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INTRODUCTION
Dysphagia is a health problem defined as the difficulty in forming and/or moving the bolus of food safely and effectively from the mouth to the stomach. It occurs in patients with neurodegenerative and oncological diseases and is currently considered a geriatric syndrome . One in five elderly people has swallowing problems. Patients with dysphagia may present multiple complications, causing a major impact on their health, nutritional and functional status, morbidity and quality of life1,2,3,4,5,6.
The suprahyoid muscles (mylohyoid, geniohyoid, digastric and stylohyoid) are considered strategic in ensuring the transit of the food bolus, as they participate in motor mechanisms, reflexes of lowering and stabilizing the mandible, anteriorization and elevation of the hyoid bone and protection of the lower airway. Understanding the action of the muscles during swallowing is essential for making diagnoses and for effective therapeutic conduct7,8,9,10.
Although it is a rare disease, Amyotrophic Lateral Sclerosis (ALS) is the most common type of motor neuron disease11,12, characterized by paresis to paralysis of all muscles in the body13. The progression of the disease leads to dysphagia in practically all people, negatively affecting the quality of life of individuals due to progressive difficulty in oral intake, weight loss, dehydration, malnutrition and limitation of social activities14,15.
Fiberoptic videoendoscopy of swallowing (VED) is one of the tests used to assess swallowing function and is currently considered an established test for identifying dysphagia in children and adults16. It effectively assesses the pharyngeal phase of swallowing, providing information on the anatomy and physiology of the pharynx and larynx, pharyngolaryngeal sensitivity, detection of laryngeal penetration and laryngotracheal aspiration16,17. Its performance in subjects with neurological diseases presents particularities, due to cognition, posture during the examination and the occurrence of fatigue, which may lead to the interruption of the examination16,18.
Since 1965, several studies have reported the importance of surface electromyography (EMG) in evaluating the muscles of the stomatognathic system. This is a non-invasive and painless examination that allows the analysis of electrical activity from muscles, evaluating failures in nerve conduction or impairment of the muscles involved in the swallowing process19,20. EMG devices are non-invasive, radiation-free, and generally low-cost21.
Thus, the objective is to evaluate the association between Surface Electromyography and Videoendoscopy of Swallowing for the diagnosis of dysphagia in subjects with Amyotrophic Lateral Sclerosis.
METHODS
Study design
This is an observational, analytical, cross-sectional study22, in which subjects with Amyotrophic Lateral Sclerosis (ALS) underwent Swallowing Videoendoscopy (VED) and Surface Electromyography (EMG’s) to evaluate the association of these exams for the diagnosis of dysphagia.
Location and period of study
Thirty-two subjects participated in the research: 16 with a defined diagnosis of Amyotrophic Lateral Sclerosis (ALS) by an attending neurologist (Group A) and who were evaluated in their homes distributed in the metropolitan region of Recife, Zona da Mata and Agreste of the state of Pernambuco - Brazil and 16 volunteers without ALS (Group B - control) who underwent examinations in an otorhinolaryngology outpatient clinic from August 17, 2021 to March 12, 2022.
Study population and eligibility criteria
Adult subjects aged between 32 and 80 years were selected and underwent Surface Electromyography (EMG) and Videoendoscopy of Swallowing (VED); matched by sex and age group.
As inclusion criteria, Group A was composed of subjects with ALS, recruited through active search, with the help of the Pró-cura da ELA association in the state of Pernambuco, Brazil. And Group B, control, was composed of subjects without dysphagic symptoms, neurological sequelae or any degenerative pathology.
Candidates for Group A with a previous diagnosis of ALS but unable to perform any of the assessment instruments, portable EMG or VED, were excluded from the study; and volunteers from Group B who differed in at least one of the inclusion criteria described above, as shown in figure 1.
Data collection
In the first stage, the research stages were described to the subjects, with the reading and signing of the free and informed consent form – TCLE.
In the second stage, the subjects underwent VED and portable EMG examinations.
