29 March 2021: Clinical Research
Effects of Synchronized Neuromuscular Electrical Stimulation (NMES) on the Submental Muscles During Ingestion of a Specified Volume of Soft Food in Patients with Mild-to-Moderate Dysphagia Following StrokeQian Zhang12ACE, Shuang Wu12ABFG*
Med Sci Monit 2021; 27:e928988
BACKGROUND: Neuromuscular electrical stimulation (NMES) is a method for producing regular contractions of muscles that have been paralyzed. This study aimed to evaluate the effects of synchronized NMES on the submental muscles during ingestion of a specified volume of soft food in patients with mild-to-moderate dysphagia following stroke.
MATERIAL AND METHODS: Eighty-three patients with mild-to-moderate dysphagia following stroke were enrolled and randomly divided into 3 groups: conventional training (CT) (n=28), eating training (ET) (n=28), and intensive swallowing training (IST) (n=27). The CT group received conventional swallow training, the ET group was given additional individual feedings with a specified volume of soft food, and the IST group received intensive swallowing training with synchronized NEMS. All of the patients were evaluated before and after the treatment with a modified barium swallow, and the Dysphagia Outcome and Severity Scale (DOSS); the numbers of patients with Stroke-Associated Pneumonia (SAP) and wet voice also were assessed.
RESULTS: After 6 weeks, DOSS scores improved in patients in all 3 groups, and there were significant differences among the groups in their scores (P<0.001 for both measures). In the CT and ET groups, there was a statistically significant difference in the number of patients with SAP before and after treatment (P=0.010 and P<0.001, respectively). There also were fewer cases in the IST group than in the CT (P=0.042) and ET groups (P=0.011). After completion of treatment, compared with the first treatment, there were significantly fewer patients with wet voices in the CT (P<0.001) and IST groups (P<0.001).
CONCLUSIONS: Feeding a specified volume of soft food plus synchronized NMES of the submental muscles can improve the swallowing function of patients with mild-to-moderate dysphagia following stroke and it reduces their risk of food aspiration.
Keywords: Deglutition Disorders, Electric Stimulation Therapy, Feeding Methods, Stroke, Aged, Aged, 80 and over, Deglutition, Eating, Facial Muscles, Food, Middle Aged, Random Allocation, stroke rehabilitation, Treatment Outcome
Dysphagia is one of the most common symptoms following stroke. About 37% to 78% of patients who have an acute stroke develop dysphagia, and it is closely related to stroke-associated pneumonia (SAP), dehydration, and malnutrition . Stroke also can result in a cognitive deficit, which is likely to affect other functions, such as swallowing. Tools such as the Abbreviated Mental Test Score (AMTS) can be used to evaluate cognitive deficit associated with stroke . A composite score ≤7 on the 10 questions is indicative of a cognitive deficit and the scale has good reliability and validity for assessment of cognitive impairment [3–5].
A videofluorographic swallowing study, also known as a modified barium swallow, is one way to evaluate swallowing, and is considered the instrument of choice by many clinicians who specialize in swallowing disorders .Various volumes and textures of food and liquid are administered and clinical impressions of the presence and degree of swallowing impairment are obtained from the radiographic images; with this method, judgments also are made regarding the coordination and timing of swallowing events .
The Dysphagia Outcome and Severity Scale (DOSS) is another evaluation method, based on a modified barium swallow. This scale can be used not only to assess swallowing function, but also to assess dietary, independence, and nutritional levels . DOSS divides swallowing function into 7 levels, with lower levels indicating more severe dysphagia . Level 1 represents severe dysphagia, wherein the patient cannot safely tolerate any oral nutrition, and has ≥1 of the following manifestations: severe pharyngeal residue or leakage and residue of oral bolus, which cannot be removed; asymptomatic aspiration when eating 2 or more types of sticky food; non-functional coughing; and an inability to complete swallowing. Level 7 represents normal swallowing function, wherein the patient can eat normally under any condition, with no compensation strategy or extra time needed. The 7 levels of swallowing function on the scale are further divided into 3 grades of dysphagia: Levels 5 and 4 for mild dysphagia; Levels 2 and 3 for moderate dysphagia; and Level 1 for severe dysphagia [9,10].
