Archives of Oral Biology 108 (2019) 104521

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Archives of Oral Biology

journal homepage: www.elsevier.com/locate/archoralbio

Tongue stretching exercises improve tongue motility and oromotor function T

in patients with dysphagia after stroke: A preliminary randomized
controlled trial
Na-Kyoung Hwanga, Hwan-Hee Kimb, Je-Myung Shimc, Ji-Su Parkd,
⁎

a
Department of Occupational Therapy, Seoul North Municipal Hospital, Seoul, Republic of Korea
b
Department of Occupational Therapy, Semyung University, Jecheon, Republic of Korea
c
Department of Physical Therapy, Kangwon National University, Samcheok, Republic of Korea
d
Advanced Human Resource Development Project Group for Health Care in Aging Friendly Industry, Dongseo University, Busan, Republic of Korea

ARTICLE INFO ABSTRACT

Keywords: Objectives: This study investigated the effect of tongue stretching exercises (TSE) on tongue motility and or-
Oral dysphagia omotor function in patients with dysphagia after stroke.
Oromotor Design: This study was designed as a 4-week, double-blind, two-group, block randomized controlled trial. A total
Function of 25 patients were randomly allocated into either the experimental (n = 13) or the control group (n = 12). The
Muscle stretching exercises
experimental group received TSE from an occupational therapist. TSE were divided into dynamic and static
Swallowing
Videofluoroscopic
passive stretching exercises (20 repetitions each). The intervention was performed five times a week for four
Swallowing study weeks. Tongue motility was measured before and after the intervention as the distance from the lower lip to the
Tongue tip of tongue during maximum protrusion of the tongue. Measurements were performed twice each time and the
Motility mean value recorded. Oromotor function was assessed using the oral phase events of the videofluoroscopic
dysphagia scale (VDS) based on a videofluoroscopic swallowing study.
Results: The experimental group showed significant differences in tongue motility, bolus formation, tongue to
palate contact, premature bolus loss, and oral transit time in the oral phase of VDS (p < 0.05 for all) before and
after the intervention, whereas the control group showed a significant difference only in lip closure (p < 0.05).
Conclusion: This study demonstrated that TSE have a positive effect on tongue motility and oromotor function in
patients with dysphagia after stroke. Therefore, we recommend TSE as an effective treatment for dysphagia.

1. Introduction
The oral phase of the swallowing process is the only phase that can
be actively controlled. The tongue is a representative structure in the
oral phase, and its functions are primarily to support bolus formation,
chewing, and transport of the bolus to the pharynx (Yano et al., 2019;
Youmans, Youmans, & Stierwalt, 2009). To fulfil these functions in the
oral phase, sufficient strength and motility of the tongue are important.
In neurological disorders such as stroke, skeletal muscle may de-
velop myopathic conditions such as paralysis, weakness, and short-
ening, which lead to functional limitations (Knarr, Reisman, Binder-
Macleod, & Higginson, 2013; Little, McGuirk, & Patten, 2014). The
tongue as a skeletal muscle is frequently affected by these problems,
which can negatively affect oromotor function (Kim et al., 2017). In
particular, weakening and shortening of the tongue can cause oral
dysphagia by limiting its motility. Therefore, it is clinically important to
identify effective intervention methods for improving tongue function
in patients with dysphagia.
Previous studies have emphasised the importance of tongue strength
and motility in patients with oral dysphagia (Kim et al., 2017;
Murakami et al., 2015; Robbins et al., 2007; Steele et al., 2016). Tongue
strength directly affects normal swallowing and is known to be an
important predictor of oral function in dysphagia patients (Lee et al.,
2016). Recently, Murakami et al. (2015) reported that the swallowing
function is closely associated with tongue motility. Sufficient strength
and motility of the tongue are both important factors to improve the

