Hospital, Seoul, Republic of Korea
d Department of Physical Therapy, College of Nursing, Healthcare Sciences and Human Ecology,

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10 Dong-Eui University, Busan, Republic of Korea

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11 Abstract.
12 BACKGROUND: Neuromuscular electrical stimulation has been used to improve swallowing function in neurologic patients
13 with dysphagia, but its effect on patients with dysphagia and Parkinson’s disease remains unclear.
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14 OBJECTIVES: This study aimed to identify the effect of effortful swallowing combined with neuromuscular electrical
15 stimulation as a novel treatment approach in dysphagic patients with Parkinson’s disease.
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16 METHODS: Participants were randomly allocated to an experimental group (n = 9) or a placebo group (n = 9). The exper-
17 imental group simultaneously received neuromuscular electrical stimulation with effortful swallowing, while the placebo
18 group received sham neuromuscular electrical stimulation with effortful swallowing. All participants received the treatment
19 for 30 min/day at five sessions per week for 4 weeks. Both groups also received the same conventional dysphagia therapy.
20 RESULTS: The experimental group showed significant differences in horizontal movement (p = 0.038) and vertical movement
(p = 0.042) compared to the placebo group, but showed no significant differences in the oral (p = 0.648) or pharyngeal phase
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21

22 (p = 0.329) of the Videofluoroscopic Dysphagia Scale compared to the placebo group, except for the Penetration-Aspiration
23 Scale (p = 0.039).
24 CONCLUSIONS: We demonstrated that neuromuscular electrical stimulation applied to the infrahyoid region combined
25 with effortful swallowing effectively increased hyoid bone movement and reduced aspiration in dysphagic patients with
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26 Parkinson’s disease.

27 Keywords: Dysphagia, Parkinson’s disease, swallowing, neuromuscular electrical stimulation

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28 1. Introduction oropharyngeal transit time, reduced hyoid bone 31

movement, decreased muscle strength, and aspiration 32

29 Dysphasic patients with Parkinson’s disease pneumonia (Kim et al., 2015). The main causes of 33

30 (PD) have common symptoms such as delayed these are bradykinesia and rigidity in the oropharyn- 34

∗ Address
geal phase, incomplete cricopharyngeal relaxation, 35
for correspondence: Jung-hoon Lee, Department of
reduced cricopharyngeal opening, and delayed initi- 36
Physical Therapy, College of Nursing and Healthcare Sciences,
Dong-Eui University, 176, Eomgwangno, Busanjin-gu, Busan, ation of the swallowing reflex in the pharyngeal phase 37

47340, Republic of Korea. E-mail: dreampt@hanmail.net. (Ertekin et al., 2002; Jost, 2016; Nagaya, Kachi, & 38

1053-8135/18/$35.00 © 2018 – IOS Press and the authors. All rights reserved
 2 J.-S. Park et al. / Effects of neuromuscular electrical stimulation in patients with parkinson’s disease

39 Yamada, 2000). There are disturbances throughout 1) oropharyngeal dysphagia after PD confirmed by 87

40 the oral, pharyngeal, and esophageal phases, partic- a videofluoroscopic swallowing study (VFSS), (2) 88

41 ularly the first two. no significant cognitive deficit (Mini-Mental State 89

42 Neuromuscular electrical stimulation (NMES) is Examination score >20), (3) age <75 years, (4) ability 90

43 widely used in clinical practice to improve the to swallow voluntarily, and (5) Hoehn and Yahr scale 91

44 swallowing function of patients with various neu- <3 points. The exclusion criteria were as follows: 92

45 rological diseases. NMES is a therapeutic method (1) other neurological disease, (2) having undergone 93

46 that delivers stimulation to the muscles through sur- deep brain stimulation, (3) neck pain or neck surgery, 94

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47 face electrodes. It is used in facilitation techniques (4) implanted electronic devices including cardiac 95

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48 to increase swallowing muscle strength and sensory pacemakers or defibrillators, (5) severe communica- 96

49 awareness, thereby improving or recovering the swal- tion problem, (6) severe dyskinesia of the head and 97

50 lowing function. Several studies reported the effects neck, and (7) history of seizure or epilepsy. Three 98

51 of NMES on patients with dysphagia after neurologic participants did not meet the criteria for inclusion and 99

52 disorder (Baijens et al., 2013; Calabro et al., 2016; were excluded from the study. Therefore, this study 100

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53 Park, Oh, Hwang, & Lee, 2016). As a result, improved involved a total of 18 participants. Written informed 101

54 hyoid bone movement, decreased pharyngeal residue, consent was obtained from all patients. The study 102

