The effect of sensory level electrical stimulation of the masseter muscle in early stroke patients with dysphagia: A randomized controlled study
Correspondence Address: Source of Support: None, Conflict of Interest: None DOI: 10.4103/neuroindia.NI_377_16
Source of Support: None, Conflict of Interest: None
Keywords: Dysphagia, masseter muscle, sensory-level electrical stimulation, stroke
Swallowing is a sensorimotor behavior controlled by numerous components that range from the central nervous system to oesophagus, and provides the passage of food from the mouth to the stomach. The term 'dsyphagia' defines all the challenges that occur in the process during the transportation of food from the mouth to the stomach.
Dysphagia is a serious cause of morbidity and mortality in stroke patients. After stroke, an apparent dysphagia was detected in 29–81% of the patients, especially during the first 3 weeks, and swallowing abnormalities in the form of slight dysphagia was noted in almost every patient., Post-stroke dysphagia increases the risk of dehydration, malnutrition, pulmonary complications, and the length of hospital stay, all of which lead to a poor functional recovery. In addition, aspiration pneumonia occurs in 43–70% of patients with post-stroke dysphagia, with a mortality rate of up to 45%. In 70% of stroke patients, pneumonia that is apparent within 72 hours of admission is almost always associated with swallowing problems. In 75% of these patients with early swallowing problems, dysphagia continues to be moderate-to-severe, and requires alternative nutritional support for up to 6 months.
Therefore, an early diagnosis and intervention for post-stroke dysphagia are critical and recommended to prevent stroke-associated pneumonia. Preventing pneumonia with an early treatment of dysphagia could have a significant impact on morbidity, mortality, length of hospital stay, functional recovery, and costs. The evaluation and management of the swallowing disorder is recommended as soon as possible in stroke patients according to the recently published guidelines.
Posture and dietary modifications, oral motor exercises to strengthen oropharyngeal muscles, maneuvers of the head and neck to facilitate swallowing, and thermal and tactile stimulation to increase sensory input are the traditional treatment methods. These treatment methods are widely accepted in clinical practice, but evidence supporting their effectiveness in dysphagia is limited.
Therefore, there is great interest in the use of electrical stimulation for patients with dysphagia. Studies have reported that electrical stimulation may play a role in the partial/complete recovery of the impaired muscle function involved in swallowing and in the functional recovery of the affected hemisphere by the restoration mechanism. Moreover, it may facilitate cerebral reorganization as a result of stimulation of the central swallowing centers in the unaffected hemisphere by compensation mechanisms. These studies were performed mostly on chronic stroke patients by using different dysphagia assessment parameters. Electrical stimulation was applied alone or as a combination therapy with different intensities, frequency, and duration for various muscles strengthening procedures without standardization.,, Electrical stimulation can also be applied at the sensory level in dysphagia treatment.
In a study comparing the motor and sensory-level electrical stimulation (SES), it has been reported that the effect of motor-level stimulation was to induce muscular contraction applied to increase muscle activity. On the other hand, the effect of SES was to stimulate the peripheral sensory system to increase the afferent drive and promote cortical plasticity. In addition, SES has been reported to be essential for the initiation and progression of swallowing, for maintaining of neural processes, and for stimulating a cortical reorganization.
The pharyngeal phase was of particular importance in these studies and the motor-level electrical stimulation of suprahyoid and infrahyoid muscles were used to increase muscle activity. However, it has been reported that both the oral and pharyngeal stages of swallowing are impaired, especially in early stroke patients., Therefore, electrical stimulation of the masseter muscle, involved in both the oral and pharyngeal phase, may seem to be more appropriate for the treatment of dysphagia in these patients.
In previous studies, the clinical and electrophysiological examination revealed that the oral phase of swallowing is relatively more affected than the pharyngeal phase, especially in early stage stroke patients with cortical involvement., Masseter muscle, which is easily accessable, assists the pharyngeal phase muscles that are mainly active in hyolaryngeal elevation; and, its activity starts at the beginning of the oral phase and continues until the end of swallowing.
