Introduction: This study compared the submental surface electromyography (sEMG) duration and amplitude during dry swallowing between irradiated head and neck cancer (HNC) survivors and age-matched normal individuals. Further, the relationship between submental and infrahyoid sEMG in the irradiated HNC group was explored. Method: Forty participants (20 HNC survivors and 20 age-matched normal individuals) participated in this study. The HNC survivors had completed organ preservation cancer treatment (at least 1-month post-treatment). They were on a complete oral diet without enteral supplementation (FOIS score> 4). Submental and infrahyoid sEMG activity was calculated for three trials of saliva swallow for each participant using sEMG. The duration and amplitude parameters considered were: onset duration – duration from the onset of swallowing to the maximum amplitude, offset duration – duration from the maximum amplitude to the end of the swallowing activity, total duration, and maximum amplitude. Results: The study found that irradiated HNC survivors exhibited prolonged temporal measures, particularly in the offset duration, which suggested a delayed descent of the hyolaryngeal complex during swallowing. Additionally, the HNC group showed a positive correlation between submental and infrahyoid sEMG. Furthermore, it was observed that the rate of increase in the duration of submental sEMG during subsequent swallowing was greater in HNC survivors which could be due to reduced salivation. Conclusion: Compared to age-matched normal individuals, irradiated HNC survivors manifest alterations in the submental muscle activities during dry swallowing as measured using sEMG. The temporal and amplitude changes are likely to have arisen as a consequence of postradiation changes.

Swallowing, also known as deglutition, is a complex, multistage sensorimotor activity requiring the synchronous participation of several neuromuscular apparatus of the upper aerodigestive tract [1, 2]. It encompasses both voluntary and involuntary mechanisms, mediated by complex but coordinated interactions between cortical centers, brainstem, cranial nerves, pharyngeal mucosal receptors, and muscular activity [1, 2]. Any pathological lesions involving these apparatuses or impairment of the neuromuscular coordination between these apparatuses due to any cause will result in dysfunctional swallowing, also known as dysphagia [1‒3]. Of the several local factors of head and neck that could affect swallowing, radiotherapy to the neck and pharynx, one of the most-widely used non-surgical therapeutic options for head and neck cancer (HNC), can hinder deglutition considerably and thus might affect the quality of life significantly [4, 5]. Despite the latest advancements in conformal radiation delivery techniques, swallowing difficulty continues to be a major issue in radiotherapy recipients for HNC to date [5, 6].

The dysphagia could result from both acute as well as delayed effects of the radiotherapy on the pharyngeal tissues that are directly involved in swallowing function, such as the mucosal lining, receptors, nerve endings, and musculature [4]. In addition, the radiation-induced damage to the salivary glands can also add to the deglutition issues in these patients [4, 7]. Although the post-treatment xerostomia may subside with time, in a significant proportion of the radiotherapy recipients, the salivary dysfunction can continue to deteriorate for several months after the therapy [8]. There also exists a discrepancy between the patient-reported perceptual scores of dysphagia after radiotherapy and the measured objective alterations in swallowing function in the same patients [9‒11]. This weak association between the patient-reported outcomes and objective measurements could be explained by reduced self-awareness of subtle swallowing problems in patients who have non-severe manifestations. Therefore, objective assessment such as surface electromyography (sEMG) may be useful in understanding the muscle physiological changes influencing swallowing skills in patients who have near-normal swallowing skills.

Considering these observations, we evaluated the activity of extrinsic muscles of swallowing in radiotherapy recipients who had near-normal swallowing and compared them with those of normal individuals without any swallowing dysfunction using submental sEMG. We used sEMG measurements of two muscle groups of the neck, the submental and infrahyoid muscles, as their utility in the assessment of oral and oropharyngeal phases of swallowing is already established [12, 13]. We hypothesized the following at the start of the study. First, group-specific differences will exist between the radiotherapy recipients and the normal individuals, for both temporal and amplitude measures of submental sEMG. Second, there will be differences between groups when the rates of change with the three subsequent trials of swallowing are compared. Third, as submental and infrahyoid muscles facilitate the hyolaryngeal excursion, changes in the temporal measures of one muscle group will cause changes in the other.

Participants

Two groups of adult participants were compared in the current study; group A comprised 20 HNC survivors who had completed definitive radiation therapy with curative intent, and group B included an age-matched group of 20 individuals with normal swallowing function and no history of HNC or any other medical conditions.

We used data from two studies conducted independently by our own research groups. From ongoing research on prophylactic swallowing therapy on radiotherapy recipients, we collated the data of a subset of 20 eligible participants (group A), with the specific objective of analyzing swallowing function in these patients who have successfully received radiotherapy. For the comparison (group B), the data set of submental sEMG of dry swallowing of 20 participants was extracted from another recent study (unpublished) that had compared sEMG measures of dry swallowing with Masako maneuver in normal individuals across different age groups. Informed consent was obtained from all the participants.

The HNC survivors were subjected to an assessment of oral food intake using the Functional oral Intake scale (FOIS) [14] and Clinical swallow evaluation using the Mann assessment of Swallowing Abilities-Cancer version (MASA-C) to determine the severity of dysphagia [15]. Patients who had completed at least 1 month after receiving the last dose of radiotherapy and had FOIS scores above four and MASA-C score >170 were only considered eligible to be included under group A.

Normal individuals were screened using the Kannada version of EAT-10 [16]. Individuals with scores less than three and never had any HNC or any comorbidities and no history of dysphagia were included under group B.

sEMG Recording

The recording of sEMG was done using MyoTrac Infiniti Encoder SA9800 (Thought Technology Ltd., Montreal, QC, Canada). Double channel recording targeting submental and infrahyoid sites was done in the HNC survivors group. During recording, each participant was seated on a chair, and the skin over the submental area and neck was prepared using sterile alcohol wipes. Two patches of triode electrodes were placed, respectively, at the submental site (in midline, below the mandible, and above the hyoid) and over the skin of infrahyoid neck (in paramedian plane, below the hyoid and lateral to thyroid cartilage) (shown in Fig. 1).

Fig. 1.

Submental and infrahyoid electrode placement.

Fig. 1.

Submental and infrahyoid electrode placement.

Close modal

Each patch is comprised of two active electrodes and one ground electrode. In both the patches, the positive and negative electrodes were kept toward the midline, and the reference (ground) electrode was positioned laterally. Similarly, while the active electrodes were aligned longitudinally in both patches, the reference electrodes were aligned laterally. These electrodes were attached to the sEMG device MyoTrac Infiniti Encoder SA9800 using a sensor cable, and the signal from the device was registered on a computer using a specialized software called BioGraph Infiniti (Thought Technology, Montreal, QC, Canada). The sEMG recordings of group B participants were limited only to the submental site.