Patients who have a mild-to-moderate swallowing dysfunction often rely partially or completely on a nasogastric tube. Guidelines for clinical nutrition indicate that for patients who have insufficient oral intake of food during the acute phase of stroke, enteral nutrition should be given via a nasogastric tube. When no risk factors are present, intermittent boluses of food, given 6 times a day for 1 hour each, are just as safe . Many experts recommend maintaining minimal oral intake, such as giving ice chips patients who are severely dysphagic, to promote oral hygiene and trigger swallowing ability, and they also recommend that patients with dysphagia be fed orally with food of a “safe texture” to promote oral hygiene and swallowing rehabilitation . Guidelines from the European Society for Clinical Nutrition and Metabolism (ESPEN) provide 88 recommendations for feeding patients with stroke and indicate that diets in which the texture of the food is modified and liquids are thickened may reduce the incidence of aspiration pneumonia in patients who have experienced a stroke and have dysphagia , but such diets are associated with an increased risk for malnutrition compared to that in patients whose swallowing function is intact .Therefore, in stroke rehabilitation, ways to promote effective oral intake and to reduce the incidence of complications are areas of significant study .
In dysphagia, the pharyngeal location is the area most prone to aspiration, which affects the safety and effectiveness of eating orally. The main manifestations of dysphagia are a decreased ability to use the mouth; a delay, lack, or prolongation of the initiation of the swallowing reflex; and a reduction in the lifting and forward movement ability of the tongue-throat complex.
Based on the principle of “plasticity” of the central nervous system, various external interventions can influence the plasticity of the nerves. These are defined as behavioral or non-behavioral interventions . The former encompasses active and/or assisted athletic training and muscle-strengthening exercises that are used for patients with dysphagia; the therapeutic exercise commonly used in swallowing training; airway protection; compensatory swallowing training; biofeedback swallowing training; and behavioral interventions. A behavioral intervention is one that an individual accepts passively and for which a clear and direct response is not required to achieve the regulatory effect.
Neuromuscular electrical stimulation (NMES) is a non-behavioral therapy for dysphagia. Because an optimal NMES system uses the minimal stimulus frequency that produces a fused response, the typical frequency range is 10 to 50 Hz . NMES induces muscle contraction or simulates normal autonomic movement through excitatory contraction to improve or restore the function of stimulated muscles or muscle groups . Skeletal muscle contains “fast” and “slow” muscle fibers that are distinguished on the basis of contraction kinetics; these fiber types are generally categorized according to differences in histochemistry. Slow-twitch, oxidative Type I fibers generate lower forces, but are fatigue resistant; fast-twitch, glycolytic Type II fibers generate higher forces but fatigue more rapidly . Because of the lower stimulation thresholds, NMES preferentially recruits Type II fibers, followed by recruitment of type I muscle fibers . Pharyngeal muscle contraction increases the protein content and capillary density of muscle, resulting in an enhanced muscle training compensation effect, thereby improving the safety of swallowing .
Although NMES has several important advantages in the treatment of swallowing dysfunction, simple electrical stimulation training is entirely passive; there is no active participation of the patient during treatment process, which is contrary to the principle of muscle strength training. Thus, active ingestion training is an important behavioral intervention for the treatment of dysphagia. In keeping with food traits recommended by the European Society for Swallowing Disorders , in a previous study , we found that a 5-mL soft bolus produced greater activation and a longer contraction time in the submental muscles of patients with post-stroke pharyngeal dysphagia. In addition, because of the high viscosity of the soft bolus, swallowing also was safer. However, risks still existed, such as food sticking to the throat, and an increased risk of aspiration. We also found that the degree of activation of the submental muscles, which are the key muscles around the hyoid bone, was significantly and positively correlated with increased difficulty in swallowing .
Tongue-hold swallow is one part of the exercise protocol for intensive swallowing (IS), which targets the swallowing muscles that are desirable for reversing sarcopenia and age-related dysphagia . In tongue-hold swallow, patients are asked to hold their tongue gently between their teeth and then swallow their saliva with their tongue in a straight position . Recent research using simultaneous pharyngeal manometry and intramuscular electromyography has confirmed that this tongue-hold maneuver significantly increases the activation of the superior pharyngeal constrictor, as well as the genioglossus and the submental musculature .