VED is an examination performed with flexible fiber optics through which food in a wide variety of consistencies is offered and, based on the parameters evaluated, the risk of glottic aspiration/bronchoaspiration can be quantified by scores.
In this study, a flexible Machida nasofibroscope was used with the subject in a sitting position, with volumes of 5 and 10ml in a syringe being offered in a pasty or pudding consistency (using the food thickener Resource Thicken Up Clear – Nestlé® brand , dyed with edible aniline in blue) and in liquid consistency, in syringes in volumes of 10, 20 and 100ml (drinking water dyed with edible aniline in blue).
The swallowing assessment protocol was completed and the O’Neil dysphagia severity scale was applied: level 7 = normal swallowing / level 6 = within functional limits / level 5 = mild dysphagia / level 4 = mild/moderate dysphagia / level 3 = moderate dysphagia / level 2 = moderately severe dysphagia / level 1 = severe dysphagia15.
For portable EMG, the Myobox 2+ Kit was used, 2 devices placed on the suprahyoid muscles (digastric , mylohyoid , geniohyoid and stylohyoid) fixed with specific adhesives19. Figure 2 shows the portable EMG devices and their arrangements on the suprahyoid muscles.
Source: author’s collection.
Figure 2 Layout of portable EMG equipment and their placement on the suprahyoid muscles in the neck
Myobox 2+ equipment (neuroUP, Brazil): is a Surface Electromyograph (EMG) with a sampling rate of 1,000Hz and which sends signals to Smartphones or Tablets with the Android or iOS operating system , via Bluetooth 4.0 protocol. The signals are processed through a digital band-pass filter, with cuts at 30Hz and 500Hz, and by a Notch filter, at 60Hz, both of the Butterworth type. These signals are digitally transformed to the Root Mean Square notation. The Myobox 2+ equipment is standardized exam by exam, that is, subject by subject19.
The electrical activity was captured using adhesive electrodes containing conductive gel positioned over the right and left suprahyoid muscles. Before being fixed, the skin was cleaned with gauze soaked in 70% alcohol and lightly abraded with steel wool. The following parameters were used for comparison between groups:
r: rest. Average of the values found in the electromyographs with the subject at rest in the intervals of maximum voluntary contractions.
cvm: Maximum voluntary contraction. Average of the values found in the electromyographs with the subject being stimulated to swallow saliva with maximum voluntary contraction following moments of rest.
R: Ratio between the resting averages multiplied by 100 and the maximum voluntary contraction averages (R= r.100/cvm).
The present study consisted of several stages, from subject recruitment, VED and adaptation of surface electromyographs bilaterally on the suprahyoid muscles to perform EMGs.
Data analysis
From the quantitative data generated through the tools proposed in the study, these data were tabulated in the Microsoft Excel® program and then imported and saved in IBM SPSS Statistics®, version 20, in which descriptive and inferential analyses were performed.
The descriptive analysis data are presented using absolute and relative numbers of the respective variables studied. The inferential analyses were performed using hypothesis tests, respecting the respective assumptions of each test according to the type of variable analyzed. In this research, a significance level (α value) of 5% (p-value < 0.05) was considered, that is, within the hypothesis tests performed, the null hypothesis is rejected when the p -values are less than 0.05, indicating that there is a statistically significant association between the variables tested.
Spearman’s rho test was used to assess correlation between numerical variables. Resting Maximum Voluntary Contraction Ratio (EMG’s) and the O’Neil Swallowing Scale (VED), since both variables presented a non-parametric distribution of data, in addition to a small sample size, being a more robust and precise test than Pearson’s correlation in this case20.
Ethical and legal aspects of research
The authors declare no potential conflicts of interest with respect to the research, authorship, and/or publication of this article. This study followed the guidelines for research involving human subjects in Resolution 466/12 of the National Health Council. We obtained approval from the Research Ethics Committee of the ABC School of Medicine, under CAAE: 43887221.2.0000.0082 and Opinion Nº. 4,804,402.