Swallowing Task

For the recording of sEMG for this study, the “Dysphagia Assessment Regular Effort Saliva Swallow” module of BioGraph Infiniti was used. We used “usual saliva swallow,” also known as “saliva swallow,” “normal swallow,” “regular effort swallow,” or “dry swallow” to record the sEMG activity in participants of both groups, wherein the participants were made to swallow the unstimulated residual saliva. Before each recording, a signal verification was done first, following which a mock swallowing trial was given to the participants to make them understand the procedure. Each cycle of swallow was carried out for a 30 s duration. The first 20 s were for the baseline measurements, where the patients were instructed to remain still and breathe quietly, following which they were asked to swallow their saliva whenever they heard the command “Swallow.” For each participant, sEMG was recorded for 90 s, comprising three cycles of dry swallow of 30 s each. The same procedure of recording was carried out for all the participants in both groups.

Signal Processing and Data Analysis

The session data were reviewed after each recording, and a Microsoft Word document containing the values related to the intended target measurements was generated after each session of recording separately. The sEMG waves of each cycle of the swallow task were segmented manually by identifying the points of onset and offset of the deglutition process. The onset (-point) was defined as the first point of upward excursion of the sEMG trace from the resting baseline; the offset (-point) was determined to be the first point where the signal returned to the baseline mark. The parameters measured from the segmented signals of sEMG were the mean durations (seconds) that included onset duration, offset duration, and total duration, and the mean peak amplitude (in microvolt – μV). As depicted in Figure 2, in each sEMG recording of a swallow cycle, the onset point, offset point, and maximum amplitude point were identified first and were used to measure the respective durations of the swallow cycle. The onset duration was measured from the swallow onset to the maximum amplitude point, and the offset duration was taken from the maximum amplitude point to the offset point. The total duration of the swallow was calculated as the time interval in seconds between the onset point and offset point. The maximum amplitude point on the sEMG swallow trace was considered as peak amplitude, and the peak amplitude of each swallow cycle was normalized based on the resting baseline potential. The morphology of the swallow wave (single, double, or multiple peaks) was also commented.

Fig. 2.

Temporal and amplitude measures of submental and infrahyoid sEMG. a represents single peak swallow and b represents multiple peak swallow (A: onset point, B: maximum amplitude point, C: offset point).

Fig. 2.

Temporal and amplitude measures of submental and infrahyoid sEMG. a represents single peak swallow and b represents multiple peak swallow (A: onset point, B: maximum amplitude point, C: offset point).

Close modal

A total of 3 swallow cycles were obtained per participant. The average of the three cycles of saliva swallowing was calculated for the amplitude as well as for the duration measures of each participant. A total of 60 swallows from 20 participants from both groups were considered for further statistical analysis. In addition, the regression coefficient was calculated to compare the changes between trials within each participant.

Statistical Analysis

Jamovi version 2.3.18.0 (https://www.jamovi.org, Sydney, Australia) was used to carry out the statistical analysis. The statistical significance was set at a p value of <0.05. The Shapiro-Wilk test (significance level p < 0.05) was used to assess data normality. Depending on the nature of the data distribution, appropriate measures of central tendency and dispersion were used for presenting the descriptive data following which an appropriate statistical test was used to compare the differences between the groups.

Cohen’s d was calculated to determine the effect size of statistically significant differences. Values of d < 0.2 are considered negligible; d = 0.2–0.5 are considered a small effect size; d = 0.51–0.8 represents a medium effect size; d > 0.8 is considered a large effect size [17]. Pearson’s correlation coefficients (rho) evaluated the association between submental and infrahyoid sEMG measures in the HNC group. To compare the rate at which the variables change during the subsequent three cycles of saliva swallowing, a regression coefficient [18] was calculated for each participant, and further, the average regression coefficient was compared between groups using the Mann-Whitney U test. Effect sizes (rank-biserial correlation) were calculated and interpreted as trivial (<0.20), small (0.20–0.59), moderate (0.60–1.19), large (1.20–2.00), or very large (>2.00) [19].

Participants’ Characteristics

The demographic details of the included participants are summarized in Table 1. In group A, all but 1 included patient were men, and the mean age of patients in group A was 57.8 years. The most common site of the primary tumor in group A was larynx (n = 9), followed by hypopharynx (n = 7). Most of the patients had stage III or IV disease (n = 15, 75%), followed by stage II (n = 4) and stage I (n = 1). Of all the included patients in group A, only 1 patient had received only radiotherapy for stage II disease of the larynx, and the rest had received 5–6 cycles of chemotherapy (cisplatin-based) concurrently with radiation. Except for 1 patient who had stage I disease of the ear canal and received 66 Gray of radiotherapy, all the included patients had received a total dose of 70 Gray. The participants for group B were selected by convenient sampling technique on a voluntary basis. This group comprised of healthcare workers of the hospital, patients and caregivers who visited the hospital for non-swallowing related issues. None had a history of HNC or neurological ailments. This group included 16 men and four women, with mean age of 56.95 years.

Table 1.