Although there are no studies evaluating the effects of motor-level electrical stimulation of the masseter muscle for the treatment of dysphagia in the literature, in studies evaluating masseter muscle activity, there is some evidence that the motor-level electrical stimulation leading to recurrent masseter muscle contraction may result in effects such as tooth destruction and fracture, jaw pain, temporomandibular dysfunction, and headache.,
In the literature, it has been reported that the sensory-level stimulation of muscles other than the masseter muscle for dysphagia treatment is well-tolerated and can be administered at home without complications.
In the light of this information, this is the first study in literature that aimed to evaluate the effects of SES to bilateral masseter muscles in early stroke patients with dysphagia.
This study was conducted at the Physical Medicine and Rehabilitation (PMR) and Otolaryngology-Head and Neck Surgery Clinics of our hospital between 2013 and 2015. Patients were hospitalized in the PMR clinic and all tests were conducted in the clinic.
The inclusion criteria were the following: patients aged between 45 and 75 years, who were admitted for any problem such as motor function impairment or disability, within the first month after ischemic stroke confirmed by magnetic resonance imaging (MRI). The diagnosis of dysphagia was obtained by evaluation of swallowing.
Patients with a history of malignancy, head and/or neck surgery, previous stroke, known pulmonary or swallowing disorder, gastroesophageal reflux disease, dementia or psychiatric disorder, hemorrhagic infarction, bilateral involvement, and smoking, were excluded from the study. In addition, the exclusion criteria for flexible fiberoptic endoscopic evaluation of swallowing (FEES) method were the presence of contagious or infectious diseases such as human immunodeficiency virus (HIV) and hepatitis types B and C; the risk of bleeding; the presence of nasal obstruction; and, the presence of decompensated heart disease. The exclusion criteria for electrical stimulation were the presence of biomedical devices such as a cardiac pacemaker sensitive to electrical field in the body; and, the presence of serious infectious diseases similar to pneumonia.
Ninety-eight patients were included in this study. The patients and their relatives (at least one person) were informed about the study, and their written consents were obtained at the beginning of the study. The approval of the Ethical Board of the hospital was obtained, and the study was conducted in accordance with the principles of the Helsinki Declaration.
The characteristics of 98 patients including their age, gender, educational status, hand dominancy, comorbidities, additive problems associated with swallowing, the infarct region, and the elapsed time after stroke were recorded.
Their educational status was noted according to the Turkish educational system as “illiterate,” “under 5-years,” “5-years,” “8-years,” “11-years,” and “more than 11 years” of education.
The stroke severity was assessed by National Institute of Health Stroke Scale (NIHSS). In this scale, patients were evaluated in 11 categories including consciousness, language, dysarthria, eye movements, visual field, negligence, facial paresis, proximal limb strength, extremity ataxia, and feeling. Each category was scored between 0–2 and 0–4. The total score was between 0 and 42. Motor functional status was graded from 1 to 6 using the Brunnstrom stage for upper extremity, hand, and lower extremity.
Assessment of swallowing function
The swallowing screen test, which is routinely used in our clinic, included the neurologic examination as well as the water swallowing test (by using 10 ml water, together with O2 saturation evaluation, conducted with the pulse oximetry method, using the second finger of the unaffected hand).
The neurological status of patients was evaluated by examining several functions including head control, sitting balance, facial paralysis, gag and pharyngeal reflexes, as well as palatal and tongue movements. The Neurological Examination Dysphagia Score (NEDS) was calculated and recorded as follows: presence of head control, sitting balance, and gag and pharyngeal reflexes = 0, absence of all = 1; absence of facial paralysis = 0, its presence = 1; normal palatal movement = 0, asymmetric palatal movement = 1, absence of palatal movement = 2; and, weak tongue protrusion = 1, weak tongue lateral movement = 2. Based on the above NEDS calculations, a score of 0–3 was considered as “normal swallowing,” and a score of 4–9 as “dysphagia.”
In water swallowing test, observations and recordings were made in terms of drinking the water in one gulp or by splitting in volumes; coughing/wet voice/water flow from the mouth and presence of laryngeal elevation during or after water swallowing; and decreases in O2 saturation by 2% and more. Each of the listed disorders was assigned one point to calculate the Bedside Dysphagia Score (BDS). The score of 0–2 was considered to be “normal swallowing” and between 3 and 6 as “dysphagia.”
Total Dysphagia Score (TDS) was obtained by summing the scores individually for BDS and NEDS, according to which “normal patients” had a total score of 0–3, whereas scores of 4–15 indicated “dysphagia.”