55 and reduced aspiration were observed. was approved by the Institutional Review Board of 103

56 Humbert et al. (2006) reported various elec- Dong-eui University. 104

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57 trode placement methods for NMES. The electrode
58 arrangement of the NMES is based on the hyoid bone 2.2. Procedures 105

59 and is applied to muscle groups such as the suprahy-

60 oid and infrahyoid muscles. Recently, Park et al. This study had a prospective two-group (experi- 106

61 (2012) introduced a new electrode placement method mental and placebo group) randomized trial design. 107
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62 of applying two pairs of electrodes to the infrahyoid Participants were randomly allocated to an experi- 108

63 muscles. This is a concept that provides electrical mental group (n = 9) or a placebogroup (n = 9) by 109

64 stimulation to the infrahyoid muscles to deliberately blocked randomization to ensure an equal number 110

65 pull down the hyoid bone, overcome it, and lift it again in both groups by an occupational therapist blinded 111

66 through effortful swallowing. In other words, resis- to the patients. 112

tance is known to offer more intense training. Thus, The experimental group received NMES using a
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67 113

68 NMES combined with effortful swallowing can be an VitalStim (Chattanooga Group, Hixson, TN, USA) 114
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69 alternative approach for dysphasia. Park et al. (2016) with effortful swallowing, whereas the placebo group 115

70 reported improved hyoid movement and swallowing received sham NMES with effortful swallowing. Two 116

71 function after use of this method in patients with dys- pairs of electrodes were placed in the anterior neck 117

72 phagia after stroke. However, no study has reported region. The electrodes were placed in the infrahyoid 118

73 on electrical stimulation applied to the infrahyoid area targeting the sternohyoid muscles (omohyoid, 119
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74 muscles in PD patients with dysphagia. Therefore, sternohyoid, and sternothyroid) (Fig. 1). 120

75 it is important to use the new electrode placement The electrical stimulation unit provided two chan- 121

76 method in patients with PD. This study aimed to nels of bipolar electrical stimulation at a fixed 80-Hz 122

77 investigate the effect of a new NMES placement pulse rate and a fixed biphasic pulse duration of 123

700 ␮s. In the experimental group, the electrical

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78 method on hyoid bone movement and swallowing 124

79 function in dysphagic patients with PD. stimulation was applied to induce a strong muscle 125

contraction; in the placebo group, sham stimulation 126

was used at an intensity of 1.0 mA. The duration of the 127

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80 2. Methods electrical stimulation in this study was set at 30 min 128

per session. The intensity was gradually increased in 129

81 2.1. Participants 0.5 mA intervals for the experimental group. All par- 130

ticipants were asked to perform an effortful swallow 131

82 This study was conducted from July 2016 to using their saliva during the stimulation. Except for 132

83 December 2016. Patients with PD and dysphagia, stimulation intensity, the procedure for the placebo 133

84 treated (n = 21) at a university hospital and local group was the same. 134

85 rehabilitation centre in the Republic of Korea were Both groups received the same conventional dys- 135

86 recruited. The inclusion criteria were as follows: phagia therapy (CDT) for 30 minutes after the NMES 136
 J.-S. Park et al. / Effects of neuromuscular electrical stimulation in patients with parkinson’s disease 3

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Fig. 1. Electrode placement.

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Fig. 2. Flowchart of this study.

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137 intervention that comprised orofacial muscle exer- Bethesda, MD, USA). The analysis was conducted 146

138 cises, thermal tactile stimulation, and therapeutic or of the VFSS image using the same method described 147
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139 compensatory maneuvers. An experienced occupa- in a previous study (Park et al., 2016). The swal- 148

140 tional therapist performed the CDT in all participants lowing process was captured using a frame during 149

141 for 30 min/day, five days a week, for 4 weeks. A the VFSS. Two picture frames of the VFSS were 150

142 flowchart of this study is shown in Fig. 2. used for the analysis: 1) rest position of the hyoid, 151

and 2) maximal excursion of the hyoid bone. The 152

143 2.3. Outcome measurement application of the vertical C2–C4 axis used an image 153

rotation technique. A straight line was drawn between 154

144 We assessed hyoid bone movement using the the most antero-inferior points, C2 and C4, and the 155

145 Image J program (National Institutes of Health, images were rotated to the true vertical 90◦ . The 156
 4 J.-S. Park et al. / Effects of neuromuscular electrical stimulation in patients with parkinson’s disease

157 antero-inferior corner of C4 was identified on each and placebo group were calculated. Effect size of 0.2, 206

158 image and used as an “anchor point,” which repre- 0.5 and 0.8 represent a small, moderate or large effect 207