Demographic details of the participants

Group A (n = 20)Group B (n = 20)
SI No.age ^gendersite of primary tumorstagetreatmentswallowing evaluationSI No.age ^gender
modalitydosetime since treatmentFOIS*MASA-C saliva**MASA-C total score***
C1 61 Male Oral cavity T4aN0M0 Definitive CT-RT 70 Gy 35# 180 N1 61 Male 
C2 55 Male Hypopharynx T2N2M0 Definitive CT-RT 70 Gy 35# 175 N2 75 Male 
C3 62 Male Oropharynx T3N1M0 Definitive CT-RT 70 Gy 35# 186 N3 36 Male 
C4 45 Male Glottis T2N0M0 Definitive RT 70 Gy 35# 192 N4 38 Male 
C5 58 Male Larynx T3N1M0 Definitive CT-RT 70 Gy 35# 198 N5 37 Female 
C6 68 Male Ear canal T1N0M0 Definitive CT-RT 66 Gy 30# 10 195 N6 66 Male 
C7 69 Male Oropharynx T3N0M0 Definitive CT-RT 70 Gy 35# 190 N7 38 Female 
C8 64 Male Larynx T3N0M0 Definitive CT-RT 70 Gy 35# 188 N8 68 Female 
C9 71 Male Larynx T2N0M0 Definitive CT-RT 70 Gy 35# 187 N9 33 Female 
C10 53 Male Hypopharynx T2N3bM0 Definitive CT-RT 70 Gy 35# 188 N10 66 Male 
C11 53 Male Larynx T2N0M0 Definitive CT-RT 70 Gy 35# 188 N11 66 Male 
C12 39 Female Nasopharynx T2N2M0 Definitive CT-RT 70 Gy 35# 189 N12 65 Male 
C13 63 Male Larynx T3N1M0 Definitive CT-RT 70 Gy 35# 192 N13 72 Male 
C14 58 Male Hypopharynx T3N3bM0 Definitive CT-RT 70 Gy 35# 177 N14 67 Male 
C15 54 Male Larynx T1aN3bM0 Definitive CT-RT 70 Gy 35# 186 N15 69 Male 
C16 44 Male Hypopharynx T2N0M0 Definitive CT-RT 70 Gy 35# 179 N16 67 Male 
C17 58 Male Larynx T2N0M0 Definitive CT-RT 70 Gy 35# 174 N17 38 Male 
C18 71 Male Hypopharynx T4N3bM0 Definitive CT-RT 70 Gy 35# 177 N18 41 Male 
C19 67 Male Larynx T3N0M0 Definitive CT-RT 70 Gy 35# 196 N19 70 Male 
C20 44 Male Larynx T3N0M0 Definitive CT-RT 70 Gy 35# 10 198 N20 66 Male 
Group A (n = 20)Group B (n = 20)
SI No.age ^gendersite of primary tumorstagetreatmentswallowing evaluationSI No.age ^gender
modalitydosetime since treatmentFOIS*MASA-C saliva**MASA-C total score***
C1 61 Male Oral cavity T4aN0M0 Definitive CT-RT 70 Gy 35# 180 N1 61 Male 
C2 55 Male Hypopharynx T2N2M0 Definitive CT-RT 70 Gy 35# 175 N2 75 Male 
C3 62 Male Oropharynx T3N1M0 Definitive CT-RT 70 Gy 35# 186 N3 36 Male 
C4 45 Male Glottis T2N0M0 Definitive RT 70 Gy 35# 192 N4 38 Male 
C5 58 Male Larynx T3N1M0 Definitive CT-RT 70 Gy 35# 198 N5 37 Female 
C6 68 Male Ear canal T1N0M0 Definitive CT-RT 66 Gy 30# 10 195 N6 66 Male 
C7 69 Male Oropharynx T3N0M0 Definitive CT-RT 70 Gy 35# 190 N7 38 Female 
C8 64 Male Larynx T3N0M0 Definitive CT-RT 70 Gy 35# 188 N8 68 Female 
C9 71 Male Larynx T2N0M0 Definitive CT-RT 70 Gy 35# 187 N9 33 Female 
C10 53 Male Hypopharynx T2N3bM0 Definitive CT-RT 70 Gy 35# 188 N10 66 Male 
C11 53 Male Larynx T2N0M0 Definitive CT-RT 70 Gy 35# 188 N11 66 Male 
C12 39 Female Nasopharynx T2N2M0 Definitive CT-RT 70 Gy 35# 189 N12 65 Male 
C13 63 Male Larynx T3N1M0 Definitive CT-RT 70 Gy 35# 192 N13 72 Male 
C14 58 Male Hypopharynx T3N3bM0 Definitive CT-RT 70 Gy 35# 177 N14 67 Male 
C15 54 Male Larynx T1aN3bM0 Definitive CT-RT 70 Gy 35# 186 N15 69 Male 
C16 44 Male Hypopharynx T2N0M0 Definitive CT-RT 70 Gy 35# 179 N16 67 Male 
C17 58 Male Larynx T2N0M0 Definitive CT-RT 70 Gy 35# 174 N17 38 Male 
C18 71 Male Hypopharynx T4N3bM0 Definitive CT-RT 70 Gy 35# 177 N18 41 Male 
C19 67 Male Larynx T3N0M0 Definitive CT-RT 70 Gy 35# 196 N19 70 Male 
C20 44 Male Larynx T3N0M0 Definitive CT-RT 70 Gy 35# 10 198 N20 66 Male 

C, case; CT-RT, concurrent chemoradiation; FOIS, functional oral intake scale; interpretation of scores; Gy, Gray (Unit of radiation dose); MASA-C, Mann assessment of Swallowing Abilities-Cancer version; N, normal; RT, radiotherapy; TNM, tumor node and metastasis staging.

^age in years; #fraction.

*Interpretation of FOIS scores: 5 – total oral intake of multiple consistencies requiring special preparation; 6 – total oral intake with no special preparation but must avoid specific foods or liquid items; 7 – total oral intake with no restrictions [15].

**Interpretation of MASA-C saliva scores: 6 – moderate dryness with discomfort, thick sticky saliva, dry thin pale oral mucosa with no glistening; 8 – mild mouth dryness, slightly thicker/stringy saliva but not altering feeding behavior; 10 – within normal limits [16].

***Interpretation of MASA-C total scores: the highest possible score is 200. Score: 185–200 = no abnormality, lower scores indicate greater severity of dysphagia.

Comparison of Submental sEMG Parameters between Groups

Submental Recordings

All the relevant measures of submental sEMG and the statistical analysis have been depicted in Table 2.

Table 2.

Comparison of submental sEMG between group A (HNC survivors) and group B (normal individuals)

sEMG parameterGroup A (HNC) (n = 20)Group B (normal) (n = 20)Statistic *p valueEffect size**
valueinterpretation
Mean values of submental recording 
Onset duration, sec 1.09±0.46 0.89±0.24 1.67 0.103 0.528 Medium 
Offset duration, sec 1.85±0.52 1.20±0.28 4.81 <0.001 1.522 Large 
Total duration, sec 2.94±0.67 2.10±0.32 5.99 <0.001 1.580 Large 
Peak amplitude, μV 56.95±15.38 78.40±29.19 −2.91 0.006 0.9 Large 
sEMG parameterGroup A (HNC) (n = 20)Group B (normal) (n = 20)Statistic *p valueEffect size**
valueinterpretation
Mean values of submental recording 
Onset duration, sec 1.09±0.46 0.89±0.24 1.67 0.103 0.528 Medium 
Offset duration, sec 1.85±0.52 1.20±0.28 4.81 <0.001 1.522 Large 
Total duration, sec 2.94±0.67 2.10±0.32 5.99 <0.001 1.580 Large 
Peak amplitude, μV 56.95±15.38 78.40±29.19 −2.91 0.006 0.9 Large 

*By independent sample t test; **by Cohen’s d; significant values marked in bold.

Duration. The average total duration of dry swallow was increased in group A as compared to group B and statistically significant. Within each group, the offset duration was longer than the corresponding onset durations. When comparing between groups, the onset duration of head and neck survivors was found to have been increased than normal group but was not statistically significant. The offset duration was significantly higher in the HNC group than the normal group.

Amplitude. The mean peak amplitude value in group A was less than that of group B in submental recording, and there was a statistical difference between the groups.

Morphology. Single peak was predominantly seen in the submental sEMG of either group. In the HNC group, 46.6% (28/60) swallows were “single peak” and in the normal individuals 68.3% (41/60) swallow cycles were “single peak.” In the HNC group, 21.6% (13/60) were “double peaks,” while in the normal individuals, 20% (12/60) were “double peaks.” More than two peaks were considered to have “multiple peaks.” HNC survivors exhibited a higher tendency to have multiple peaks during swallowing. 31.6% (19 out of 60) of the swallows in group A had multiple peaks, compared to 11.6% (7 out of 60) in group B (Fig. 3).

Fig. 3.

Submental sEMG waves obtained during three tasks of dry swallow in the study. a represents submental recordings obtained in a HNC survivor and b represents submental recordings obtained in a normal participant.

Fig. 3.

Submental sEMG waves obtained during three tasks of dry swallow in the study. a represents submental recordings obtained in a HNC survivor and b represents submental recordings obtained in a normal participant.