RESULTS
Sixteen subjects diagnosed with Amyotrophic Lateral Sclerosis (ALS) participated in the study. who were evaluated in their homes distributed in the metropolitan region of Recife, forest and rural areas of the state of Pernambuco – Brazil.
In table 1, it can be seen that most of the subjects in group A had been diagnosed for more than 3 years, needed feeding via gastrostomy (GTT) and caregivers, and had difficulty moving and speaking. When compared, groups A and B showed statistically significant differences for these variables (p <0.01).
Table 1 Social and pathophysiological characteristics of subjects in groups A (ALS) and B (control), in the state of Pernambuco, Brazil, from August 2021 to March 2022
| Variables | Group A n; proportion % (95%CI) | Group B n; proportion % (95%CI) | p-value (OR/95%CI) |
|---|---|---|---|
| Sex | |||
| Masculine | 8; 25% (0.26-0.73) | 8; 25% (0.26-0.73) | 1.00/0.25-3.9 |
| Feminine | 8; 25% (0.26-0.73) | 8; 25% (0.26-0.73) | ≥0.05 |
| Age | |||
| 30-44 | 2; 6.2% (0.22-0.33) | 2; 6.2% (0.22-0.33) | - |
| 45-59 | 8; 25% (0.26-0.73) | 8; 25% (0.26-0.73) | >0.05 |
| 60 years and over | 6; 18.8% (0.17-0.61) | 6; 18.8% (0.17-0.61) | |
| ALS time | |||
| 0 to < 1 year | 1; 3.1% (0.004-0.24) | 16; 50% (0.88-1.00) | |
| From 1 year to < 2 years | 1; 3.1% (0.004-0.24) | 0; 0% (0.00-0.11) | - |
| From 2 years to <3 years | 3; 9.4% (0.05-0.41) | 0; 0% (0.00-0.11) | < 0.01 |
| 3 years or older | 11; 34.4% (0.44-0.87) | 0; 0% (0.00-0.11) | |
| Via GTT Feeding | |||
| Alternative | |||
| Yes | 9; 28.1% (0.32-0.78) | 0; 0% (0.0-0.11) | 3.28 /1.77-6.09 |
| No | 7; 21.9% (0.21-0.67) | 16; 50% (0.88-1.00) | <0.01 |
| Need a caregiver | |||
| Familiar | 13; 40.6% (0.58-0.95) | 0; 0% (0.0-0.11) | - |
| Third | 3; 9.4% (0.05-0.41) | 0; 0% (0.0-0.11) | <0.01 |
| No | 0; 0% (0.00-0.11) | 16; 50% (0.88-1.00) | |
| Difficulty moving | |||
| Yes | 13; 40.6% (0.58-0.95) | 0; 0% (0.0-0.11) | 6.33/ 2.24-17.89 |
| No | 3; 9.4% (0.05-0.41) | 16; 50% (0.88-1.00) | <0.01 |
| Speech difficulty | |||
| Yes | 14; 43.8% (0.66-0.97) | 0; 0% (0.0-0.11) | <0.01 |
| No | 2; 6.2% (0.22-0.33) | 16; 50% (0.88-1.00) | 9.0/ 2.43-33.24 |
Regarding the values of the O’Neil swallowing scale (VED parameter), it was observed that subjects in group A presented lower scores/greater dysphagic changes with an average of 4.12 (mild/moderate dysphagia) when compared with subjects in group B with the same age and sex who obtained an average of 7 (normal swallowing) (figure 3).
Figure 3 Graph showing the difference in O’Neil Swallowing Scale values between Groups A (ALS) and B (control), in the state of Pernambuco, Brazil, from August 2021 to March 2022
The values of the measures of central tendency and dispersion of the two exams were calculated:
For VED, we obtained the following values: Group A, median: 3.5 (2:7) and group B, median: 7, with p -value : 0.0002.