In a study by Marilia et al that enrolled 83 patients with subacute stroke and dysphagia, 17 received traditional dysphagia therapy plus a swallow maneuver. At the same time that the swallow maneuver was performed, 2 Intelect VitalStim electrodes were placed just at or above the level of the thyroid notch over the thyrohyoid muscle. Combining the traditional dysphagia therapy with NMES improved the swallowing function and feeding in the patients with severe-to-profound post-stroke dysphagia .
Another study explored the effects of an intensive exercise-based swallowing program that incorporated lingual and respiratory exercises for patients with Parkinson disease (PD). The results suggested that an intensive exercise-based swallowing program had an overall positive and potentially additive or synergistic effect after a 4-week training period .
The aim of the present study was to evaluate the effects of synchronized NMES on the submental muscles during ingestion of a specified volume of soft food in patients with mild-to-moderate dysphagia following stroke.
Material and Methods
The Declaration of Helsinki, which dictates ethics in clinical trials, was taken into consideration in development of the present study. The methods used were approved by the Ethics Committee of the Affiliated Hospital of Guizhou Medical University. All patients were asked to sign a written informed consent form before data collection.
Eighty-three patients with post-stroke pharyngeal dysphagia were enrolled at the Affiliated Hospital of Guizhou Medical University between June 1, 2018 and May 31, 2020. The inclusion criteria were as follows: clinical diagnosis of initial cerebral infarction or cerebral hemorrhage, confirmed by brain computed tomography or magnetic resonance imaging (MRI); disease course of 1 to 3 months; age 40 to 80 years old; stable vital signs; ability to swallow at least 50 mL of soft food in 30 min; a simple intelligence test scale AMTS score >7 points [2–5]; a DOSS score of 2 to 6, suggesting mild-to-moderate dysphagia [8–10]; pharyngeal dysphagia or oropharynx dysphagia diagnosed with a modified barium swallow [6,7]; and achievement of direct eating. The exclusion criteria were as follows: malignant tumors, serious medical diseases or other neurological diseases; mental disorders or cognitive dysfunction; dysphagia not triggered by stroke; head, neck, or gastroesophageal surgery; and dysphagia combined with an uncontrolled lung infection. Patients who met the inclusion criteria were divided into 3 groups, using the random number table method: conventional training (CT), eating training (ET), and intensive swallowing training (IST). The same experienced physician generated the random allocation sequence, enrolled the participants, and assigned them to the interventions. The therapist was aware of the allocation, but all the physicians who conducted the evaluation procedures – including all the scale measurements and analysis of the modified barium swallow data – were blinded to group assignment.
Each patient received the following conventional swallowing training: (1) oral-motor and pharyngeal swallowing exercises to strengthen the swallowing musculature (eg, lip, tongue, and jaw exercises, Masako exercise, Shaker exercise, gargling or vocal cord adduction exercises); (2) instruction in airway protection maneuvers (supraglottic swallow or supersupraglottic swallow); (3) thermal/tactile stimulation; (4) oral hygiene education; (5) direct eating training (ET) as per each individual’s willingness; and (6) positioning strategies (eg, chin tuck, head turn, or head tilt) and practice with swallowing maneuvers (eg, Mendelsohn maneuver). The choice of specific positioning strategies and swallowing maneuvers or exercises was based on DOSS score and clinical swallowing examination. Treatment sessions each lasted 30 min and were performed once a day for 5 days a week for 6 weeks, for a total of 30 training sessions.
In addition, NMES treatment with the Intelect VitalStim model 5900 was performed. Before treatment, a patient’s neck skin was cleaned with 75% medical alcohol, or with physiological saline for those allergic to alcohol, to reduce interference and increase conductivity. The treatment electrode was placed on both sides of the anterior median line of the neck, between the submental and the upper part of the hyoid bone, and exposure was limited to the maximum contraction of the muscle with the electrode that a patient could withstand, which was usually 6.3 to 13.2 mA (average 11.6 mA). During direct ET, patients were kept relaxed and in a compensatory and safe eating position in a quiet environment. Suitable tableware was chosen, based upon a patient’s tolerance for and choice of paste food to eat. During direct ET, patients were asked to swallow the first mouthful before taking the next one, and not to eat too fast .