Close modal

Infrahyoid Recordings in the HNC Group

In HNC survivors, the peak amplitude obtained by the infrahyoid recording was lower compared to the submental recording (as shown in Fig. 4). There were 25% (15/60) “multiple peaks,” 63.3% (38/60) “single peaks,” and 11.6% (7/60) “double peaks” in the infrahyoid recordings in the HNC group.

Fig. 4.

sEMG waves in a HNC survivor. a represents submental recording and b represents infrahyoid recordings.

Fig. 4.

sEMG waves in a HNC survivor. a represents submental recording and b represents infrahyoid recordings.

Close modal

Effect of Repeated Efforts of Swallow on Submental sEMG

We measured the change in the duration and peak amplitude of submental muscle activity during the subsequent cycles of dry swallow in each participant, and the mean change was further compared between the two study groups. As shown in Table 3, total swallow duration and offset duration for the submental recording were statistically significant between groups. In other words, the submental sEMG yielded a longer duration of subsequent dry swallows, particularly in the offset phase in the HNC group than the normal group. However, there were no significant differences in the amplitude measures.

Table 3.

Comparison of the regression coefficient of submental sEMG across three trials of dry swallowing between the groups

sEMG parameterGroup A (HNC) (n = 20)Group B (normal) (n = 20)Statistic *p valueEffect size**
valueinterpretation
Median (Q1, Q3) values of Submental recording 
Onset duration, sec 0.025 (−0.0625, 0.212) 0.050 (−1.100, 0.100) 196 0.45 0.022 Small 
Offset duration, sec 0.125 (−0.0125, 0.313) 0.000 (−0.100, 0.0500) 125 0.021 0.37 Small 
Total duration, sec 0.250 (−0.113, 0.462) 0.075 (−0.112, 0.150) 130 0.029 0.35 Small 
Peak amplitude, μV 1.75 (0.00, 5.00) 0.00 (−3.13, 8.13) 199 0.51 0.005 Small 
sEMG parameterGroup A (HNC) (n = 20)Group B (normal) (n = 20)Statistic *p valueEffect size**
valueinterpretation
Median (Q1, Q3) values of Submental recording 
Onset duration, sec 0.025 (−0.0625, 0.212) 0.050 (−1.100, 0.100) 196 0.45 0.022 Small 
Offset duration, sec 0.125 (−0.0125, 0.313) 0.000 (−0.100, 0.0500) 125 0.021 0.37 Small 
Total duration, sec 0.250 (−0.113, 0.462) 0.075 (−0.112, 0.150) 130 0.029 0.35 Small 
Peak amplitude, μV 1.75 (0.00, 5.00) 0.00 (−3.13, 8.13) 199 0.51 0.005 Small 

*By Mann-Whitney U test.

**By biserial correlation.

Significant values marked in bold.

Correlation between the Submental and Infrahyoid sEMG Measures in HNC Survivors

Descriptive values of submental and infrahyoid measures in HNC survivors are indicated in Table 4. In this group, the submental total duration was correlated with infrahyoid total duration (r = 0.644; p = 0.001). As shown in Table 5, this correlation is also manifested in the respective onset durations (r = 0.711; p < 0.001) as well as offset durations (r = 0.613; p = 0.002) of submental and infrahyoid sEMG measures. There was also a correlation between infrahyoid activity duration and infrahyoid amplitude (r = −0.560; p = 0.005).

Table 4.

Mean and standard deviation of submental sEMG and infrahyoid sEMG in HNC survivors (group A) (n = 20)

sEMG parameterSubmental sEMGInfrahyoid sEMG
Onset duration, sec 1.09±0.46 1.10±0.32 
Offset duration, sec 1.85±0.52 1.71±0.67 
Total duration, sec 2.94±0.67 2.81±0.77 
Peak amplitude, μV 56.95±15.38 39.35±22.78 
sEMG parameterSubmental sEMGInfrahyoid sEMG
Onset duration, sec 1.09±0.46 1.10±0.32 
Offset duration, sec 1.85±0.52 1.71±0.67 
Total duration, sec 2.94±0.67 2.81±0.77 
Peak amplitude, μV 56.95±15.38 39.35±22.78 
Table 5.

Correlation between submental and infrahyoid sEMG measures in HNC survivors (group A) (n = 20)

sEMG measuresPearson’s rp value
Submental total duration versus submental amplitude 0.298 0.101 
Infrahyoid total duration versus infrahyoid amplitude 0.560 0.005 
Submental total duration versus infrahyoid total duration 0.644 0.001 
Submental amplitude versus infrahyoid amplitude 0.195 0.205 
Submental onset versus infrahyoid onset 0.711 <0.001 
Submental offset versus infrahyoid offset 0.613 0.002 
sEMG measuresPearson’s rp value
Submental total duration versus submental amplitude 0.298 0.101 
Infrahyoid total duration versus infrahyoid amplitude 0.560 0.005 
Submental total duration versus infrahyoid total duration 0.644 0.001 
Submental amplitude versus infrahyoid amplitude 0.195 0.205 
Submental onset versus infrahyoid onset 0.711 <0.001 
Submental offset versus infrahyoid offset 0.613 0.002 

Significant values marked in bold.

In order to understand the post-radiation therapy objective changes in the activity of muscles involved in swallowing, we measured sEMG of submental and infrahyoid muscles in radiotherapy recipients who had no major swallowing issues. We preferred sEMG over other modalities as it provides an objective and real-time graphical representation of muscle activity related to swallowing, and is simple, non-radioactive, non-invasive, and less time-consuming as well as comfortable to the patients [12, 13]. Our own experience with sEMG recordings in swallowing assessment has yielded encouraging results in the past [20]. In the present study, we relied on the sEMG activities of submental muscles (also known as suprahyoid muscles, comprising of anterior belly of the digastric, mylohyoid, and geniohyoid), and infrahyoid muscles (also known as para-laryngeal muscles, comprising sternohyoid, omohyoid, and sternothyroid), as both are crucially involved in pharyngeal phase of swallowing [21‒24].

sEMG Study of Swallowing Function

sEMG recordings of both the submental region [21‒26] and infrahyoid region [21, 24, 26] have shown to be reliable measures of the swallowing function. sEMG studies involving healthy adults of different age groups have compared and reported changes in amplitude and duration of muscle activity across different age groups for different swallowing tasks [24‒29].

Studies involving sEMG recordings of healthy individuals have found differences in the activation of submental muscles between normal swallowing and maneuvers such as the Mendelsohn maneuver [21, 23], effortful swallow [23], and expiratory muscle training [23]. Compared to several other sites in the cervical region, submental (or suprahyoid) and infrahyoid (or para-laryngeal) regions are shown to be most appropriate for assessing the muscular activity related to the pharyngeal phase of swallowing, as these regions get strong sEMG signals corresponding to biomechanical events of pharyngeal swallowing [30].