DISCUSSION
In the present study, carried out in the state of Pernambuco, Brazil, from August 2021 to March 2022, we found an association between Videoendoscopy of Swallowing (VED) and Surface Electromyography (EMG’s) for the diagnosis of dysphagia in subjects living with Amyotrophic Lateral Sclerosis (ALS).
Table 1 presents the social and pathophysiological characteristics of the study subjects, in which the participants are matched by sex and age, therefore, showing no statistically significant differences between groups A and B for these variables (p = 1.00). This concern was necessary because this was a study that evaluated the functionality of the suprahyoid muscles.
It was observed that most of the subjects in group A had been diagnosed for more than 3 years, needed feeding via gastrostomy (GTT) and needed caregivers, mainly family members. In addition, they had difficulty moving and speaking. When compared, groups A and B showed statistically significant differences for these variables (p <0.01).
Odds ratio analyses showed that group B was 3.28 times more likely to not use an alternative feeding route (GTT) (95%CI=1.77-6.09), 6.33 times more likely to not have difficulty moving (95%CI=2.24-17.89) and 9 times more likely to not have difficulty speaking (95%CI=2.43- 33.24) when compared with group A (ALS).
For EMG’s, we obtained the following values: Group A, median: 44.5 (32.5:5.8) and group B, median: 15.2 (12.3:20.0), with p-value: 0.0001.
Regarding the surface electromyography parameters (measured by R = r.100/cvm), when comparing the subjects in group A with the subjects in group B, it was observed that there was a statistically significant difference, indicating changes in swallowing (neurogenic dysphagia) in the subjects with higher EMG values.
Spearman correlation analyses were performed to assess the relationship between the variables measured by VED and EMG examinations (p < 0.001).
In the evaluation of VED, using the O’Neil swallowing scale, it was observed that the subjects in group A presented lower scores, indicating greater dysphagic changes , with an average of 4.12 (mild/ moderate dysphagia), compared to the subjects in group B, who obtained an average of 7 (normal swallowing). This demonstrates a greater risk of laryngeal penetration and laryngotracheal aspiration in subjects living with ALS (figure 3)21.
Thus, a statistically significant difference was identified in the values of the O’Neil swallowing scale between Groups A and B (p = 0.001), in which it was observed that the lowest values of the O’Neil swallowing scale were for Group A (ELA) (table 2).
Table 2 Results of tests for differences in levels of neurogenic dysphagia measured by the O’Neil Swallowing Scale (VED) and the Rest to Maximum Voluntary Contraction Ratio (EMG’s) between subjects in the ALS group and the control group, in the state of Pernambuco, Brazil, from August 2021 to March 2022
| Scores | |||||||
|---|---|---|---|---|---|---|---|
| M | DP | p-value | Mean Difference | Mean Difference CI (95%) | |||
| Lower limit | Upper limit | ||||||
| Videoendoscopy of swallowing (O’Neil swallowing scale) | A | 4.12 | 0.00 | 0.001 | -2.87 | -4.17 | -1.62 |
| B | 7.00 | 2.47 | |||||
| Surface electromyography (r.100/cvm) | A | 41.75 | 16.78 | 0.002 | 25.67 | 17.23 | 34.38 |
| B | 16.08 | 5.41 | |||||
M= mean; SD= standard deviation; Df= degrees of freedom; 95% CI= 95% confidence interval.
Regarding the surface electromyography parameters (measured by R = r.100/cvm), when comparing the subjects in group A with the subjects in group B, it was observed that there was a statistically significant difference, indicating changes in swallowing (neurogenic dysphagia) in the subjects with higher EMG values.
In this sense, we can state that there was a statistically significant difference in the values of the Maximum Voluntary Contraction Rest Ratio between Groups A and B (p = 0.002), in which it is observed that the highest values of the Maximum Voluntary Contraction Rest Ratio were for Group A (ELA), as demonstrated in table 2 and figure 4.