Abbreviations: TSE, tongue stretching exercises; VFSS, videofluoroscopic swallowing study; VDS, videofluoroscopy dysphagia scale; ROM, range of motion; TDT,
traditional dysphagia treatment; GTO, Golgi tendon organ
⁎
Corresponding author at: Advanced Human Resource Development Project Group for Health Care in Aging Friendly Industry, Dongseo University, 47, Jurye-ro,
Sasang-gu, Busan, Republic of Korea.
E-mail address: jisu627@hanmail.net (J.-S. Park).

https://doi.org/10.1016/j.archoralbio.2019.104521
Received 3 May 2019; Received in revised form 3 August 2019; Accepted 10 August 2019
0003-9969/ © 2019 Elsevier Ltd. All rights reserved.
N.-K. Hwang, et al. Archives of Oral Biology 108 (2019) 104521

swallowing function of patients with dysphagia. However, studies on

tongue function in patients with dysphagia have focused mostly on
improving the strength of the tongue (Kim et al., 2017; Robbins et al.,
2007).
Although TSE are commonly used in clinical practice to reduce
shortening and increase the motility of the tongue as well as to improve
overall oromotor function, there are no studies on the effect of this
intervention. The purpose of this study was to investigate the effects of
TSE on tongue motility and oromotor function in patients with dys-
phagia after stroke. The first hypothesis of this study is that TSE will
increase tongue motility. The second hypothesis is that this will have a
positive impact on oromotor function.

2. Materials and methods

2.1. Subjects

Stroke patients with dysphagia (n = 25) were recruited from the

oropharnygeal dysphagia clinic of a university hospital in South Korea.
Fig. 1. Tongue stretching exercises.
The inclusion criteria for participation were as follows: oropharyngeal
dysphagia after stroke confirmed by a videofluoroscopic swallowing
study (VFSS), duration of dysphagia < 3 months, and ability to swallow 2.4. Outcome measurements
voluntarily. Exclusion criteria were: trigeminal neuropathy, significant
tongue deviation or facial asymmetry, parafunctional habits (e.g., The motility of the tongue and the oromotor function was measured
clenching, bruxing, tongue thrusting), and communication disorders. We in all patients before and after the intervention. Tongue motility was
explained the objectives and requirements of our study to all partici- measured using the distance from the lower lip to the maximum pro-
pants, and they voluntarily signed informed consent forms. Ethical ap- trusion point of the tip of the tongue during the active movement based
proval was obtained from the Semyung University Institutional Review on the method used in a previous study (Lazarus et al., 2014) (Fig. 2).
Board before conducting the study (SMU-2016-12-001). On both occasions, measurements were taken two times and the mean
value in millimetres recorded. Tongue motility was measured by an
occupational therapist with three years of clinical experience.
2.2. Procedures
The VDS is a comprehensive swallowing assessment based on the
VFSS findings. The VDS is divided into the oral phase (seven items: lip
A total of 25 patients were randomly allocated into either the ex-
closure, bolus formation, tongue-to-palate contact, mastication,
perimental (n = 13) or the control group (n = 12) by blocked rando-
apraxia, premature bolus loss, and oral transit time) and the pharyngeal
mization. The allocation sequence was generated via a web-based
phase (seven items: pharyngeal triggering, vallecular residues, pyriform
randomization tool (http://www.randomizer.org/) by an occupational
sinus residues, laryngeal elevation, pharyngeal wall coating, phar-
therapist blinded to the patients. Both groups received TDT by occu-
yngeal transit time, and aspiration) (Kim et al., 2014) (Table 1). Or-
pational therapists. TDT included oral facial massage, thermal-tactile
omotor function during swallowing was assessed based on the sequence
stimulation, and compensatory skill straining.
of events during the oral phase of the VDS. The analysis of VDS based
In addition, the experimental group practised the following TSE:
First, the patient was asked to stick the tongue out of their mouth while
they were sitting in a comfortable position in a chair or wheelchair. The
therapist would then use a dry gauze to hold the tongue tightly with
both hands. The TSE were divided into dynamic and static passive
stretching exercises. For the dynamic passive stretching, the therapist
pulled the patient's tongue to the end feel point of the ROM, where the
tongue was maximally out of the mouth, and held it there for about
2–3 s before gently guiding it back into the mouth. For the static passive
stretching exercise the therapist also pulled the tongue to the end feel
point but held it for about 20 s before allowing it to glide back (Fig. 1).
Both dynamic and static passive stretching was performed 20 times per
day, which was set based on our pilot trial. The intervention was per-
formed five times a week for four weeks. Assessments regarding tongue
motility and oromotor function were conducted by an occupational
therapist and a rehabilitation physician blind to treatment allocation.