Difference in the duration and patterns of sEMG measures between healthy and dysphagia patients across different food bolus have been reported in literature [31, 32]. Similarly, comparison of submental sEMG in older adults with and without sarcopenia has been reported [33]. sEMG measurements across different swallow tasks have been reported in surgically treated HNC patients [20, 34]. However, studies that have evaluated the utility of sEMG in radiotherapy recipients of HNC are scanty [35, 36].

sEMG Measurements in Irradiated HNC Survivors

sEMG recording of the submental region has been shown to be a sensitive, valid, and reliable predictor of swallowing [37]. Nederkoorn and colleagues reported sEMG to be a useful tool for measuring salivary flow. They correlated the number of swallows observed in sEMG with the amount of saliva obtained in cotton rolls [38]. However, the temporal and amplitude aspects have not been examined.

A study by Carvalho and colleagues evaluated HNC survivors’ swallowing ability using videofluoroscopy and sEMG. They reported that a majority of patients had lower than appropriate levels of salivary production and some patients presented with residue and penetration. They also analyzed the electrical activity of the suprahyoid muscle and the upper orbicularis oris muscle during swallowing [36]. The orbicularis oris muscle had a shorter swallowing time compared to the other muscles. However, these findings were not compared with normal individuals.

In our study, we found that the total swallow durations of submental sEMG were significantly higher in the HNC group than in the normal individuals during dry swallow. In particular, the onset duration of submental sEMG was longer though not significantly (p > 0.05) in the HNC group and the offset duration was significantly longer (p < 0.05) in the HNC group. The longer onset duration may be explained by longer muscle activity needed to initiate swallowing and also due to complexity involved in accumulating saliva prior to swallow, and longer offset time could be attributed to the motility changes of swallowing structures that are seen in post-radiation therapy patients. Increased duration of laryngeal motion has been reported in videofluoroscopy studies of HNC patients treated with organ preservation protocols [39]. Changes reported are slow or delayed laryngeal vestibule closure [39‒41] and delayed pharyngeal swallow [42] in the first few months after treatment with radiation/chemoradiation for HNCs [43]. Based on the findings of Smith et al. [44], it was noted that the length of laryngeal elevation appeared to extend progressively, in patients who are beyond a year after completion of radiation therapy and were attributed to fibrosis.

Previous literature has reported that the duration of submental sEMG during saliva swallowing tends to be longer than that of liquid bolus swallow in normal individuals [28]. Furthermore, it has been observed that a prolonged duration of saliva swallow is also evident in geriatric individuals as compared to younger adults. In a study conducted on normal Chinese individuals, it was noted that the duration of submental and infrahyoid sEMG during saliva swallow increased gradually with age [27]. These findings suggest that age and swallowing task may also play a role in the duration of sEMG during swallow and may have implications for clinical practice.

The lesser amplitude of the submental muscles in the HNC could possibly be attributed to the reduced quantity of saliva as compared to normal individuals. In addition, acute post-radiation changes such as reduced tissue elasticity as well as edematous neck may also have an influence on the lesser amplitude recordings in this group.

sEMG amplitude is reported to be influenced by various factors such as skin and electrode impedance, the depth of the muscle from the skin surface, and variations in muscle size among individuals [45]. A decrease in the submental sEMG mean amplitude with increasing age has been reported in other studies for saliva swallow task [45] and food bolus [46]. This may be attributed to a combination of age related skin and muscle changes.

Interestingly, a study conducted by Sakai revealed that patients with sarcopenic dysphagia showed higher submental muscle amplitudes during swallowing, the authors attributed it to the lower muscle mass and fat percentage in these patients [33]. The amplitude of EMG has been noted to decrease with an increase in the distance between muscle and electrode, indicating that augmented subcutaneous tissue can diminish sEMG amplitude [47]. Following head and neck radiation treatment, soft-tissue alterations like skin thickening, epiglottic thickening, and subcutaneous fat stranding are documented [48]. These changes can lead to a reduction in submental sEMG amplitude.

Moreover, external lymphedema of the face and neck has been documented to manifest 2–6 months post-HNC treatment [49], with the submental region identified as the most common site for external lymphedema in irradiated HNC patients [50]. It is probable that these factors contribute to a decreased amplitude in submental recording.

While a few recent studies have reported the utility of sEMG measurements in assessing the swallowing function in HNC, their patient population, objectives, and methodology were variable [20, 34‒36]. Most notably, a recently published study from China has evaluated the sEMG activity in 10 radiotherapy recipients of nasopharyngeal carcinoma and compared it with 10 healthy volunteers, using a unique high-density sEMG with 96 electrodes [35]. However, they have used food with different consistencies to measure the average power of suprahyoid and infrahyoid muscles during swallowing. Another study from Brazil evaluated the correlation of sEMG of neck muscles in swallows of different consistencies with the swallowing function in 17 participants of HNC, but several of their patients had received surgical treatment in addition to radiotherapy [36]. Also, both these studies included patients with significant dysphagia in their analyses.

Our study is unique from these in that we have evaluated the sEMG recordings of dry swallow only in radiotherapy recipients with normal or near-normal swallow and eliminated the influence of boluses and disease or surgery-related factors on swallowing. Though all our patients had adequate functional swallowing skills as they were able to consume a complete oral diet, the MASA-C saliva domain scores is suggestive of reduced salivation in a majority of our HNC survivors, as shown in Table 1. Since the task for sEMG recording was focused on saliva swallowing, it is possible that this reduced salivation may have impacted the temporal and amplitude measures of submental sEMG. Nevertheless, it is important to note that there was no objective test conducted to measure salivation. Furthermore, the MASA-C saliva domain scores are based on clinical observations, and as such attribution of hyposalivation with sEMG measures cannot be ascertained.

Radiation-induced tissue and muscular changes too could hinder the muscle amplitude and duration in submental sEMG recording. Fibrosis is less likely to be a factor, as the effect of radiation on muscle and resultant fibrosis takes longer time to manifest after radiation than the post-radiation interval in our study [35]. However, computed tomography and magnetic resonance imaging studies have revealed interstitial edema of soft tissues, skin thickening, and subcutaneous reticulations as the early post-radiation changes in HNC patients [51, 52]. Hence, it is important to consider the impact of post-radiation skin and muscular changes in irradiated patients as it is highly probable that they can affect the submental sEMG activity.

Biomechanical Correlates of sEMG Recording during Swallowing

The sEMG signals from neck muscles have been shown to correlate well with the biomechanical events of the pharyngeal phase of the deglutition process, including the changes in pharyngeal pressures and in both dry swallow and effortful swallow [22, 53]. Also, the complex interplay between the sEMG activity of these muscles, the external movements of the hyolaryngeal framework, including hyolaryngeal excursion, and the different types of swallows, and different types of boluses, has all been well documented [23]. One of the most critical events for airway protection during the pharyngeal phase of swallowing is hyolaryngeal excursion [23, 54]. Both groups of muscles, submental and infrahyoid, play a crucial role in the initiation and execution of hyolaryngeal excursion [21‒24].