159 sents a stable point (resting position) of the hyoid respectively. 208

160 before swallowing from the distance of the moving

161 hyoid. Hyoid displacement represents the distance
162 from the resting position to the maximal excursion
163 position during swallowing; the most supero-anterior 3. Results 209

164 point of the hyoid indicates maximum displacement

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165 after swallowing. Horizontal and vertical displace- 3.1. General characteristics of participants 210

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166 ment of the hyoid were calculated by subtracting the
167 point values (x, y) measured on the resting position The patients’ general characteristics are described 211

168 image (pre-swallow image) from that measured on in Table 1 with no significant between the two groups 212

169 the maximal excursion image: anterior displacement, (p > 0.05). 213

170 (x2-x1)-(Ox2-Ox1); vertical displacement: (y2-y1)-

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171 (Oy2-Oy1). The pre-swallow image coordinates were
172 x1 and y1 , while the maximal excursion image coor- 3.2. Effects on kinematics of the hyoid bone 214

173 dinates were x2 and y2 . The coordinates of the anchor

174 point of the pre-swallow image were Ox1 and Oy1 , The experimental group showed significant 215

improvement in horizontal and vertical movements

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175 while those of the excursion image were Ox2 and 216

176 Oy2 . of the hyoid bone (p = 0.015 and p = 0.008 respec- 217

177 The Videofluoroscopic Dysphagia Scale (VDS) is tively), and the placebo group also showed significant 218

178 a comprehensive swallowing assessment based on improvement (p = 0.05 and p = 0.043 respectively). 219

179 the VFSS findings. The VDS is divided into the After the intervention, the experimental group 220
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180 oral stage (seven items: lip closure, bolus forma- showed significantly different values in horizon- 221

181 tion, tongue-to-palate contact, mastication, apraxia, tal movement (p = 0.038) and vertical movement 222

182 premature bolus loss, and oral transit time) and the (p = 0.042) compared to the placebo group (Table 2). 223

183 pharyngeal stage (seven items: pharyngeal triggering, In a comparison of the extent of change in the 224

184 vallecular residues, pyriform sinus residues, laryn- groups, both groups showed significant differences 225

geal elevation, pharyngeal wall coating, pharyngeal in vertical movement but not in horizontal movement
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185 226

186 transit time, and aspiration) (Kim et al., 2012). of the hyoid bone (p = 0.009 and p = 0.093, respec- 227

tively) (Table 3). Effect sizes were observed for the

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187 The Penetration-Aspiration Scale (PAS) is a 228

188 standard tool that reflects airway penetration and horizontal (0.9) and vertical movement (0.9) of the 229

189 aspiration. Penetration is defined as the passage of hyoid bone. 230

190 material into the larynx that does not pass below the
191 vocal folds, while aspiration refers to the action of
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192 material penetrating the larynx and entering the air- 3.3. Effects on swallowing function 231

193 way below the true vocal folds (Rosenbek, Robbins,

194 Roecker, Coyle, & Wood, 1996). The experimental group showed a significant 232

improvement in the total score (p = 0.021), the pha- 233

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ryngeal phase of VDS (p = 0.028), and the PAS 234

195 2.4. Statistical analysis (P = 0.007); the placebo group showed a significant 235

improvement only in the total score (p = 0.041). After 236

196 The statistical analyses were performed using the intervention, the experimental group showed no 237
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197 SPSS version 15.0 (IBM Corporation, Armonk, NY, significant differences in the oral (p = 0.648) and pha- 238

198 USA). Descriptive statistics are presented as means ryngeal (p = 0.329) phase of VDS compared to the 239

199 with standard deviations. To evaluate the intervention placebo group, except in PAS (p = 0.039) (Table 2). 240

200 effects, the Wilcoxon signed-rank test was used to A comparison of the extent of change in the groups 241

201 compare measures pre- and post-intervention in each revealed significant differences in PAS except for 242

202 group. The Mann-Whitney U test was used to com- the oral and pharyngeal phase of VDS (p = 0.006, 243

203 pare the intergroup changes in outcome measures. 0.903, and 0.308, respectively) (Table 3). Effect sizes 244

204 Significance level was set at p < 0.05. Effect sizes were observed for the oral phase (0.1) and pharyngeal 245

205 (Cohen d) of changed scores comparing experimental phase (0.5) of VDS and PAS (2.0). 246
 J.-S. Park et al. / Effects of neuromuscular electrical stimulation in patients with parkinson’s disease 5

Table 1
Characteristics of participants
Characteristics Experimental group (n = 9) Placebo group (n = 9)
Age (year), mean ± SD (range) 63.44 ± 13.55 54.67 ± 13.82
Gender, male/female 5/4 3/6
ICH 4 5
Infarction 5 4
Time since onset of stroke, weeks, mean ± SD (range) 36.44 ± 7.5 (29–48) 36.11 ± 7.94(28–50)
Stimulation intensity (mA) 13.2 ± 1.52 3.5 ± 1.12

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SD: standard deviation. ICH: Intra cerebral hemorrhage.