ET GROUP: In addition to the conventional swallowing training, this group of patients was given direct ET with soft food (viscosity 4750 to 5113 cP) , depending on their willingness to eat it. The food was prepared with thickener and water at a temperature of 25°C. With a patient seated, the therapist applied a 5-mL food bolus onto the middle of the tongue using a spoon. The patient was allowed to swallow, and an additional 1 to 2 swallowing actions were performed to clean the food that remained in the pharynx. During the first week, the training time was gradually increased, based on patient tolerance; a maximum of 100 mL of food was fed. Each training session lasted for 30 min and had 30 swallowing actions. The training sessions were held for 5 days per week for 6 weeks, for a total of 30 days.
IST GROUP: In addition to the conventional swallowing therapy, the patients in the IST group received intensive swallowing training with tongue-hold swallow [22,23]. During direct eating/swallowing training, a patient was asked to hold their tongue gently between their teeth. The therapist then applied a 5-mL food bolus onto the middle of the tongue using a spoon, and the patient swallowed it with their tongue in a straight position when they felt the maximum intensity of current stimulation in the submental muscles with synchronized electrical stimulation using the VitalStim neuromuscular stimulator. The NMES treatment was performed the same as in the CT group. The patients in the IST group also were asked to finish swallowing the soft food bolus within 30 min, and they received no more than 100 mL of the food. Each training session lasted for 30 min and had 30 swallowing actions. The training sessions were held for 5 days per week for 6 weeks, for a total of 30 days.
Before and after ET, sputum and secretions in the mouths of patients in all 3 groups were cleaned up. When patients experienced bucking, eating was immediately stopped, the patients were instructed to cough, and the Heimlich technique was used, if necessary . In cases of serious bucking, a fiberoptic bronchoscope was to be used to clear the foreign body from the airway; however, none of the patients had serious bucking.
ADJUSTMENT OF VISCOSITY OF THE FOOD BOLUS: Food with 2 different viscosities was prepared, using a thickener (Urdiet, Guangzhou, China) that consisted of iohexol and water, and the viscosity value was measured with an NDJ-5S Rotational Viscometer (Shanghai Fangrui, Shanghai, China) at a temperature of 25°C. The 3 solutions were as follows: 1. iohexol aqueous solution: viscosity 5 to 10 mPa/s; 2. nectar-like bolus: viscosity 272 to 343 mPa/s; and 3. soft bolus: viscosity 4750 to 5113 mPa/s .
VITALSTIM NEUROMUSCULAR ELECTRICAL STIMULATION:
Electrical stimulation was performed with an Intelect VitalStim model 5900 (Chattanooga Group, Hixson, Tennessee, United States). The parameters set were bidirectional square wave, waviness width 300 μs, fixed-frequency 80 Hz, and galvanic stimulation intensity 0 to 25 mA.
MODIFIED BARIUM SWALLOW:
The modified barium swallow examination was performed using a remote-controlled, twin-bed PLD5000 X-ray machine (Perlead, Zhuhai, China). All subjects were examined in both a 90-degree sitting and a lateral position, according to the evaluation criteria for DOSS. For patients who could not sit still, the torso was fixed onto the examination chair using the waist fixation strap, with the patient’s head fixed using a cushion behind the neck to avoid interference with the swallowing inspection. The video examination area was from the top of the nasal cavity down to the 7th cervical vertebra. During the examination, each patient was asked to swallow 5 mL of a nectar-like bolus, iohexol aqueous solution, and a soft bolus; 6 swallows were completed – 3 in a sitting position and 3 in a lateral position. Each patient underwent this assessment before and after treatment. In the event of coughing, a patient was instructed to try to cough up the inhaled bolus, and before proceeding to the next step, a wet voice assessment and pharyngeal auscultation were performed to ensure that there was no wet voice or any buzzing or blisters heard in the throat.
Data from the patients’ modified barium swallow recordings and on their oral eating abilities were graded using a DOSS scale [8–10] and their efficacy and total efficiency were calculated. Treatment was considered markedly effective if the DOSS score increased by >2 levels, effective if the score improved by ≤2 levels, and ineffective if there was no change in DOSS. The formula for the total rate of effectiveness in the 3 groups of patients was as follows: Total efficiency =(number of cases with markedly effective outcome+number of cases with effective outcome)/(total number of cases)×100%
STROKE-ASSOCIATED PNEUMONIA: Stroke-associated pneumonia (SAP) refers to infective inflammation of the lung parenchyma (including the alveolar wellsite and the pulmonary interstitium) in patients who have had a stroke and had no prior pulmonary infection .The evaluation criteria for SAP were new findings of pulmonary invasive lesions on imaging; fever ≥38°C; new cough or exacerbation of original respiratory symptoms, with or without chest pain; signs of lung consolidation and/or moist rales; and peripheral blood leukocytes ≥10×109/L or ≤4×109/L. The diagnostic criteria were new findings of pulmonary invasive lesions on imaging plus ≥2 clinical indications of an infection. In the present study, none of the patients had SAP at enrollment and the number of cases of SAP in the 3 groups was assessed after 6 weeks of treatment.