Figure 4 Graph showing the difference in the values of the Maximum Voluntary Contraction Rest Ratio between Groups A (ALS) and B (control), in the state of Pernambuco , Brazil, from August 2021 to March 2022
There was also a significant difference in the electromyographic values of the Resting Maximum Voluntary Contraction Ratio between the subjects living with ALS and the subjects in the control group. This finding can be explained by the increase in contracture (spasticity) of the muscles, especially the suprahyoid muscles , of the subjects with ALS at rest. Therefore, since rest and the Resting Maximum Voluntary Contraction Ratio are directly proportional, increasing the resting value results in an increase in the Resting Maximum Voluntary Contraction Ratio.
Spearman correlation analyses were performed to assess the association between variables measured by VED and EMG examinations.
Through the graphical evaluation (figure 5) of the scatter matrix, it was possible to perceive that there was a strong statistical correlation between the Resting Maximum Voluntary Contraction Ratio and the O’Neil Swallowing Scale. The correlation coefficient was r = -0.747, indicating a strong negative correlation (inversely proportional) between these variables21,23. In other words, the higher the value of the Resting Maximum Voluntary Contraction Ratio, the lower the value of the O’Neil Swallowing Scale tended to be.
Figure 5 Scatterplot between the Maximum Voluntary Contraction Rest Ratio versus the O’Neil Swallowing Scale, in the state of Pernambuco, Brazil, from August 2021 to March 2022
In this research, the suprahyoid muscles were used because it is understood that they have an important function in the physiology of swallowing, promoting anteriorization, elevation and laryngeal stabilization, protecting the lower airway from the entry of saliva and/or food, preventing bronchoaspiration, as in the study carried out by Lobo MB et al. (2016)24.
In accordance with our research, Bashford J et al. (2019)25 carried out a systematic review, totaling 42 studies, on surface electromyographic changes in subjects living with ALS. It was observed that EMG’s offer significant practical and analytical flexibility compared to invasive techniques, thus we can assess that its use in our and other studies is a reality still little used in clinical practice and that it can bring many benefits in the prevention, diagnosis and monitoring of subjects with ALS25.
As in this study, Vaiman M et al. (2004) found that EMG is a non-invasive, simple and reliable screening method for assessing swallowing disorders, providing low levels of discomfort for the subject26.
Ramroop H. et al. (2023)27, stated that when the diagnosis of ALS is suspected, electrodiagnostic testing is necessary. This test assesses the integrity of lower motor neurons and is crucial for diagnosing motor neuron disease, as neuroimaging and laboratory studies are often normal. Nerve conduction studies (NCS) and needle electromyography (EMG) are important to support the diagnosis of ALS and rule out other similar diseases. In this study, needle EMG was used, which is more uncomfortable for the individual, when we think of a screening and diagnostic exam27. In our study, we used EMG because we understand that it is a more comfortable exam and with less risk of complications when compared to needle EMG.
In medical investigative practice, both in otorhinolaryngology and in other specialties; having instruments to assess dysphagia early, avoiding respiratory complications, sarcopenia, and even death; is very important.
In this study, EMG was performed and its results compared with those of VED (gold standard in the investigation of dysphagia), verifying that it is a complementary exam that is easy to perform, low cost and with great association with VED. Knowing this, for the evaluation of dysphagia in subjects living with ALS, EMG appears as an alternative, and can be performed on the suprahyoid muscles for a practical, fast and effective diagnosis.
Being an unprecedented work and of important content for the scientific and investigative community, we did not limit ourselves to its execution. For the recruitment and evaluation of subjects with ALS that would be carried out at the Oswaldo Cruz University Hospital, in the state of Pernambuco, Brazil, due to the COVID-19 pandemic, the subjects were recruited, with the support of the PRÓ- CURA association of ALS and evaluated in their homes distributed in the metropolitan region of Recife, forest and agreste zone of the state of Pernambuco - Brazil.
CONCLUSION
Thus, there was an association between Surface Electromyography and Videoendoscopy of Swallowing for the diagnosis of dysphagia in subjects with Amyotrophic Lateral Sclerosis . Portable Surface Electromyography has shown to be an important examination for the early diagnosis of neurogenic dysphagia.