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Table 2
Changes in parameters before and after treatment
Experimental group Placebo group Between
(Mean ± SD) (Mean ± SD) group
Before After p-value Before After p-value p-values

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treatment treatment treatment treatment
VDS-total 59.22 ± 6.26 54.11 ± 5.62 0.021∗ 56.28 ± 9.35 53.28 ± 10.21 0.041∗ 0.690
VDS-oral phase 17.83 ± 1.64 17.39 ± 1.36 0.18 15.11 ± 6.35 14.22 ± 6.22 0.18 0.648
VDS-pharyngeal phase 41.39 ± 5.92 36.72 ± 5.67 0.028∗ 41.17 ± 4.38 39.06 ± 4.73 0.093 0.329
Horizontal displacement of the hyoid bone (cm) 1.36 ± 0.26 1.65 ± 0.17 0.015∗ 1.32 ± 0.13 1.41 ± 0.22 0.05∗ 0.038†

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Vertical displacement of the hyoid bone (cm) 1.39 ± 0.18 1.71 ± 0.25 0.008∗ 1.4 ± 0.18 1.5 ± 0.26 0.043∗ 0.042†
PAS 5.11 ± 1.45 2.33 ± 0.71 0.007∗ 4.11 ± 1.27 3.67 ± 1.32 0.429 0.039†
SD: standard deviation. VDS: videofluoroscopic dysphagia scale, PAS: penetration-aspiration scale, ∗ p < 0.05 by Wilcoxon test, † p < 0.05
by Mann-Whitney U test.

Table 3
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Comparison of the differences after the 6-week treatment in the two groups
Experimental group Placebo group Between group
(Mean ± SD) (Mean ± SD) p-value
VDS-total 5.11 ± 5.12 3 ± 3.44 0.426
VDS-oral phase 0.44 ± 0.92 0.89 ± 2.03 0.903
4.67 ± 5.31 2.11 ± 3.38
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VDS-pharyngeal phase 0.308

Horizontal displacement of the hyoid bone (cm) 0.29 ± 0.2 0.12 ± 0.17 0.093
Vertical displacement of the hyoid bone (cm) 0.32 ± 0.17 0.09 ± 0.14 0.009†
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PAS 2.78 ± 1.2 0.44 ± 1.59 0.006†

SD: standard deviation. VDS: videofluoroscopic dysphagia scale, PAS: penetration-aspiration scale, † p < 0.05 by Mann-Whitney U test.

247 4. Discussion epiglottic tilt (Jang, Leigh, Seo, Han, & Oh, 2015). 264
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However, when the NMES is applied to the infrahyoid 265

248 This study examined the effects of NMES com- muscles, the hyoid bone is lowered due to infrahyoid 266

249 bined with effortful swallowing for patients with PD muscle contraction. When the effortful swallowing 267

250 and dysphagia. We first attempted a new electrode is overcome, the hyoid bone move up again (Park 268
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251 placement method with proven efficacy in patients et al., 2012). In other words, since resistance occurs 269

252 with PD. during effort swallowing, it can be more effective in 270

253 The results of this study confirm that the experi- raising the hyoid bone than performing effort swal- 271

254 mental treatment was more effective for improving lowing only. Previous studies (Baijens et al., 2012, 272
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255 hyoid bone antero-superior movement than the 2013; Heijnen, Speyer, Baijens, & Bogaardt, 2012) 273

256 placebo treatment. Therefore, we demonstrated that using NMES for patients with PD did not measure 274

257 effortful swallowing with NMES applied to the hyoid movement; thus, direct comparison with this 275

258 infrahyoid muscles is an effective method for improv- study is difficult. However, the results of this study 276

259 ing hyoid bone movement. are similar to those of previous studies using NMES 277

260 The results of this study can be attributed to the fol- and effortful swallowing in stroke patients (Park et 278

261 lowing reasons. First, effortful swallowing is known al., 2012). 279

262 to be effective at increasing the antero-superior move- Improved hyoid bone movement is an important 280

263 ment of the hyolaryngeal complex and responding to factor for patients with dysphagia. This is because 281
 6 J.-S. Park et al. / Effects of neuromuscular electrical stimulation in patients with parkinson’s disease