WET VOICE CASES AND OCCURRENCES:
Wet voice refers to a change in vocal pitch due to the attachment to or retention of a bolus or foreign body on the vocal cords. All of the patients were assessed for wet voice before and immediately after the end of each eating treatment. Before each treatment, the patients said their names or a paragraph at a normal volume. After completing the eating treatment, the names or the same paragraph were repeated to determine whether there were changes in tone such as hoarseness, reduced pitch, or humming in the voice. The number of patients in each group who had a wet voice between the end of the first and the 30th treatments was recorded.
The data were analyzed and processed by SPSS statistical software, version 21.0. All data were tested for normal distribution before analysis. Data following a normal distribution were expressed as means±standard deviation. Data following a non-normal distribution were expressed as medians±quartile spacing, and were analyzed using a non-parametric median. Quartile data were analyzed using a chi-square test. Differences in age, disease course, neurological function score, and nutritional status among the 3 groups prior to treatment were analyzed with a 1-way analysis variance (ANOVA) and a Kruskal-Wallis test. Before and after treatment, the DOSS assessment, the number of SAP cases, the number of occurrences and cases of wet voice, the number of tube-feeding cases, and the differences before and after treatment were subject to a Wilcoxon rank sum test. The Kruskal-Wallis test (for multiple independent samples) was used to compare the treatment effects among the 3 groups. When the difference was statistically significant, Fisher’s least significant difference
Median DOSS scores and interquartile ranges for swallowing function after treatment were 4 (3.75), 5 (4.75), and 6 (6) in the CT, ET, and IST groups, respectively. In all 3 groups, it was significantly better than before treatment (all P<0.001; Table 2). The IST group had the best swallowing function after treatment, followed by the ET group; the CT group had the worst swallowing function. Total efficacy, as assessed by DOSS score after treatment, was significantly better in the IST group (96.3%) than in the CT (67.9%, P<0.001) and ET groups (78.6%, P<0.001) (Table 3).
There were no cases of acute lung infection in any of the patients at the time of enrollment. During the treatment period, patients in all 3 groups experienced SAP. There were significant differences before and after treatment in the CT (n=6, 21.4%; P=0.010) and ET groups (n=15, 53.6%; P<0.001) but not in the IST group (n=2, 7.4%; P=0.160). The rate of new SAP cases was the highest in the ET group. A pairwise comparison showed that there were statistically significant differences between the IST and ET groups (P=0.011) and between the IST and CT groups (P=0.042) after treatment (Table 4).
WET VOICE CASES:
There was no statistically significant difference in the number of cases of wet voice among the 3 groups after the first training (P=0.51). After the 30th treatment, the number of cases of wet voice was significantly lower than before treatment in the CT (n=7, 25.0%; P<0.001) and the IST groups (n=6, 22.2%; P<0.001). There was no statistically significant difference in the number of cases in the ET group before and after treatment (n=21, 75.0%; P=0.480). There were statistically significant differences among the 3 groups (P<0.001), and the number of cases of wet voice was higher in the ET group than in the CT group (P<0.001) or the IST group (P<0.001) after 30 treatments (Table 5).
The present study had some limitations. First, the results cannot be generalized because of the small sample size. Also, the research was performed at a single center. Because the intervention period was only 6 weeks, it was not possible to evaluate long-term effects. Only patients with mild or moderate stroke were included, and none with severe dysphagia associated with stroke; therefore, the results cannot be generalized to every patient who has had a stroke. Bias could also be an issue because the patients enrolled were in the convalescence stage of stroke recovery and the possibility of natural recovery cannot be ruled out. Therefore, no definitive conclusions can be drawn about the treatment until a study is conducted with a true control group and that addresses the limitations previously described.