Mann assessment swallowing ability test
Swallowing evaluation was done with the Mann Assessment of Swallowing Ability (MASA). Twenty-four areas were evaluated as follows: alertness, cooperation, auditory comprehension, aphasia, apraxia, dysarthria, respiratory status, respiratory rate during swallowing, saliva swallowing, lip seal, tongue movement, strength and coordination of swallowing, oral preparation, palate and gag reflexes, bolus clearance, oral transit, cough reflex, voluntary cough, voice intensity, presence or requirement of tracheostomy, pharyngeal phase of swallowing, and pharyngeal response to swallowing. The scoring was done by a physiatrist and the scale ranged from 38 to 200 points.
Flexible fiberoptic endoscopic evaluation of swallowing
The test was performed by the same otolaryngology specialist using a nonducted fiberoptic nasopharyngoscope of 3.4 mm diameter, a light source, camera, monitor, and a digital video recorder (Karl Storz GmbH and Co KG, Tuttlingen, Germany). All evaluations were performed in the sitting position or an upright position, to the extent possible. No local anesthetic agent was used to avoid its effects on palatal and pharyngeal functions. Before the procedure, a lubricant gel was applied on the distal tip of the nasopharyngoscope and an antifog agent was applied on the lens. The tip of the nasopharyngoscope was inserted from the nostril, and the general pharyngeal phase was evaluated. In order to evaluate penetration and aspiration of food, and the presence of a residue, 10 ml water was used as the liquid, 10 ml of yoghurt as the semisolid, and a matchbox-sized biscuit as the solid food. Findings were recorded as video images. At the end of the examination, dysphagia level was scored from 1 to 6, according to the protocol of the endoscopic assessment of dysphagia developed by Dziewas et al. Accordingly, 1 point was considered as “normal swallowing” whereas 2–6 points were considered as “dysphagia.”
The phase of swallowing disorders (i.e., oral or pharyngeal phase disorder) were analyzed and recorded, according to results of bedside screening tests and FEES.
Assessment of functional disability
The functional disability status was assessed using the functional independence measure (FIM). The functional independence measure analyzed two different aspects of disability as motor and cognitive functions. There were 18 questions and 6 sections including self-care, sphincter control, transfers, locomotion, communication, and social cognition, with each item being scored from 1 to 7.
Study evaluation protocol
The study was performed by a group of independent experts blinded to treatment allocation. The bedside screening tests and FIM assessment were performed by the same PMR specialist (designated as the first specialist) on the day of hospital admission (1st day). Afterwards, the patients underwent endoscopic evaluation by an otolaryngology specialist blinded to physical examination findings and the the patient was referred to another PMR specialist (designated as the second specialist).
The patients were randomly allocated by block randomization, and a table of random numbers was prepared by the second PMR specialist. According to the table, patients were divided into two groups that were designated as the stimulation (group 1) and the sham (group 2) groups. After 4 weeks of treatment (on the 29th day), the initial assessment performed by the 1st PMR specialist and the otolaryngology specialists were repeated as evaluation tests.
The method for randomization was applied to all patients who were hospitalized and eligible for the study criteria between 2013 and 2015. According to the order of hospitalization, patients were numbered and grouped as 1.,4.,5.,8… for group 1, and 2.,3.,6.,7. for group 2 by using double block randomization table. Twenty-three patients from group 2, and 10 patients from group 1, were excluded after randomization because of protocol violations. These included those who were transferred to other clinics because of some medical problems (19 patients), those who were unable to continue the study due to living in different cities (10 patients); and, those who were unadapted to the rehabilitation process (4 patients).
All patients under the supervision of the same physiotherapist received daily care for oral hygiene, thermal (cold) and tactile stimulation, swallowing maneuvers, head and trunk positioning, dietary modification, and oral motor exercises including lips, tongue, and jaw movements. This was in accordance with the different patient swallowing characteristics and were given for 60 minutes a day, 5 days a week, for 4 weeks; cognitive, respiratory, and sensorimotor functional rehabilitation programs were added to this program.
