Effect of segmental tongue function training on tongue pressure attributes in individuals with dysphagia after receiving radiotherapy for nasopharyngeal carcinoma

Abstract

Objective

This study aimed to assess the impact of segmental tongue function training on tongue pressure characteristics in nasopharyngeal carcinoma after radiotherapy(NPCR) patients who experience dysphagia. The findings of this research are crucial in understanding the potential benefits of tongue rehabilitation exercises for individuals with NPC patients. Hence, it is essential to explore the effects of this type of training on tongue pressure and its associated characteristics.

Methods

A group of eighteen NPCR dysphagia patients underwent a two-week segmental tongue function training. The researchers assessed their tongue motor function by measuring the tongue pressure (P) and endurance time (ET) in three different regions of the tongue-the anterior tongue region (TAR), central tongue region (TCR), and posterior tongue region (TPR). To gather accurate data, a new flexible tongue pressure sensor with 9 measuring sites arranged in a 3 × 3 configuration was used to measure the pressure exerted by the tongue on the palate. The measurements were taken both before and after the segmental tongue function training.

Results

The segmental tongue function training resulted in significant improvements in tongue pressure for the anterior(P_TAR) and central(P_TCR) parts of the tongue(P < 0.05). However, there was no significant change in tongue pressure for the posterior(P_TPR) part of the tongue(P > 0.05). Additionally, there were no significant differences in the endurance time for each part of the tongue(P > 0.05).

Conclusions

Segmental tongue function training improved the P_TAR and P_TCR in NPCR dysphagia patients within 2 weeks, and the improvement gradually decreased from the anterior part of the tongue to the posterior part of the tongue. Meanwhile, there were no significant differences in PTPR and ET of between each part before and after treatment. This suggests that a longer duration weeks of training may be needed to improve the PTPR and ET in these patients, or alternatively, more targeted training programs could be designed.

Introduction

Radiotherapy is a prominent therapeutic strategy for nasopharyngeal carcinoma(NPC), encompassing radiotherapy(RT) [1] and concurrent chemoradiotherapy (CCRT) [2]. Although it can treat the locoregional tumor, it also causes some acute and late toxicities side effects [3]. Compared to oropharyngeal cancer patients after surgery, the most common late toxicities side effects for NPC patients are the tongue muscle atrophy and fibrosis [4, 5]. These conditions make the NPC patients’ tongue pressure decrease after radiotherapy(The pattern of decline was that the tongue pressure decreased in all regions, and it became more and more obvious from the anterior to the posterior of the tongue [6]), which causes dysphagia [7]. Efficient and safe swallowing heavily relies on tongue pressure(P), which plays a crucial role in propelling food from the oral cavity through the pharynx to the esophagus [8]. Decreased tongue pressure leads to a decline in tongue base to pharyngeal wall contact, resulting in prolonged oral and pharyngeal transit time and an elevated risk of aspiration [9]. Due to the different types of muscle fibers in each part of the tongue, radiation therapy results in an inconsistent decrease in tongue pressure [10]. There were many studies on the decrease in tongue pressure of the whole tongue in patients after radiotherapy [11], but few about each part of the tongue pressure.

Segmental tongue function training [12–14], such as electrical stimulation of the tongue [15], can improve both tongue strength and movement.The increase in tongue pressure and improvement in swallowing function reflect the enhancement of tongue muscle strength and tongue movement. This improvement has been observed not only in healthy individuals but also in patients with chronic dysphagia resulting from chemoradiotherapy. Although more and more studies have shown that segmental tongue function training can improve tongue pressure in NPCR patients, it has not been precise to which part of the tongue and there are limited effective tongue pressure rehabilitative approaches. According to a research conducted by Wall et al., the most effective form of tongue rehabilitation training for individuals who have undergone radiotherapy for NPCR patients is preventive training specifically guided for tongue rehabilitation [16]. Nevertheless, findings by Lazarus et al. revealed some limitations in real-time monitoring of patients’ training intensity, movement accuracy and compliance, ultimately leading to unsatisfactory outcomes in terms of rehabilitation [17].

This study focused on the effect of segmental tongue function training on characteristics of each part of tongue pressure in NPCR patients with dysphagia. Furthermore, we would like to identify the extent to which 2-week segmental tongue function training improves tongue muscle pressure at different parts in NPCR patients, which will aid treatment decisions in these patients.