2.3. Videofluoroscopic swallowing study

A VFSS was performed to analyse oromotor function. Participants

sat in an upright position at a about 1.5 m distance from the X-ray tube,
with the head stabilised. The subjects were given boiled rice. Lateral
fluoroscopic projection of swallowing was recorded at 30 frames per
second.
VFSS were performed immediately before the start of the inter-
vention (pre-training), and after 4 weeks of treatment (post-training). Fig. 2. Tongue motility measurement.

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N.-K. Hwang, et al. Archives of Oral Biology 108 (2019) 104521

Table 1 tongue motility between the two groups after the intervention (p =
Videofluoroscopic dysphagia scale. 0.108) (Table 3). However, when comparing the amount of change in
Parameter Findings Parameter Findings motility of the tongue between both groups, significant differences were
observed (p < 0.001) (Table 4).
LC Intact 0 TPS Normal 0
Inadequate 2 Delayed 4.5 3.3. TSE effects on oromotor function
None 4
BF Intact 0 VR None 0
Inadequate 3 < 10% 2 The experimental group showed a significant difference in bolus
None 6 10–50% 4 formation, tongue-to-palate contact, premature bolus loss, and oral
> 50% 6 transit time after as compared to before the intervention (p = 0.002,
Mastication Intact 0 LE Normal 0
0.008, 0.016, and 0.031, respectively). On the other hand, the control
Inadequate 4 Delayed 9
None 8 group showed no significant difference after as compared to before the
Apraxia None 0 PSR None 0 study period except for lip closure (p = 0.031). There was a significant
Mild 1.5 < 10% 4.5 difference in bolus formation between both groups after the interven-
Moderate 3 10–50% 9 tion (p = 0.017) (Table 3). In a comparison of the amount of change in
Severe 4.5 > 50% 13.5
TPC Intact 0 CPW No 0
oromotor function between both groups, no significant differences were
Inadequate 5 Yes 9 observed (p > 0.5) (Table 4).
None 10
PBL None 0 PTT < 1.0s 0 3.4. Side effects related to TES
< 10% 1.5 > 1.0s 6
10-50% 3
> 50% 4.5 No patient reported tongue muscle pain, fatigue or discomfort
OTT < 1.5s 0 Aspiration None 0 during or after the completion of the TSE in the experimental group.
> 1.5s 3 Penetration 6
Aspiration 12 4. Discussion
LC: Lip Closure, BF: Bolus Formation, TPC: Tongue to palate contact, PBL:
Premature bolus loss, OTT: Oral transit time, TPS: Triggering of pharyngeal
Motor dysfunction of the tongue after stroke can cause various
swallow, VR: Vallecular residue, LE: Laryngeal elevation, PSR: Pyriform sinus problems. Shortening of the tongue muscles restricts its motility in the
residue, CPW: Coating on the pharyngeal wall, PTT: Pharyngeal transit time. oral phase of swallowing, negatively affecting chewing, and control and
formation of the bolus. Restoring or maintaining adequate motility of
on the VFSS was performed by an experienced occupational therapist the tongue is important for safe swallowing (Daniels, Brailey, &
together with are rehabilitation physician. Foundas, 1999; Nakamori et al., 2016). This study investigated the ef-
fects of TSE on tongue motility and oromotor function in patients with
dysphagia after stroke.
2.5. Statistical analysis
In our study, tongue protrusion increase by 4.1 mm and 1.3 mm in
the experimental group and control group, respectively, corresponding
The statistical analyses were performed using SPSS Statistics for
to 20% and 5%, respectively, of the original ROM. The soft tissue of the
Windows version 15.0 (SPSS Inc., Chicago, IL, USA). Descriptive sta-
tongue is mainly composed of skeletal muscle that reacts in a specific