There have been very few studies conducted where researchers have simultaneously recorded sEMG with VFSS [22, 23] or EGG [21] in order to analyze the biomechanical factors associated with sEMG. Generally, the submental sEMG peak amplitude precedes the maximum hyoid angle of elevation and maximum hyoid displacement during both the dry swallow as well as with other effortful swallows [21, 23, 54]. Our study finds that the offset duration of submental sEMG is significantly longer in radiotherapy recipients than the normal subjects, highlighting a delay in the hyolaryngeal descent in irradiated patients. In addition, our co-relation matrix depicts a statistically significant association between the submental and infrahyoid temporal measures in the irradiated patients. As per the literature reports, these findings could also possibly reflect on the further long-term worsening of the swallowing scores in some of these patients, as the activity of infrahyoid muscles, which are crucial for laryngeal protection, tend to worsen with time after radiotherapy [55].

Regression Co-Efficient of Repeated Swallows and Miscellaneous Findings

In our study, the rate of change in submental muscle activity duration within the subsequent three times of saliva swallowing was significantly more than the rate of change in the control group. This could also probably reflect on the effect of xerostomia on the initiation of the pharyngeal phase of swallowing in radiotherapy recipients, thereby making subsequent swallows arduous.

On comparison of activities within the group, the amplitude of the muscle activity obtained from the infrahyoid location was lesser than the submental recordings in HNC survivors (shown in Table 4). These results corroborate with literature reports that infer lesser sEMG activity of the infrahyoid group than the submental group, which in turn is lesser than the recording obtained with masseter [29]. Nevertheless, there existed a positive correlation between infrahyoid and submental muscle activity duration, mirroring the synergistic effect of both muscle groups in facilitating swallowing. Both submental and infrahyoid muscles work closely during hyolaryngeal excursion [21].

The results of our study are also in consonance with earlier findings with regard to waveform patterns of sEMG, single peaks predominated during the dry swallow in both radiation recipients and normal individuals, followed by double peaks and multiple peaks. Double and multiple peaks have been reported in sEMG studies of normal individuals [45] and post-surgical HNC patients [20].

Limitations and Future Scope

Some of the limitations of this exploratory study are as follows. An instrumental assessment of swallowing function, either by videofluoroscopy, functional endoscopic evaluation of swallowing, or pharyngeal manometry, could have aided correlation of the sEMG with the intraluminal physical and pressure changes. As clinical swallow assessments cannot rule out silent aspiration or pharyngeal residues that patients may not be aware of, information from instrumental assessment could have provided valuable information about biomechanical functions.

Literature suggests that there is a higher variability in the onset of hyoid elevation among individuals [56]. To accurately identify the peak hyoid elevation, especially in cases where multiple peaks are present, simultaneous videofluoroscopic assessments along with sEMG may be a more effective approach to understand the biomechanics.

Changes in sEMG in our study are likely to be due to composite effect of radiation on the muscle and reduced salivation. Future studies on the similar lines could make involve patients with different severity of dysphagia and also aim to validate the results of sEMG by multidimensional assessment, including patient-reported tools on self-perceived swallowing issues. sEMG of swallowing tasks with food items may give additional information regarding time and exertion needed to form a cohesive bolus after fragmentation and addition of saliva, and it may be relevant to patients with post radiation changes.

To provide a more accurate analysis of the hyposalivary changes in the patient group being studied, it would be advantageous to include sialometry to objectively assess salivary flow rate; this could be particularly beneficial while conducting a saliva swallow task in sEMG. In addition, as in most of the other studies, the patient population in our study too was heterogenous with multiple sites of primary tumor. Further studies could include a particular site of the HNC for analyzing the effect of radiotherapy using sEMG findings. Lastly, considering the significant similarities in the neuromuscular and mucosal lining of the phonatory apparatus and upper digestive system, future sEMG studies could also explore the effects of radiotherapy on the voice of individuals with non-laryngeal cancer.

The present study serves to reinforce the utility of sEMG for noninvasive visual evaluation and measurement of swallowing, in addition to its potential as a biofeedback tool in dysphagia intervention. Further investigations into the application of sEMG in the assessment of swallowing are promising, especially in areas where fiberoptic endoscopic evaluation of swallowing and/or modified barium swallow studies are not easily accessible.

It is a simple and non-invasive method with no potential risks. The results of this study suggest that assessing swallowing using sEMG might be an indicator of post-radiation changes and swallowing dysfunction in HNC survivors. Additionally, it sheds light on the potential usage of sEMG measures in identifying sub-clinical dysphagia; however, prospective longitudinal studies are further needed to validate these findings.

Both studies were reviewed and approved by Kasturba Medical College and Kasturba Hospital Institutional Ethics Committee (IEC-362/2020 and IEC2-273/2022). Written informed consent was provided by all participants.

The authors have no competing interests to declare that are relevant to the content of this article.

No funding was received for conducting this study.

The authors confirm contribution to the paper as follows: study conception and design: V.U.A and J.J.V; data collection: J.J.V and S.J.P; analysis and interpretation of results J.J.V, V.U.A, V.G, K.D., K.S., and B.R.; draft manuscript preparation: J.J.V.; manuscript revisions: V.A., K.D., K.S., S.J.P., V.G., and B.R. All authors approved the final version of the manuscript.

The data that support the findings of this study are not publicly available due to privacy reasons but are available from the corresponding author upon reasonable request. Further inquiries can be directed to the corresponding author.