The mechanism underlying NMES also should be explored, not only to identify the actual swallowing function, but also to understand the relationship between neural activity in the brain and the muscles. In future studies, brain monitoring technologies such as functional near infrared spectroscopy, functional MRI, and diffuse tensor imaging should be employed to estimate brain function as a way to evaluate the proposed treatment methods.
Feeding a specified volume of soft food with synchronized NMES of the submental muscles can improve swallowing function in patients with mild-to-moderate dysphagia following stroke and it can reduce their risk of food aspiration.
TablesTable 1. Patient demographics. Table 2. Differences in DOSS scores before and after treatment. Table 3. Evaluation of training effectiveness based on DOSS level scores after treatment. Table 4. Differences among groups in incidence of SAP before and after treatment. Table 5. Differences among the groups in incidence of wet voice before and after treatment.
1. Martino R, Foley N, Bhogal S, Dysphagia after stroke: Incidence, diagnosis, and pulmonary complications: Stroke, 2005; 36; 2756-63
2. Sun JH, Tan L, Yu JT, Post-stroke cognitive impairment: Epidemiology, mechanisms and management: Ann Transl Med, 2014; 2; 80
3. Mansutti I, Saiani L, Palese A, Detecting delirium in patients with acute stroke: A systematic review of test accuracy: BMC Neurol, 2019; 19; 310
4. Quinn TJ, Elliott E, Langhorne P, Cognitive and mood assessment tools for use in stroke: Stroke, 2018; 49; 483-90
5. Hodkinson HM, Evaluation of a mental test score for assessment of mental impairment in the elderly: Age Ageing, 1972; 1; 233-38
6. Martin-Harris B, Jones B, The videofluorographic swallowing study: Phys Med Rehabil Clin N Am, 2008; 19; 769-85
7. Matsuo K, Palmer JB, Video fluoroscopic techniques for the study of oral food processing: Curr Opin Food Sci, 2016; 9; 1-10
8. Zarkada A, Regan J, Inter-rater reliability of the Dysphagia Outcome and Severity Scale (DOSS): Effects of clinical experience, audio-recording and training: Dysphagia, 2018; 33; 329-36
9. O’Neil KH, Purdy M, Falk J, Gallo L, The dysphagia outcome and severity scale: Dysphagia, 1999; 14; 139-45
10. Alfonsi E, Restivo DA, Cosentino G, Botulinum toxin is effective in the management of neurogenic dysphagia. clinical-electrophysiological findings and tips on safety in different neurological disorders: Front Pharmacol, 2017; 8; 80
11. Wirth R, Smoliner C, Jäger M, Guideline clinical nutrition in patients with stroke: Exp Transl Stroke Med, 2013; 5; 14
12. Burgos R, Bretón I, Cereda E, ESPEN guideline clinical nutrition in neurology: Clin Nutr, 2018; 37; 354-96
13. Wright L, Cotter D, Hickson M, Comparison of energy and protein intakes of older people consuming a texture modified diet with a normal hospital diet: J Hum Nutr Diet, 2005; 18; 213-19
14. Foley NC, Martin RE, Salter KL, A review of the relationship between dysphagia and malnutrition following stroke: J Rehabil Med, 2009; 41; 707-13
15. Martin RE, Neuroplasticity and swallowing: Dysphagia, 2009; 24; 218-29
16. Dimitrijevic MM, Dimitrijevic MR, Clinical elements for the neuromuscular stimulation and functional electrical stimulation protocols in the practice of neurorehabilitation: Artif Organs, 2002; 26; 256-59
17. Jostarndt-Fogen K, Puntschart A, Hoppeler H, Fibre-type specific expression of fast and slow essential myosin light chain mRNAs in trained human skeletal muscles: Acta Physiol Scand, 1998; 164; 299-308
18. Sheffler LR, Chae J, Neuromuscular electrical stimulation in neurorehabilitation: Muscle Nerve, 2007; 35; 562-90
19. Rofes L, Arreola V, Martin A, Natural capsaicinoids improve swallow response in older patients with oropharyngeal dysphagia: Gut, 2013; 62; 1280-87