tistics are presented as means with standard deviations. The Shapiro-
way to elongation such as stretching, which may have a positive effect
Wilk test was used to check normality of the outcome variables. To
on the motility of the tongue. Stretching generally aims to increase the
evaluate the intervention effects, the Wilcoxon signed-rank test was
distance between the origin and insertion of a muscle, thereby in-
used to compare measures pre- and post-intervention in each group.
creasing the length of the musculotendinous unit (Witvrouw, Mahieu,
The Mann-Whitney U test was used to compare the intergroup changes
Danneels, & McNair, 2004).
in outcome measures. The significance level was set at p < 0.05. Effect
Muscles are immobilized in a contracted state, muscle length is
sizes (Cohen’s d) were calculated by dividing the standardized mean
decreased, extensibility is reduced, and passive viscoelastic stiffness is
difference between the two groups by the pooled standard deviation for
increased (Gajdosik, 2001; Prentice, 2015). After a stroke, the skeletal
the data. An effect size of 0.2, 0.5 and 0.8 represents a small, moderate
muscles including the tongue remain contracted for a long time, and the
and large effect, respectively.
resulting deterioration further shortens the length of the muscles and
eventually decreases the ROM and increases stiffness. Previous studies
3. Results have shown that long-term sustained stretching of the muscles after
stroke is effective in increasing muscle elongation and flexibility, de-
3.1. Participants creasing stiffness and, consequently, in increasing the ROM (Abdel-
aziem, Draz, Mosaad, & Abdelraou, 2013; Knudson, 1999).
A total of 21 participants completed this study. Four participants When stretching lasts for at least six to eight seconds, the GTO as a
dropped out prior to the follow-up examination because of discharge stretch receptor becomes activated because the pulled muscle stretches
from the hospital (Fig. 3). A summary of the clinical and demographic the tendon (Hindle, Whitcomb, Briggs, & Hong, 2012). The high fre-
features of the subjects (n = 21) is shown in Table 2. No significant quency and speed of the discharge from the GTO inhibits the stimulus of
differences in the baseline characteristics were observed between the the secondary sensory neurons the muscle spindle. The stimulus from
experimental and the control group (p > 0.05). the GTO relaxes the muscle reflexively with increasing muscle tension,
which overwhelms the stimulus of the muscle spindle, the stimulus of
3.2. TSE effects on motility of the tongue the muscle spindle is gradually decreased, and inhibits the alpha motor
neuron that innervates the extrinsic fibres (Guissard & Duchateau,
The motility of the tongue was significantly different before 2006; Prentice, 2015). Thus, the contracted muscle is gradually relaxed,
(25.9 ± 8.6 mm) and after the intervention (30.0 ± 8.4 mm) in the resulting in a stretching effect. Moreover, owing to muscle physiology,
experimental group (p = 0.001). On the other hand, there was no stretching can decrease muscle stiffnessbyinducing an increase in cal-
significant difference in the control group (24.9 ± 11.0 mm and cium ions (Ca+) within the neuromuscular junction and promoting
26.2 ± 11.8 mm; p = 0.072). There was no significant difference in sarcomerogenesis (De Deyne, 2001; Yamashita, Ishii, & Oota, 1992). All

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N.-K. Hwang, et al. Archives of Oral Biology 108 (2019) 104521

Fig. 3. CONSORT diagram of participant recruitment.