Apart from this traditional treatment, the patients in group 1 received intermittent galvanic stimulation to bilateral masseter muscles for 60 minutes a day, 5 days per week, for 4 weeks up to a total of 20 sessions (Intelect Advanced- Chattonooga, UK). In this method, after the patients were positioned in 90° supported/unsupported seating, 2 pieces of 4 × 5 cm surface electrodes were placed, one over the ramus of the mandible, and another over the masseter muscle (the chin being in the intercuspal position and in the midline).
The current stimulation intensity was established by determining the threshold sensibility using an incremental protocol and fixed during the treatment session. The sensory approach, i.e., the sensory threshold, was identified as the lowest current level at which the patient felt a tingling sensation on the skin. The amplitude of the electrical current level was approximately 4–6 mA. Patients were not instructed to perform any oropharyngeal exercises or swallowing training during the electrical stimulation treatment.
Patients in group 2 received sham stimulation, the electrodes were placed at the same positions as in active stimulation; however, the stimulator was turned off. Therefore, the patients received no current stimulation for the treatment period.
The dysphagia severity, determined by FEES and NEDS, BDS, total swallowing, and MASA scores, as well as FIM scores, were reassessed after treatment. In addition, the intensity of discomfort during the electrical stimulation was evaluated using a 0–100 mm visual analog scale (VAS). The responses to treatments and changes between the groups were compared.
Statistical analysis was performed using the Statistical Package for the Social Sciences version 15.0 (SPSS, Inc.; Chicago, IL, USA) for Windows. Normality of the continuous variables was assessed by the Shapiro–Wilk test. Descriptive statistics were shown as mean ± standard deviation for continuous variables and frequencies and percentages (%) for nominal variables. Statistically significant differences in repeated measurements within the groups were evaluated with the Friedman test and Wilcoxon signed rank test. The Bonferroni correction was used to control possible type I errors in intragroup comparisons (P < 0.025). As none of the continuous variables were normally distributed, the Mann–Whitney U test was used for the comparison of non-normally distributed continuous variables. On the other hand, the significance of difference for nominal variables was analyzed using Fisher exact test. The results were considered significant ifthe P value < 0.05.
The average age of the 98 patients [22 (22.4%) female, 76 (77.6%) male patients) included in the study was 61.59 ± 9.97 years, and the mean elapsed time after stroke was 14.52 ± 5.53 days. The mean NIHSS score of patients was 9.62 ± 4.05. The demographic and disease characteristics of patients according to the groups are presented in [Table 1]. The two groups were similar in demographics and disease characteristics (P > 0.05).
The means of BDS, NEDS, TDS, and MASA scores of the patients before treatment were 5.71 ± 1.44, 6.35 ± 1.74, 10.03 ± 2.62, and 142.41 ± 27.53, respectively. The mean of dysphagia level determined by FEES was 3.75 ± 1.22, and there was no patient, assessed at level 1, being designated as normal.
The mean FIM motor functional status, cognitive function score, and the total disability score of patients were 33.15 ± 21.30, 20.42 ± 10.12, and 53.06 ± 27.33, respectively. The distribution and comparison of pretreatment evaluation parameters between the groups are shown in [Table 2]. There were no differences in the evaluation parameters between the groups (P > 0.05).
The oral phase of swallowing was impaired in the majority of patients (n = 96, 98%, group 1: n = 58, group 2: n = 38). Forty-four (44.9%, group 1: n = 23, group 2: n = 21) patients had an impairment of swallowing during the pharyngeal phase.
The comparison of the pre- and posttreatment measurements according to the groups are shown in [Table 3].
There was a significant improvement in all parameters, except for the motor FIM score in the stimulation group (group 1; P< 0.025). In group 2, there were no significant changes in the evaluation parameters (P > 0.025).
The average discomfort during the electrical stimulation was 10.15 ± 5.88, and was 10.05 ± 6.45 in group 1 and 12.10 ± 5.77 in group 2. There was no significant difference between the groups (P = 0.902). The comparison of the pre- and post treatment changes between the groups are presented in [Table 4].
Pre- and post-treatment changes, including swallowing evaluation methods and cognitive and total functional independence scores, were significantly improved in the stimulation group (P < 0.025). There was no significant difference in the motor functional independence levels between the groups (P = 0.131).
After the treatment, 38 (38.8%) patients suffered from oral phase disorder (group 1:n = 7, group 2:n = 31) and 21 (21.4%) from pharyngeal phase disorder (group 1:n = 8, group 2:n = 13).