Methods

Between July 2022 and April 2023, a total of 18 patients with dysphagia due to NPCR were recruited from the rehabilitation department of the Third Affiliated Hospital of Sun Yat-sen University. All patients had dysphagia for the first time and had not received swallowing training before. Table 1 presents the demographic information of all patients. The inclusion criteria of the patients was as follows: (1) having a diagnosis of NPC confirmed by MRI and histologically diagnosed with malignant tumors in the nasopharynx; (2) dysphagia was diagnosed by Videofluoroscopic swallowing study (VFSS) [18], presence of oral or pharyngeal dysphagia, impaired safety or effectiveness; (3) clinical examination showed no abnormalities in the oral cavity and intact dentition; (4) pharyngeal and vomiting reflexes were absent; (5) screening with a quick questionnaire detected impairment in hearing and comprehension. Individuals who scored > 24 on the Mini-Mental State Examination(MMSE) [19] and < 24 on the Hearing Handicap Inventory for the Elderly-Screening(HHIE-S) [20] were included in the study; (6) patients had to be fully aware and willing to participate in the therapy, as well as capable of giving informed consent; (7) adequate physical and endurance was necessary to fulfill the exercise prescription requirements.

Table 1.

Demographic information of NPC patients

Variables	Gender(m%)	Age(y)	Radiotherapy sessions (n)	Time to last radiotherapy session (y)	Dysphagia onset (y)
NPC Patients (n = 18)	77.78%	53.78 ± 11.38	34.22 ± 0.42	10.56 ± 4.45	2.39 ± 0.68
Range	/	38–79	32–35	5–25	1–4

Abbreviation NPC, Nasopharyngeal carcinoma; m, male; y,year; n,number

The exclusion criteria for all patients was as follows: (1) the history of neurogenic conditions that can lead to weakness in the muscles of the tongue, including stroke, Parkinson’s disease, amyotrophic lateral sclerosis (ALS), tongue cancer, and laryngeal carcinoma; (2) recurrent or metastatic nasopharyngeal tumors; (3) oral structural abnormalities detected during clinical examination; (4)some patients were unable to complete the test and train due to oral pain and discomfort; (5) inability to comply with commands given by the tongue pressure sensors was observed; (6) patients were taken muscle relaxants; (7) unstable vital signs; and (8) patients or their family members exhibited uncooperative behavior.

This study underwent a thorough review and was approved by the Ethics Committee of The Third Affiliated Hospital of Sun Yat-sen University (Approval No: CUHK Attached SAN Medical Ethics [2021]02-200-01). All individuals participating in the study provided written informed consent for the utilization of their medical data and any remaining specimens.

Treatment

In this research, a total of 18 patients to evaluation from a team of medical professionals prior to the intervention. Following this, the medical team developed an training program focused on enhancing tongue function for all patients. The program was conducted by a proficient speech-language pathologist (SLP) possessing a 13-year experience in dysphagia therapy.

The training program consisted of 10 days of treatment, with two sessions per day. Each treatment session included intensive exercises on the anterior tongue (TAR), center tongue (TCR), posterior tongue (TPR) and the whole tongue, as well as low-frequency electrical tongue stimulation, as shown in Table 2 [21–24]. Each type of exercise was repeated 10 times within each session. Each exercise holding for 10 repetitions with a 10-second rest interval between each repetition. Holding for 10s means that the patient holds the movement for 10 s at the end of completing the movement (Fig. 1). Patients were instructed to take a one-minute break after each intense training session and were allowed to perform oral cleaning during this interval. The medical team regularly evaluated the patients’ progress and made necessary adjustments to the segmental tongue function training. Additionally, the SLP modified the training program according to each patient’s individual needs.The exercise prescription was based on the meta-analysis by Banda et al. [25], as well as the Korean version of clinical dysphagia rehabilitation guidelines [26], and is clinically feasible.

Table 2.