20. Baijens LW, Clavé P, Cras P, European Society for Swallowing Disorders-European Union Geriatric Medicine Society white paper: Oropharyngeal dysphagia as a geriatric syndrome: Clin Interv Aging, 2016; 11; 1403-28
21. Wu S, Chu L, Liu CF, Effect of changes in bolus viscosity on swallowing muscles in patients with dysphagia after stroke: Chin Med J (Engl), 2018; 131; 2868-70
22. Balou M, Herzberg EG, Kamelhar D, An intensive swallowing exercise protocol for improving swallowing physiology in older adults with radiographically confirmed dysphagia: Clin Interv Aging, 2019; 14; 283-88
23. Hammer MJ, Jones CA, Mielens JD, Evaluating the tongue-hold maneuver using high-resolution manometry and electromyography: Dysphagia, 2014; 29; 564-70
24. Simonelli M, Ruoppolo G, Iosa M, 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; 103-10
25. Jenks J, Pitts LL, Effects of an intensive exercise-based swallowing program for persons with Parkinson’s Disease and complex medical history: A single-case experiment: Am J Speech Lang Pathol, 2019; 28; 1268-74
24. Bütefisch CM, Khurana V, Kopylev L, Enhancing encoding of a motor memory in the primary motor cortex by cortical stimulation: J Neurophysiol, 2004; 91; 2110-16
25. Kim YH, You SH, Ko MH, Repetitive transcranial magnetic stimulation-induced corticomotor excitability and associated motor skill acquisition in chronic stroke: Stroke, 2006; 37; 1471-76
26. Saigusa H, Niimi S, Yagi T“Direct” indirect training approach to rehabilitation of dysphagia patients – a new method for rehabilitation with a feeding-tube: Nihon Jibiinkoka Gakkai Kaiho, 1998; 101; 1012-21 [in Japanese]
27. Vaiman M, Eviatar E, Surface electromyography as a screening method for evaluation of dysphagia and odynophagia: Head Face Med, 2009; 5; 9
28. Ichikawa M, Oishi S, Mochizuki K, Influence of body position during Heimlich maneuver to relieve supralaryngeal obstruction: A manikin study: Acute Med Surg, 2017; 4; 418-25
29. Li Y, Song B, Fang H, External validation of the A2DS2 score to predict stroke-associated pneumonia in a Chinese population: A prospective cohort study: PLoS One, 2014; 9; e109665
30. Lake DA, Neuromuscular electrical stimulation. An overview and its application in the treatment of sports injuries: Sports Med, 1992; 13; 320-36
31. Wakabayashi H, Matsushima M, Momosaki R, The effects of resistance training of swallowing muscles on dysphagia in older people: A cluster, randomized, controlled trial: Nutrition, 2018; 48; 111-16
32. Ko KR, Park HJ, Hyun JK, 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; 600-10
33. Michou E, Mistry S, Jefferson S, Characterizing the mechanisms of central and peripheral forms of neurostimulation in chronic dysphagic stroke patients: Brain Stimul, 2014; 7; 66-73
34. Calabro RS, Nibali VC, Naro A, Is non-invasive neuromuscular electrical stimulation effective in severe chronic neurogenic dysphagia? Report on a post-traumatic brain injury patient: Neurorehabilitation, 2016; 38; 53-57
35. Park JW, Oh JC, Lee HJ, Effortful swallowing training coupled with electrical stimulation leads to an increase in hyoid elevation during swallowing: Dysphagia, 2009; 24; 296-301
36. Rofes L, Arreola V, López I, Effect of surface sensory and motor electrical stimulation on chronic poststroke oropharyngeal dysfunction: Neurogastroenterol Motil, 2013; 25; 701-888
37. Paine PA, Hamdy S, Chitnis X, Modulation of activity in swallowing motor cortex following esophageal acidification: A functional magnetic resonance imaging study: Dysphagia, 2008; 23; 146-54
38. Shaw GY, Sechtem PR, Searl J, Transcutaneous neuromuscular electrical stimulation (VitalStim) curative therapy for severe dysphagia: Myth or reality?: Ann Otol Rhinol Laryngol, 2007; 116; 36-44
39. Hamdy S, Rothwell JC, Aziz Q, Long-term reorganization of human motor cortex driven by short-term sensory stimulation: Nat Neurosci, 1998; 1; 64-68