In our study, there was a significant improvement in the dysphagia severity scores, evaluated by bedside screen tests and FEES in cognitive and total functionality levels (except for motor functional independence level), in the stimulation group. In the sham group, there were no significant changes in the evaluation parameters. There was no difference between the groups in terms of discomfort felt by the patients during the course of the treatment.
Functional treatment of dysphagia is based on restoration, compensation, and adaptation mechanisms. Electrical stimulation may play a role in the partial/complete recovery of impaired muscle function involved in the act of swallowing as well as in the functional recovery of the affected hemisphere by restoration mechanism, provided that reorganization occurs as a result of stimulation of the central swallowing centers in the unaffected hemisphere by compensation mechanisms.
In previous studies evaluating the effectiveness of electrical stimulation in stroke patients with dysphagia, increasing the muscle activity, as a primary effect of stimulation, was of particular importance. In these studies, stimulation of suprahyoid and infrahyoid muscles, which are active during the pharyngeal phase, were preferred. They helped in improving the hyolaryngeal elevation, thus preventing aspiration, one of the most important consequences of dysphagia.,,,,,,
Electrical stimulation has been shown to be effective primarily in chronic stroke patients with dysphagia in uncontrolled studies, when applying electrical stimulation alone at different intensities. The suprahyoid and infrahyoid muscles were stimulated using a broad range of therapy sessions, from 3 to 40, using videofloroscopy (VF) and FEES as aspiration parameters, as in this study. Alternative nutritional method usage and dietary modifications were also evaluated., However, in some of the comparison studies, it has been reported that traditional therapies such as thermal tactile stimulation and modifications, as well as electrical stimulation were both equally effective, and there was no difference between the methods;,,, whereas, other studies claimed that these methods were not effective when performed alone. In the recent years, a majority of studies have proposed that a combination of therapies is more effective than monotherapy.,,,
Therefore, we preferred to study the combination therapy, that included the traditional methods as well as electrical stimulation, and evaluated patients by the penetration/aspiration scale of FEES that is easily applicable at the bedside to objectively measure the effectiveness of therapy. As a result, we found that the combination therapy is more effective than the traditional method.
The above mentioned studies were mostly performed during the chronic phase dysphagia in stroke patients with predominant aspiration signs. It is reasonable to think that the therapy for pharyngeal phase muscles is effective in chronic stroke patients.A thereputic benefit may be obtained despite of disuse atrophy of these muscles.
However, some of the previous studies reported that, regardless of the pharyngeal phase disorder, the oral phase disorder was also found up to 97% patients, especially in early stroke patients.,, Moreover, studies have reported that, in order to ensure a sufficient control of swallowing, swallowing therapies for the oral phase are essential for the initiation and continuation of swallowing, as well as for maintenance of the neural processes.,
The masseter muscle was selected for electrical stimulation in our study. Although there are many oral phase muscles, such as the orbicularis oris and tongue muscles, that play a very significant role in preparing and transferring the bolus, the masseter muscle is a large muscle which is easily accessible. Thus, a surface electrode may be easily applied to it. Its stimulation does not require any additional patient positioning or cooperation. There is no discomfort while performing the procedure, such as opening the mouth.,
Despite the fact that masseter muscle is considered as a chewing muscle that is affected in the oral phase, it also has an important action during swallowing. The activity of the masseter muscle starts at the beginning of the oral phase; then it assists the pharyngeal phase muscles that are mainly active in hyolaryngeal elevation; and, its activity continues until the end of swallowing. In other words, it has an activity during both the oral and pharyngeal phases. Moreover, without the activity of the masseter muscle, insufficient supra- and infrahyoid muscles activity and prolonged swallowing time have been reported in trials evaluating the activity of the swallowing muscles.,
These results support our decision in the masseteric muscle selection for electrical stimulation. Thus, the stimulation of masseter muscle, which is active both in the oral and pharyngeal phase, is more effective than targeting the pharyngeal phase muscles only.