1.
Ambrocio
KR
,
Miles
A
,
Bhutada
AM
,
Choi
D
,
Garand
KL
.
Defining normal sequential swallowing biomechanics
.
Dysphagia
.
2023
;
38
(
6
):
1497
510
.
2.
Matsuo
K
,
Palmer
JB
.
Anatomy and physiology of feeding and swallowing: normal and abnormal
.
Phys Med Rehabil Clin N Am
.
2008
;
19
(
4
):
691
707
. vii.
3.
Molfenter
SM
,
Steele
CM
.
Use of an anatomical scalar to control for sex-based size differences in measures of hyoid excursion during swallowing
.
J Speech Lang Hear Res
.
2014
;
57
(
3
):
768
78
.
4.
King
SN
,
Dunlap
NE
,
Tennant
PA
,
Pitts
T
.
Pathophysiology of radiation-induced dysphagia in head and neck cancer
.
Dysphagia
.
2016
;
31
(
3
):
339
51
.
5.
Crowder
SL
,
Douglas
KG
,
Yanina Pepino
M
,
Sarma
KP
,
Arthur
AE
.
Nutrition impact symptoms and associated outcomes in post-chemoradiotherapy head and neck cancer survivors: a systematic review
.
J Cancer Surviv
.
2018
;
12
(
4
):
479
94
.
6.
Pytel
A
,
Zielińska
A
,
Staś
J
,
Chabowski
M
.
Quality of life, psychological distress, and nutritional status of polish patients with head and neck cancer treated with radiotherapy
.
J Clin Med
.
2023
;
12
(
2
):
659
.
7.
Dirix
P
,
Nuyts
S
,
Van den Bogaert
W
.
Radiation-induced xerostomia in patients with head and neck cancer: a literature review
.
Cancer
.
2006
;
107
(
11
):
2525
34
.
8.
Martin
A
,
Murray
L
,
Sethugavalar
B
,
Buchan
C
,
Williams
GF
,
Sen
M
, et al
.
Changes in patient-reported swallow function in the long term after chemoradiotherapy for oropharyngeal carcinoma
.
Clin Oncol
.
2018
;
30
(
12
):
756
63
.
9.
Rogus-Pulia
NM
,
Pierce
MC
,
Mittal
BB
,
Zecker
SG
,
Logemann
JA
.
Changes in swallowing physiology and patient perception of swallowing function following chemoradiation for head and neck cancer
.
Dysphagia
.
2014
;
29
(
2
):
223
33
.
10.
Vermaire
JA
,
Raaijmakers
CPJ
,
Verdonck-de Leeuw
IM
,
Jansen
F
,
Leemans
CR
,
Terhaard
CHJ
, et al
.
Mastication, swallowing, and salivary flow in patients with head and neck cancer: objective tests versus patient-reported outcomes
.
Support Care Cancer
.
2021
;
29
(
12
):
7793
803
.
11.
Kirsh
E
,
Naunheim
M
,
Holman
A
,
Kammer
R
,
Varvares
M
,
Goldsmith
T
.
Patient-reported versus physiologic swallowing outcomes in patients with head and neck cancer after chemoradiation
.
Laryngoscope
.
2019
;
129
(
9
):
2059
64
.
12.
Vaiman
M
.
Standardization of surface electromyography utilized to evaluate patients with dysphagia
.
Head Face Med
.
2007
;
3
:
26
.
13.
Stepp
CE
.
Surface electromyography for speech and swallowing systems: measurement, analysis, and interpretation
.
J Speech Lang Hear Res
.
2012
;
55
(
4
):
1232
46
.
14.
Crary
MA
,
Mann
GDC
,
Groher
ME
.
Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients
.
Arch Phys Med Rehabil
.
2005
;
86
(
8
):
1516
20
.
15.
Carnaby
GD
,
Crary
MA
.
Development and validation of a cancer-specific swallowing assessment tool: masa-C
.
Support Care Cancer
.
2014
;
22
(
3
):
595
602
.
16.
Krishnamurthy
R
,
Balasubramanium
RK
,
Hegde
PS
.
Evaluating the psychometric properties of the Kannada version of EAT 10
.
Dysphagia
.
2020
;
35
(
6
):
962
7
.
17.
Cohen
J
.
A power primer
.
Psychol Bull
.
1992
;
112
(
1
):
155
9
.
18.
Matthews
JN
,
Altman
DG
,
Campbell
MJ
,
Royston
P
.
Analysis of serial measurements in medical research
.
BMJ
.
1990
;
300
(
6719
):
230
5
.
19.
Hedges
LV
.
Distribution theory for glass’s estimator of effect size and related estimators
.
J Educ Stat
.
1981
;
6
(
2
):
107
.
20.
Harsha Raj
G
,
Aithal
VU
,
Guddattu
V
.
Comparison of pharyngoesophageal segment biomechanics between persons with total laryngectomy with and without dysphagia using sEMG: a multicentric swallow study
.
Dysphagia
.
2020
;
35
(
5
):
843
52
.
21.
Ding
R
,
Larson
CR
,
Logemann
JA
,
Rademaker
AW
.
Surface electromyographic and electroglottographic studies in normal subjects under two swallow conditions: normal and during the Mendelsohn manuever
.
Dysphagia
.
2002
;
17
:
1
12
.
22.
Crary
MA
,
Carnaby Mann
GD
,
Groher
ME
.
Biomechanical correlates of surface electromyography signals obtained during swallowing by healthy adults
.
J Speech Lang Hear Res
.
2006
;
49
(
1
):
186
93
.
23.
Wheeler-Hegland
KM
,
Rosenbek
JC
,
Sapienza
CM
.
Submental sEMG and hyoid movement during Mendelsohn maneuver, effortful swallow, and expiratory muscle strength training
.
J Speech Lang Hear Res
.
2008
;
51
(
5
):
1072
87
.
24.
Poorjavad
M
,
Talebian
S
,
Ansari
NN
,
Soleymani
Z
.
Surface electromyographic assessment of swallowing function
.
Iran J Med Sci
.
2017
;
42
(
2
):
194
200
.
25.
Ng
KB
,
Guiu Hernandez
E
,
Erfmann
KLC
,
Jones
RD
,
Macrae
P
,
Huckabee
M-L
.
Effect of volitional effort on submental surface electromyographic activity during healthy swallowing
.
Dysphagia
.
2022
;
37
(
2
):
297
306
.
26.
Vaiman
M
,
Eviatar
E
,
Segal
S
.
Surface electromyographic studies of swallowing in normal subjects: a review of 440 adults. Report 1. Quantitative data: timing measures
.
Otolaryngol Head Neck Surg
.
2004
;
131
(
4
):
548
55
.
27.
Liu
L-L
,
Zhong
Y-J
,
Chen
X-P
,
Shuai
L
,
Feng
Z
.
Surface electromyography of pharyngeal swallowing in healthy Chinese individuals: establishment of a timing and amplitude database
.
Dysphagia
.
2023
;
38
(
5
):
1398
405
.
28.
Perlman
AL
,
Palmer
PM
,
McCulloch
TM
,
Vandaele
DJ
.
Electromyographic activity from human laryngeal, pharyngeal, and submental muscles during swallowing
.
J Appl Physiol
.
1999
;
86
(
5
):
1663
9
.
29.
Vaiman
M
,
Eviatar
E
,
Segal
S
.
Surface electromyographic studies of swallowing in normal subjects: a review of 440 adults. Report 2. Quantitative data: amplitude measures
.
Otolaryngol Head Neck Surg
.
2004
;
131
(
5
):
773
80
.
30.
Zaretsky
E
,
Pluschinski
P
,
Sader
R
,
Birkholz
P
,
Neuschaefer-Rube
C
,
Hey
C
.
Identification of the most significant electrode positions in electromyographic evaluation of swallowing-related movements in humans