282 the hyolaryngeal movement directly affects the pha- combined therapy and is more effective than effortful 334

283 ryngeal phase during swallowing. Therefore, we swallowing alone in muscle re-education for dyspha- 335

284 evaluated swallowing function using VDS based on gia (Park et al., 2016). Therefore, the application 336

285 VFSS. There was no significant difference between of these two methods is theoretically superior to 337

286 the two groups in swallowing function during the effortful swallowing only (Guillen-Sola et al., 2016). 338

287 oral and pharyngeal phase. Interestingly, for a more A three patients in the experimental group showed 339

288 accurate and sensitive assessment of penetration- signs of fatigue after a 30-minute treatment session, 340

289 aspiration, the PAS score on the 8-point scale showed which was due to the decrease of tolerance during the 341

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290 a significant intergroup difference, indicating that this intervention by elevation of the hyoid bone through 342

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291 intervention method is helpful for decreasing aspira- continuous swallowing. Careful observation of the 343

292 tion. In other words, this study showed that effortful patient’s level of fatigue is needed, but we believe 344

293 swallowing and NMES did not improve the over- that to elicit a therapeutic response such as improved 345

294 all swallowing function but was helpful for reducing swallowing function, patients need to be challenged 346

295 aspiration. to reach beyond the range of tolerable fatigue. 347

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296 The reduction in aspiration observed in this study This study applied NMES with effortful swallow- 348

297 may be due to several reasons. First, the reduction ing to patients with PD and dysphagia. As a result, 349

298 of aspiration is probably due to improvement of the hyoid bone movement was increased and the aspi- 350

299 antero-superior movement of the hyolaryngeal com- ration was reduced. Therefore, we recommend this 351

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300 plex. Enhancement of the antero-superior movement intervention to improve swallowing in patients with 352

301 of the hyolaryngeal complex affects the pharyngeal PD and dysphagia. 353

302 phase and is closely related to the airway protection This study has some limitations. First, sample 354

303 mechanism such as epiglottic tilt. More precisely, size may have influenced the results, therefore these 355

304 anterior and upward movement of the hyoid bone results cannot be generalized. Second, absence of 356
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305 affects the upper esophageal sphincter opening and follow-up after the end of intervention did not 357

306 airway protection, respectively (Park et al., 2016). allow for determination of the durability of effects. 358

307 Second, from a different point of view, a change in Third, brain imaging was not performed; hence, 359

308 the central nervous system induced by NMES can be swallowing-related cortical change could not be 360

309 explained to some extent. NMES has a central as well confirmed. 361

as peripheral effect, such as a change in skeletal mus-

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311 cles. NMES provides afferent input to the swallowing

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312 center in the brain stem or pharyngeal motor cortex

5. Conclusion 362
313 and activates it (Guillen-Sola et al., 2016). Apply-
314 ing electrical stimulation to the pharynx changes the
This study demonstrated that NMES is effective 363
315 excitability of the pharyngeal motor cortex, i.e., facil-
in improving the oropharyngeal swallowing function 364
316 itation of neural plasticity possibly has a positive
in patients with Parkinson’s disease and dysphagia.
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365
317 effect on improved swallowing function.
Therefore, NMES can be recommended as a medical 366
318 Third, it can be explained by the synergistic effect
treatment. 367
319 of NMES and effortful swallowing. NMES is known
320 to be effective in selectively stimulating type 2 fibers
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321 as a treatment that is known to effectively strengthen

322 muscles, prevent atrophy, and retrain the neuromus- Conflict of interest 368

323 cular system by inducing muscle contraction via

324 nerve fiber depolarization (Freed, Freed, Chatburn, This research was performed without funding. No 369
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325 & Christian, 2001; Permsirivanich et al., 2009; Shaw conflicts of interest are declared. 370

326 et al., 2007). However, unlike NMES, effortful swal-

327 lowing spontaneously induces muscle contraction,
328 which further stimulates type 1 fibers (Shaw et al., References 371
329 2007). Swallowing-related muscles, like other skele-
330 tal muscles, are composed of type 1 and 2 muscle
Baijens, L. W., Speyer, R., Passos, V. L., Pilz, W., Roodenburg, N., 372
331 fibers, but type 2 fibers tend to be heavier. The syn- & Clave, P. (2012). The effect of surface electrical stimulation 373
332 chronous recruitment of both type I and type II fibres on swallowing in dysphagic Parkinson patients. Dysphagia, 374

333 can generate greater swallowing muscle force during 27(4), 528-537. doi: 10.1007/s00455-011-9387-4 375
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