The above mentioned studies also preferred motor-level stimulation due to the inclusion of patients with chronic stroke. In studies including the early stroke patients, as was done in our study, both the combination therapy (the traditional method and motor-level electrical stimulation) and only motor-level electrical stimulation to pharyngeal phase muscles were compared; these studies reported an improvement in dysphagia severity within 15 to 18 total therapy sessions.,
Although, no study has reported a method similar to our work in the literature, in studies using SES, 5 to 72 session of SES (alone or in combination) of supra- and infrahyoid muscles, evaluated by VF/FEES, have been shown to be effective in decreasing the dysphagia level and aspiration frequency in chronic stroke patients, with no adverse events.,, These studies, having results similar to our study, indicated the efficacy of both motor and SES stimulation in the treatment of dysphagia.
The studies evaluating the motor activity of the masseter muscle demonstrated tooth destruction, jaw pain, temporomandibular dysfunction, and headache due to repetitive masseter muscle contractions., It has been reported that the anatomical relationship between the masseter muscle and mandible, teeth, and temporomandibular joint may lead to such findings. Therefore, in our study we chose the stimulation of masseter muscle on the sensory-level rather than the motor-level.
Other studies revealed that the SES can also increase muscle activity, and can also enhance sensory input to swallowing center by stimulating muscle proprioceptors, affecting the initiation of swallowing and in improving the swallowing function that occurs after cortical reorganization.,, In two recent reviews, evaluating both the motor and sensory-level stimulation studies, it was proposed that the effect of motor-level stimulation may be secondary to the sensory input increase.,
In this study, similar to the results published in literature, there was a significant improvement of dysphagia in the SES plus traditional therapy group compared to soley the traditional group, and there was no significant difference related to the discomfort level during therapy between the two groups. In addition, no adverse events were observed due to the masseter muscle stimulation.
A different aspect of our study was to assess the general cognitive and motor functional disability of patients. Unexpectedly, we found that there was a significant improvement in the cognitive function in the stimulation group, which may indirectly support the idea of cortical reorganization by the sensory inputs.
Although there is no study investigating the association between cognitive function and the stimulation of the masseter muscle, animal studies assessing the effect of sensory stimulation on cognitive function have shown that the neural plasticity induced by growth factors and modulatory neurotransmitters can increase cognitive function. Furthermore, there are also studies indicating that the sensory-level transcutaneous electrical stimulation applied on the hand and foot improved the cognitive functions, such as attention, perception, memory, relearning, and language in patients who have suffered from stroke or brain injury.
Moreover, the areas associated with swallowing function that were activated during the functional magnetic resonance imaging (fMRI) study were the primary sensorimotor cortex, the dorsolateral prefrontal cortex, the insula and frontal operculum, the anterior cingulate cortex, the supplementary motor areas in both hemispheres, and the dorsolateral prefrontal cortex that were related to both swallowing and cognitive functions (e.g., alertness, attention, and memory). Cognitive function can also be represented in bilateral hemispheres as may be the swallowing function, and this may suggest that cortical reorganization may also ocur for cognitive functions following masseteric stimulation.
First, we have planned our work considering the effects of masseter muscle on swallowing, as has been mentioned above. However, there are other branches of sensory nerves in this region of stimulation. We have not conducted an objective electrophysiological evaluation of the masseter muscle. Second, the purpose of our study was to evaluate the effect of the masseter muscle stimulation. We did not use stimulation additionally or alternately on the infrahyoid or suprahyoid muscles. If we had used these applications, the efficiency of the treatment would perhaps have increased. Third, we did not design a fMRI study to evaluate the cortical involvement objectively. In addition, we were unable to quantify the neurological status on a long-term follow-up of our patients. Large-scale, multicentric studies are needed to conclusively validate our results.
Aspiration is one of the most important consequences of dysphagia, increasing the morbidity and mortality associated with it. Aspiration specifically refers to the pharyngeal phase disorders. However, voluntary oral phase is important in terms of initiating and maintining swallowing; moreover, it is often impaired in early stages of stroke.
Therefore, selecting the masseter muscle for electrical stimulation therapy based on its oral and pharyngeal phase functions, and using SES for generation of cortical reorganization may provide an effective treatment for dysphagia in stroke patients. Furthermore, this method can also be helpful in improving the cognitive function of these patients who have suffered from stroke.
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Conflicts of interest
There are no conflicts of interest.
[Table 1], [Table 2], [Table 3], [Table 4]