The intervention protocol

Region	Objective	Intervention	Duration of maintenance	Frequency/day	Total frequency
TAR	To increase TAR flexibility	1.TAR flexibility training: Patients were instructed to touch their teeth with TAR as much as possible, including the medial and lateral parts of the upper alveolar and the medial and lateral parts of the lower alveolar bone.	10s	10 times per session, 2 sessions a day	10 days per cycle
	To increase TAR flexibility	2.TAR active movement training: Patients try their best to use TAR to lick lips, including up, down, left and right four directions. The patient complete 10 repetitions of elevation (up), 10 repetitions of depression (down), 10 repetitions of lateralization to the right (right) and 10 repetitions of lateralization to the left (left).
	To increase the forward and upward force of the tongue	3.TAR suction cotton swab training (TAR resistance training): Place the swab in the TAR and draw it with the force of the front of your tongue (suction the swab into your mouth like you would drink from a straw).
TCR	To increase the muscle strength of the TCR	1.TCR resistance training: SLP pressed their index and middle fingers on the TCR of the patient, and instructed the patient to maintain the TCR with maximum force against the downward pressure of SLP’s fingers.
TPR	To increase the muscle strength of the TPR	1.Modified Tongue-hold swallows: which involved wrapping a patient’s tongue with gauze, pulling it forward, and then instructing the patient to forcefully pull it back into the oral cavity against the resistance of traction and to swallow immediately
		2.TPR resistance training: SLP pressed their index and middle fingers on the TPR of the patient, and instructed the patient to maintain the TPR with maximum force against the downward pressure of SLP’s fingers
The whole tongue	To increase the whole tongue flexibility	1.Tongue passive motor function training: SLP wrapped the patient’s tongue with gauze and pulled it forward, including up, down, left and right directions.The patient complete 10 repetitions of elevation (up), 10 repetitions of depression (down), 10 repetitions of lateralization to the right (right) and 10 repetitions of lateralization to the left (left).
	To increase the tongue muscle fibre (Guangzhou Longzhijie Technology Co., LTD. Production of swallowing neuromuscular low-frequency electrical stimulator, model LGT−2350 A.)	2.Low frequency electrical stimulation training: the reference electrode was attached to the posterior skin surface of the seventh cervical vertebra, and the active elctrode provided by the handheld electrode, which was used to stimulate the patient’s mouth and the tongue surface (including the TAR, TCR and TPR areas), and slowly slide back and forth. It has a pulse width of 100us, a frequency of 80 Hz, and an intensity up to the maximum tolerated intensity that causes tongue muscle contraction (Fig. 4).	10 min	1 sessions a day	10 days

Abbreviation TAR, Anterior tongue region; TCR, Center tongue region; TPR, Posterior tongue region; s, second; min, minutes

Fig. 1.

Flow chart of the Intervention Protocol; s,seconds; min, minutes; h,hour

Data collection

The tongue pressure and tongue endurance time before and after treatment were assessed by a flexible nine-site (The precision of each sites can reach 0.15%~0.06%.) tongue pressure sensor developed by our team (Fig. 2). The patients were in a seated position with the head in a neutral position in a quiet treatment room. The head position was kept constant during the examination. The assessor sits laterally to the patients and explains the purpose and methods of the examination (Fig. 3a). Before the formal measurement, a complete practice was performed to ensure that the patient mastered the tongue pressure measurement method. A custom-made disposable film was used to wrap the sensor pad and placed on the surface of the tongue. The patient were then instructed to bite the first soft ring and hold the handle by themselves or the therapist to help them to hold the handle. Instructions were given on a flat panel monitor, providing guidance on how to perform the tongue pressure test and how to measure the tongue endurance time. Measurements were not recorded until the patient had completed the procedure instructions. After three tests had been completed, the maximum pressure value, the unit of pressure is kilopascals (kPa). Patients could rest for 15s between the two stress tests. The maximum tongue endurance time, the unit of endurance time is seconds(s). Patients could rest for 30s between endurance time tests. The tongue endurance time was defined as the time that the patient’s tongue pressure value was maintained at more than 50% of the maximum tongue pressure value [27]. At each site was displayed on the table (Fig. 3b and c). The maximum tongue pressure value and maximum tongue pressure endurance time of each patient were recorded before and after segmental tongue function training. The maximum tongue pressure and tongue endurance time were measured at 8 am before the first and the day after the last tongue strengthening training, respectively, to ensure consistent tongue muscle status.

Fig. 2.

A new flexible nine-sites tongue pressure sensor, which includes three parts (TAR, TCR, and TPR. S1 to S3 represent the three sites in the TAR part, similarly S4 to S6 represent the TCR part, and S7 to S9 represent the TPR part). A soft ring with teeth to hold was set in front of the sensor

Fig. 3.

a Tongue pressure measurement: The patients were in a seated position with the head in a neutral position in a quiet treatment room. The head position was kept constant during the examination. The assessor sits laterally to the patients and explains the purpose and methods of the examination. b and c The results were transmitted to a tablet computer monitor in real-time and recorded.(b) test results of maximum tongue pressure; (c) test results of maximum tongue pressure endurance time. TAR, TCR and TPR are shown from top to bottom. Endurance time was scaled in seconds

Fig. 4.