40. Steele CM, Miller AJ, Sensory input pathways and mechanisms in swallowing: A review: Dysphagia, 2010; 25; 323-33
41. Mulheren RW, Ludlow CL, Vibration over the larynx increases swallowing and cortical activation for swallowing: J Neurophysiol, 2017; 118; 1698-708
42. Wakabayashi H, Matsushima M, Momosaki R, The effects of resistance training of swallowing muscles on dysphagia in older people: A cluster, randomized, controlled trial: Nutrition, 2018; 48; 111-16
43. Biyouki F, Laimi K, Rahati S, Morphology of muscular function in chronic tension-type headache: A pilot study: Acta Neurol Belg, 2016; 116; 317-24
44. Carnaby-Mann GD, Crary MA, McNeill dysphagia therapy program: A case-control study: Arch Phys Med Rehabil, 2010; 91; 743-49
45. Langdon PC, Lee AH, Binns CW, High incidence of respiratory infections in ‘nil by mouth’ tube-fed acute ischemic stroke patients: Neuroepidemiology, 2009; 32; 107-13
46. Huang GQ, Lin YT, Wu YM, Individualized prediction of stroke-associated pneumonia for patients with acute ischemic stroke: Clin Interv Aging, 2019; 14; 1951-62
47. Rofes L, Arreola V, Mukherjee R, Sensitivity and specificity of the Eating Assessment Tool and the Volume-Viscosity Swallow Test for clinical evaluation of oropharyngeal dysphagia: Neurogastroenterol Motil, 2014; 26; 1256-65
48. Kuhlemeier KV, Palmer JB, Rosenberg D, Effect of liquid bolus consistency and delivery method on aspiration and pharyngeal retention in dysphagia patients: Dysphagia, 2001; 16; 119-22
49. Young A, The relative isometric strength of type I and type II muscle fibres in the human quadriceps: Clin Physiol, 1984; 4; 23-32
50. Sun SF, Hsu CW, Lin HS, Combined Neuromuscular Electrical Stimulation (NMES) with Fiberoptic Endoscopic Evaluation of Swallowing (FEES) and traditional swallowing rehabilitation in the treatment of stroke-related: Dysphagia, 2013; 28; 557-66
51. Stevens-Lapsley JE, Balter JE, Wolfe P, Relationship between intensity of quadriceps muscle neuromuscular electrical stimulation and strength recovery after total knee arthroplasty: Phys Ther, 2012; 92; 1187-96
52. Kletzien H, Russell JA, Leverson G, Effect of neuromuscular electrical stimulation frequency on muscles of the tongue: Muscle Nerve, 2018; 58; 441-48
26 January 2023 : EditorialEditorial: The XBB.1.5 (‘Kraken’) Subvariant of Omicron SARS-CoV-2 and its Rapid Global Spread
Med Sci Monit In Press; DOI: 10.12659/MSM.939580
19 January 2023 : Clinical ResearchEvaluation of Health-Related Quality of Life and Mental Health in 729 Medical Students in Indonesia During ...
Med Sci Monit In Press; DOI: 10.12659/MSM.938892
19 January 2023 : Clinical ResearchDetermining the Impact of the COVID-19 Pandemic on Dental Care in the Serbian Adult Population: An Online Q...
Med Sci Monit 2023; 29:e939238
30 Jan 2023 : Clinical ResearchSplenic Artery Steal Syndrome in Patients with Liver Cirrhosis: A Retrospective Clinical Study
Med Sci Monit In Press; DOI: 10.12659/MSM.938998
27 Jan 2023 : Database AnalysisAssociation Between Neutrophil-Lymphocyte Ratio and All-Cause Mortality in Critically Ill Patients with Chr...
Med Sci Monit In Press; DOI: 10.12659/MSM.938554
27 Jan 2023 : Clinical ResearchProposal for a Simple Equation for Limb Muscle Weight Calculation
Med Sci Monit In Press; DOI: 10.12659/MSM.938606
Most Viewed Current Articles
13 Nov 2021 : Clinical ResearchAcceptance of COVID-19 Vaccination and Its Associated Factors Among Cancer Patients Attending the Oncology ...
Med Sci Monit 2021; 27:e932788
30 Dec 2021 : Clinical ResearchRetrospective Study of Outcomes and Hospitalization Rates of Patients in Italy with a Confirmed Diagnosis o...
Med Sci Monit 2021; 27:e935379
08 Mar 2022 : Review articleA Review of the Potential Roles of Antioxidant and Anti-Inflammatory Pharmacological Approaches for the Man...
Med Sci Monit 2022; 28:e936292