.
Eur Arch Oto-Rhino-Laryngol
.
2017
;
274
(
2
):
989
95
.
31.
Koyama
Y
,
Ohmori
N
,
Momose
H
,
Kondo
E
,
Yamada
S
,
Kurita
H
.
Detection of swallowing disorders using a multiple channel surface electromyography sheet: a preliminary study
.
J Dent Sci
.
2021
;
16
(
1
):
160
7
.
32.
Koyama
Y
,
Ohmori
N
,
Momose
H
,
Yamada
S
,
Kurita
H
.
Detection of swallowing disorders with a multiple-channel surface electromyography sensor sheet
.
J Dent Sci
.
2022
;
17
(
3
):
1185
92
.
33.
Sakai
K
,
Nakayama
E
,
Rogus-Pulia
N
,
Takehisa
T
,
Takehisa
Y
,
Urayama
KY
, et al
.
Submental muscle activity and its role in diagnosing sarcopenic dysphagia
.
CIA
.
2020
;
15
:
1991
9
.
34.
Constantinescu
G
,
Hodgetts
W
,
Scott
D
,
Kuffel
K
,
King
B
,
Brodt
C
, et al
.
Electromyography and mechanomyography signals during swallowing in healthy adults and head and neck cancer survivors
.
Dysphagia
.
2017
;
32
(
1
):
90
103
.
35.
Leung
KKY
,
Fong
R
,
Zhu
M
,
Li
G
,
Chan
JYK
,
Stewart
M
, et al
.
High-density surface electromyography for swallowing evaluation in post-radiation dysphagia
.
Laryngoscope
.
2023
;
133
(
11
):
2920
8
.
36.
de Carvalho
MI
,
Gatti
M
,
Guedes
RLV
,
Froes
RCF
,
Costa
DR
,
da Silva Vitor
J
, et al
.
Swallowing, nutritional status, and salivary flow in patients after head and neck cancer treatment, a pilot study
.
Sci Rep
.
2021
;
11
(
1
):
20233
.
37.
Vaiman
M
,
Eviatar
E
,
Segal
S
.
Surface electromyographic studies of swallowing in normal subjects: a review of 440 adults. Report 3. Qualitative data
.
Otolaryngol Head Neck Surg
.
2004
;
131
(
6
):
977
85
.
38.
Nederkoorn
C
,
Smulders
FTY
,
Jansen
A
.
Recording of swallowing events using electromyography as a non-invasive measurement of salivation
.
Appetite
.
1999
;
33
(
3
):
361
9
.
39.
Kotz
T
,
Abraham
S
,
Beitler
JJ
,
Wadler
S
,
Smith
RV
.
Pharyngeal transport dysfunction consequent to an organ-sparing protocol
.
Arch Otolaryngol Head Neck Surg
.
1999
;
125
(
4
):
410
3
.
40.
Kotz
T
,
Costello
R
,
Li
Y
,
Posner
MR
.
Swallowing dysfunction after chemoradiation for advanced squamous cell carcinoma of the head and neck
.
Head Neck
.
2004
;
26
(
4
):
365
72
.
41.
Logemann
JA
,
Pauloski
BR
,
Rademaker
AW
,
Lazarus
CL
,
Gaziano
J
,
Stachowiak
L
, et al
.
Swallowing disorders in the first year after radiation and chemoradiation
.
Head Neck
.
2008
;
30
(
2
):
148
58
.
42.
Eisbruch
A
,
Schwartz
M
,
Rasch
C
,
Vineberg
K
,
Damen
E
,
Van As
CJ
, et al
.
Dysphagia and aspiration after chemoradiotherapy for head-and-neck cancer: which anatomic structures are affected and can they be spared by IMRT
.
Int J Radiat Oncol Biol Phys
.
2004
;
60
(
5
):
1425
39
.
43.
Pauloski
BR
,
Rademaker
AW
,
Logemann
JA
,
Newman
L
,
MacCracken
E
,
Gaziano
J
, et al
.
Relationship between swallow motility disorders on videofluorography and oral intake in patients treated for head and neck cancer with radiotherapy with or without chemotherapy
.
Head Neck
.
2006
;
28
(
12
):
1069
76
.
44.
Smith
RV
,
Kotz
T
,
Beitler
JJ
,
Wadler
S
.
Long-term swallowing problems after organ preservation therapy with concomitant radiation therapy and intravenous hydroxyurea: initial results
.
Arch Otolaryngol Head Neck Surg
.
2000
;
126
(
3
):
384
9
.
45.
Vaiman
M
,
Eviatar
E
,
Segal
S
.
Evaluation of normal deglutition with the help of rectified surface electromyography records
.
Dysphagia
.
2004
;
19
(
2
):
125
32
.
46.
Krishnan
G
,
Goswami
S
.
Surface electromyographic activity of submental muscles during swallow of masticated bolus across age and gender
.
Review
.
2022
.
47.
Nordander
C
,
Willner
J
,
Hansson
G
,
Larsson
B
,
Unge
J
,
Granquist
L
, et al
.
Influence of the subcutaneous fat layer, as measured by ultrasound, skinfold calipers and BMI, on the EMG amplitude
.
Eur J Appl Physiol
.
2003
;
89
(
6
):
514
9
.
48.
Bronstein
AD
,
Nyberg
DA
,
Schwartz
AN
,
Shuman
WP
,
Griffin
BR
.
Soft-tissue changes after head and neck radiation: CT findings
.
AJNR Am J Neuroradiol
.
1989
;
10
(
1
):
171
5
.
49.
Deng
J
,
Ridner
SH
,
Dietrich
MS
,
Wells
N
,
Wallston
KA
,
Sinard
RJ
, et al
.
Factors associated with external and internal lymphedema in patients with head-and-neck cancer
.
Int J Radiat Oncol Biol Phys
.
2012
;
84
(
3
):
e319
28
.
50.
Jeans
C
,
Brown
B
,
Ward
EC
,
Vertigan
AE
,
Pigott
AE
,
Nixon
JL
, et al
.
Comparing the prevalence, location, and severity of head and neck lymphedema after postoperative radiotherapy for oral cavity cancers and definitive chemoradiotherapy for oropharyngeal, laryngeal, and hypopharyngeal cancers
.
Head Neck
.
2020
;
42
(
11
):
3364
74
.
51.
Gehani
A
,
Sen
S
,
Chatterjee
S
,
Mukhopadhyay
S
.
Imaging features of postradiotherapy changes in head and neck cancers
.
Indian J Radiol Imaging
.
2021
;
31
(
3
):
661
9
.
52.
Glastonbury
CM
,
Parker
EE
,
Hoang
JK
.
The postradiation neck: evaluating response to treatment and recognizing complications
.
AJR Am J Roentgenol
.
2010
;
195
(
2
):
W164
71
.
53.
Huckabee
M-L
,
Butler
SG
,
Barclay
M
,
Jit
S
.
Submental surface electromyographic measurement and pharyngeal pressures during normal and effortful swallowing
.
Arch Phys Med Rehabil
.
2005
;
86
(
11
):
2144
9
.
54.
Schultz
JL
,
Perlman
AL
,
VanDaele
DJ
.
Laryngeal movement, oropharyngeal pressure, and submental muscle contraction during swallowing
.
Arch Phys Med Rehabil
.
1994
;
75
(
2
):
183
8
.
55.
Xinou
E
,
Chryssogonidis
I
,
Kalogera-Fountzila
A
,
Panagiotopoulou-Mpoukla
D
,
Printza
A
.
Longitudinal evaluation of swallowing with videofluoroscopy in patients with locally advanced head and neck cancer after chemoradiation
.
Dysphagia
.
2018
;
33
(
5
):
691
706
.
56.
Gay
T
,
Rendell
JK
,
Spiro
J
,
Mosier
K
,
Lurie
AG
.
Coordination of oral cavity and laryngeal movements during swallowing
.
J Appl Physiol
.
1994
;
77
(
1
):
357
65
.