Low frequency electrical stimulation training: the reference electrode was attached to the posterior skin surface of the seventh cervical vertebra, and the active elctrode provided by the handheld electrode, which was used to stimulate the patient’s mouth and the tongue surface (including the TAR, TCR and TPR areas), and slowly slide back and forth

All assessments were performed by a SLP with 8 years of experience to ensure the accuracy of the measurement data.

Data analysis

The measurement site design for this study was based on a previous research that found no notable variation in muscle fiber composition between the left, middle and right sides of the TAR, TCR and TPR. However, there were differences observed in muscle fibers from the anterior, middle and posterior parts of the tongue [28, 29]. To accurately capture these differences, the oral tongue was divided into three parts: TAR, TCR, and TPR [30]. Each part was further subdivided into three sites, with S1 to S3 representing TAR, S4 to S6 representing TCR, and S7 to S9 representing TPR (Fig. 3). The results obtained from the measurements were displayed on a tablet computer in real-time and recorded for analysis.

Tongue pressure measurement

The defined pressure at each part (Px) was determined by calculating the average of the maximal tongue pressure obtained from the three tests.P_TAR represents the mean maximum tongue pressure at the TAR part; P_TCR represents the mean maximum tongue pressure at the TCR part; P_TPR represents the mean maximum tongue pressure at the TPR part. The P_TAR, P_TCR and P_TPR were compared before and after segmental tongue function training [31].

Endurance time

The average endurance time of each section (ETx) was determined by calculating the average of endurance times obtained from three tests. ET_TAR represents the mean maximum tongue endurance time of TAR part; ET_TCR represents the mean maximum tongue endurance time of TCR part; ET_TPR represents the mean maximum tongue endurance time of TPR part. The ET_TAR, ET_TCR and ET_TPR were compared before and after segmental tongue function training [27].

Statistical analysis

The statistical analyses for this study were conducted using SPSS 25.0 software. The paired T-test was used to compare the differences in tongue pressure and endurance time before and after treatment. The tongue pressure parameters (TAR, TCR, TPR) and endurance time parameters (TAR, TCR, TPR) all followed a normal distribution. The significance level for statistical significance was set at a P-value < 0.05.

Results

The data on P_TAR,P_TCR,P_TPR,ET_TAR,ET_TCR and ET_TPR were recorded before and after the treatment, and the results are presented in Table 3. After the treatment, there was a significant increase in P_TAR (P < 0.01) and P_TCR (P < 0.05). However, there were no significant changes in P_TPR, ET_TAR,ET_TCR and ET_TPR following the treatment (P > 0.05).

Table 3.

Assessment results before and after treatment (paired t-tests)

	Before	After	t-value	P-value
PTAR(kPa)	13.88 ± 3.55	26.17 ± 5.52	-3.353	0.004
PTCR(kPa)	10.58 ± 2.80	15.27 ± 3.51	-2.265	0.037
PTPR(kPa)	9.72 ± 3.51	9.01 ± 1.54	0.241	0.813
ETTAR (s)	29.13 ± 7.87	21.82 ± 8.10	1.106	0.284
ETTCR (s)	23.54 ± 7.44	18.01 ± 4.97	1.074	0.298
ETTPR (s)	9.57 ± 2.75	17.96 ± 5.67	-1.565	0.136

Abbreviation P_TAR, anterior tongue region pressure; P_TCR, central tongue region pressure; P_TPR, posterior tongue region pressure; ET_TAR, anterior tongue region endurance time; ET_TCR, central tongue region endurance time; ET_TPR, posterior tongue region endurance time; kPa, kilopascal; s,seconds

Discussion

Abnormal maximum tongue pressure and tongue endurance time are common complications of patients with NPCR. Segmental intensive tongue function training, based on quantitative analysis of tongue pressures in different regions, might be helpful. Our results showed that two weeks of segmental tongue function training could improve P_TAR and P_TCR due to NPCR patients with dysphagia, except for tongue endurance time. It suggests that tongue strengthening training can be used as a rehabilitation treatment for patients with dysphagia in NPCR.