Table 2 tongue motility through stretching may have influenced these essentials
Characteristics of participants. of oral motor function, especially the coordination of the oral muscles.
Characteristics Experimental group Control group In this study, regular TSE in the experimental group resulted in
(n = 11) (n = 10) significant improvements in bolus formation, tongue-to-palate contact,
premature bolus loss, and oral transit time. These events are all related
Age (year) 60.5 ± 12.5 62.2 ± 10.3
to tongue motility in the oral phase. Adequate strength and motility of
Gender(n)
Men 6 5
the tongue are especially important for bolus formation and tongue-to-
Women 5 5 palate contact (Clark, Henson, Barber, Stierwalt, & Sherrill, 2003; Lee
Time since onset of stroke, 8.2 ± 2.9 9.1 ± 2.7 et al., 2016). During the oral phase of the swallowing process, a bolus is
weeks appropriately shaped by continuous movements of the tongue. Tongue-
Type of stroke (n)
to-palate contact then moves the bolus to the tongue base to be swal-
Hemorrhage 7 6
Infarction 4 4 lowed (Matsuo & Palmer, 2008). Therefore, adequate motility of the
Paretic side (n) tongue may directly affect oromotor function.
Right 8 7 This study has some limitations. First, it is difficult to generalize the
Left 3 3
results of this study, because the sample size was small. Second, there is a
possibility that there is an error related to the measurement of tongue
Mean ± standard deviation.
motility. Because we did not confirm the inter-rator reliability of the
tongue motility measure. Third, this study was conducted on a only 4 -
these factors may collectively contribute to an enhancement in motor week schedule, so the intervention period was rather short. It is therefore
performance after stretching. This theoretical evidence supports the necessary to observe changes in effects through further intervention
results of this study. time. Finally, this study has difficulties in quantitative measurement
Oromotor function includes muscle tone, muscle strength, ROM because of the oromotor function measurement using the oral phase item
(ability to move specific structures independently of each other) and the of VDS, and there is a limitation in the validity of the evaluation.
coordination of many muscles including the tongue, the orbicularis oris,
masseter, and buccinator (Morris & Klein, 2000; Pu, Murry, Wong, Yiu, & 5. Conclusion
Chan, 2017). Stretching is known to be an effective method that im-
proves performance and flexibility by releasing tension in and increasing The results of this study demonstrate that TSE has a positive effect
the length of the muscle (Witvrouw et al., 2004). In this study, increased on motility of the tongue and oromotor function in patients with

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N.-K. Hwang, et al. Archives of Oral Biology 108 (2019) 104521

Table 3
Changes in parameters before and after treatment.
Experimental group Control group Comparison between group after Cohen’d
intervention
Before After p-value Before After p-value

Tongue motility (unit: cm) Oromotor 2.59 ± 0.86 3.00 ± 0.84 0.001* 2.49 ± 1.10 2.62 ± 1.18 0.072 0.108 0.28
function
LC 2.00 ± 1.26 1.27 ± 1.01 0.063 2.80 ± 1.03 1.80 ± 0.63 0.031* 0.185 −0.3
BF 3.55 ± 1.81 1.09 ± 1.51 0.002* 3.90 ± 1.45 2.70 ± 0.95 0.063 0.017† 0.98
Mastication 2.55 ± 2.02 1.09 ± 1.87 0.063 2.40 ± 2.07 1.20 ± 1.93 0.125 0.633 0.13
Apraxia 0.00 ± 0.00 0.00 ± 0.00 1.000 0.00 ± 0.00 0.00 ± 0.00 1.000 1.000 0
TPC 5.00 ± 3.87 1.36 ± 2.34 0.008* 3.50 ± 2.42 2.00 ± 2.58 0.125 0.438 1.24
PBL 1.77 ± 1.31 0.82 ± 0.78 0.016* 1.80 ± 1.18 1.20 ± 0.95 0.063 0.266 0.4
OTT 2.18 ± 1.40 0.82 ± 1.40 0.031* 1.50 ± 1.58 0.90 ± 1.45 0.250 0.633 0.53

Mean ± standard deviation.

*p < 0.05 by Wilcoxon test, †p < 0.05 by Mann-Whitney U test.
LC: lip closure, BF: bolus formation, TPC: tongue to palate contact, PBL: premature bolus loss, OTT: oral transit time, ES: effect size.

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