Segmental tongue function training can improve the tongue pressure of TAR and TCR

One of main syndromes in NPCR patients with dysphagia is inadequate food transport due to reduced tongue pressure [32]. Our results showed that two weeks of intensive tongue movement training increased pressure at TAR and TCR, but not at TPR. Some studies have showed that TAR suction cotton swab training [21, 24, 25], TCR resistance training [21] and Low frequency electrical stimulation [15, 33] could increase tongue muscle strength. The possible reason for this result is that TAR and TCR are mainly composed of type II fast muscle fibers [33]; whereas muscle fibers in the TPR region were primarily type I. Type II muscle fibers might be more sensitive to training and contribute to greater muscle strength. Type I muscle fibers require longer loading times in order to stimulate muscle fiber growth [34]. Additionally, slow muscle fibers in the TPR region have a shorter half-life and more susceptible to radiation therapy, which could lead to more serious muscle atrophy of posterior tongue. Therefore we considered that it would take longer for muscle strength to increase in the TPR region. Another possible reason for the observed phenomenon is the relatively independent movement of different parts of the tongue [35, 36]. During swallowing, there is a change in lingual delivery pressure gradient from the front to the back. Further research has indicated that during swallowing exercise, the movement of TAR and TCR is more easily triggered, and the associated muscles are more readily activated [33]. In addition, the pressures exmaination in this study is measured during tongue upward movement, When tongue moves upward, not all TPR fibers are recruited [37, 38], while TAR and TCR fibers were more likely to be recruited.

Segmental tongue function training can not improve the tongue endurance time

Scardella AT et al. [39] and Robin DA et al. [40] found that the tongue endurance time decreased with increasing tongue muscle strength in normal participants. However, our previous study showed that maximal tongue endurance at different of sites instead prolonged patients with NPCR compared to normal populations, which represent an adaptive compensation [41]. Our results showed that short-term tongue strengthening training in NPCR patients could increase TAR and TCR pressure, but there was no significant change in endurance time. The possible reasons were as follows: Our prescription for tongue-strengthening exercises was for short periods of repetitive exercises, while the adaptation for endurance training required long periods of repetitive exercises [42]. Although tongue pressures increased after training, the overall tongue drive was still lower than that of the healthy population. The longer tongue endurance in NPCR patients may still be an adjusting strategy. These are beneficial for increasing the effectiveness and safety of swallowing. We still don’t know whether long-term continuous high-intensity training could effect tongue endurance, which might be our future research.

Limitations

This study acknowledges several limitations. Firstly, the small sample size prevents the findings from being fully representative of all levels of NPCR dysphagia. More extensive data collection is necessary to conduct further studies according to the severity of patient dysfunction. Secondly, the current research is restricted in its ability to accurately determine the optimal timing for rehabilitation interventions and the duration of rehabilitation for tongue pressure and tongue endurance in NPCR patients. Based on our previous research and clinical experience, the best time to start rehabilitation for patients with NPCR dysphagia may be when the articulation is slightly unclear. Thirdly, the lack of uniformity in the hospitals where radiotherapy was conducted prevented the researchers from obtaining crucial information such as TNM characteristics of the tumor, radiation dosage, and irradiation site. Fourthly, the absence of a control group limits the ability to assess the effectiveness of each specific treatment within the tongue intensification protocol. Finally, there is a need to validate the maintenance of the achieved results in the medium to long term.

In conclusion, enhanced tongue motor function training can increase tongue pressure at TAR and TCR in NPCR patients, which can be further promoted and applied in clinical practice.

Author contributions

All authors contributed to the study conception and design.Conceptualization: [XCQ]. [WHM].Methodology: [WXM]. [YC]. Assessment: [ZF]. Formal analysis and investigation: [ZYW]. [SSM].Writing - original draft preparation: [ZF]. Writing - review and editing: [ZF], [XCQ]. Funding acquisition: [DZL]. Supervision: [WXM]

Funding

This study was funded by Guangzhou Key Field Research and Development Plan (Grant No. 202007030001).

Data availability

The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

Declarations

Ethics approval and consent to participate

The study was approved by the Third Affiliated Hospital of Sun Yat-sen University (Approval No: CUHK Attached SAN Medical Ethics [2021]02-200-01) and was conducted according to the principles of the Declaration of Helsinki. Written informed consent was obtained from all participants.

Consent for publication

All participants and/or their legal guardian(s) have given informed consent for their identifying information/images to be published in online open-access publications.

Competing interests

The authors declare no competing interests.