Application of ultrasonography in assessing oropharyngeal Dysphagia in stroke patients.
ABSTRACT This study applied submental ultrasonography (SUS) to measure changes in dysphagic stroke patients' tongue thickness and hyoid bone displacement when swallowing 5 mL of water and correlated the results with the severity of clinical dysphagia. We included 60 stroke patients (30 tube-feeding-dependent and 30 on regular oral intake) and 30 healthy controls. An additional 10 healthy people were recruited to assess the reliability of SUS. Measurements of hyoid bone displacement using videofluoroscopic swallowing study (VFSS) and SUS were compared for 12 stroke patients to assess the correlation between the two methods. Changes in tongue thickness and hyoid bone displacement were significantly less in the tube-feeding group. Those with a tongue thickness change of less than 1.0 cm and hyoid bone displacement of less than 1.5 cm were likely to be tube-feeding. SUS showed good intra-rater/inter-rater reliability and correlated well with VFSS measurement. SUS can be an adjunct assessment tool of swallowing.
d Original Contribution
APPLICATION OF ULTRASONOGRAPHY IN ASSESSING OROPHARYNGEAL
DYSPHAGIA IN STROKE PATIENTS
MING-YEN HSIAO,* YEUN-CHUNG CHANG,yWEN-SHIANG CHEN,* HUI-YA CHANG,z
and TYNG-GUEY WANG*
*Department of Physical Medicine and Rehabilitation;yDepartment of Medical Imaging, National Taiwan University Hospital
and National Taiwan University College of Medicine, Taipei City, Taiwan, ROC; andzDepartment of Rehabilitation,
Puli Christian Hospital, Nantou, Taiwan, ROC
(Received 16 February 2012; revised 5 April 2012; in final form 24 April 2012)
AbstractThis study applied submental ultrasonography (SUS) to measure changes in dysphagic stroke patients’
tongue thickness and hyoid bone displacement when swallowing 5 mL of water and correlated the results with
the severity of clinical dysphagia. We included 60 stroke patients (30 tube-feeding-dependent and 30 on regular
oral intake) and 30 healthy controls. An additional 10 healthy people were recruited to assess the reliability of
SUS. Measurements of hyoid bone displacement using videofluoroscopic swallowing study (VFSS) and SUS were
compared for 12 stroke patients to assess the correlation between the two methods. Changes in tongue thickness
intra-rater/inter-rater reliability and correlated well with VFSS measurement. SUS can be an adjunct assessment
tool of swallowing. (E-mail: email@example.com, firstname.lastname@example.org)
Medicine & Biology.
? 2012 World Federation for Ultrasound in
Key Words: Ultrasound, Dysphagia, Stroke.
Oropharyngeal dysphagia is a common complication of
stroke. Previous studies have shown that one-fourth to
half of all stroke patients develop dysphagia (Gordon
et al. 1987; Smithard et al. 1996; Mann 2002), which
can result in aspiration pneumonia, malnutrition and
dehydration. Dysphagia also impedes long-term func-
tional recovery and increases mortality (Gariballa et al.
1998; Sellars et al. 2007; Smithard et al. 2007). Objective
assessment of dysphagia facilitates determining whether
a patient must depend on tube feeding. Further clarifica-
tion between the oral or pharyngeal phase of dysphagia
may help additional management.
Clinical swallowing evaluations, videofluoroscopic
the swallowing function of dysphagic patients. Clinical
evaluations lack sufficient diagnosing accuracy and sensi-
tivity (Smithard et al. 1998; Martino et al. 2000). VFSS is
geal dysphagia (Logemann 1997). However, the radiation
exposure and the need to transport stroke patients limit
the use of VFSS in certain conditions. Furthermore, the
results of VFSS must be interpreted carefully because
tion. FEES, although portable and radiation-free, is an
invasive and less quantitative procedure.
Ultrasonography has long been used to evaluate the
swallowing process but without conclusive results
(Shawker et al. 1983, 1984; Stone and Shawker 1986;
Sonies et al. 1996; Yang et al. 1997; Kuhl et al. 2003).
ing function showed decreased tongue movement and/or
larynx elevation in the group of dysphagia (Shawker
et al. 1983; Sonies et al. 1996; Yang et al. 1997; Kuhl
et al. 2003). However, these studies did not recommend
quantitative measurements for diagnosing dysphagia.
With a diagnostic cut-off value, submental ultrasonog-
Address correspondence to: Tyng-Guey Wang, MD, Department
of Physical Medicine and Rehabilitation, E-mail: email@example.com;
and Yeun-Chung Chang, MD, PhD, Department of Medical Imaging,
National Taiwan University Hospital, No.1, Changde Street, Zhongz-
heng District, Taipei City 10048, Taiwan, ROC. E-mail: ycc5566@
Ultrasound in Med. & Biol., Vol. -, No. -, pp. 1–7, 2012
Copyright ? 2012 World Federation for Ultrasound in Medicine & Biology
Printed in the USA. All rights reserved
0301-5629/$ - see front matter
sonography provide additional information to help clini-
cians understand the complex swallowing function of
a patient. Therefore, this study attempted to determine
the cut-off value of larynx elevation and the change in
tongue thickness for defining the severity of dysphagia
when assessing the swallowing function of stroke patients
by submental ultrasonography.
MATERIALS AND METHODS
We recruited 60 stroke patients and 40 healthy
participants for the study sample. This study was
approved by the Ethics Committee of the university
hospital. Written informed consent was obtained from
September 2011, patients admitted to rehabilitation
wards that were conscious and cooperated adequately
were recruited to this study. A stroke was defined accord-
ing to criteria established by the World Health Organiza-
tion based on computed tomography and magnetic
resonance imaging evidence. Participants’ basic data,
location of stroke, lesion characteristics and the duration
from stroke onset to ultrasonographic examination were
recorded. Participants underwent a clinical examination
by a speech therapist, who graded them using the func-
tional oral intake scale (FOIS). FOIS was designed with
good reliability, validity and sensitivity to changes in
swallowing function to document the functional oral
intake of stroke patients (Crary et al. 2005). In this study,
30 of the stroke patients were graded as dependent on
tube feeding (FOIS 1–3) and the other 30 were graded
as having oral intake (FOIS 4–7). Thirty age-matched
healthy participants were recruited as the control. Addi-
tionally, 10 healthy adults were recruited and underwent
four submental ultrasonographic examinations per-
formed by two examiners to evaluate the intra-rater and
inter-rater reliability of the submental ultrasonography.
Ultrasonographic examinations on 90 participants
were performed by one of the study authors. Repeated
examinations by another author were conducted on the
tal ultrasonographic examination. Both examiners had
undergone 1 month of training. This study used a self-
designed ultrasound machine with a curvilinear trans-
ducer (BS3C673 Convex Array, 3.5MHz, BSUS20-32C;
Broadsound Corporation, Taiwan). The machine was
be used easily at the bedside (Fig. 1a). Images were
recorded at a frame rate of 22.5 per second.
able upright position, with their heads leaning on thewall
or on the chair back. The transducer was placed in the
midsagittal plane in the submental area, with the trans-
ducer minimally touching the submental area. The trans-
ducer was manually positioned using the technique
described by Stone (2005) (Fig. 1b). Participants were
Fig. 1. Submental ultrasonographicexamination.(a)Self-designedultrasoundmachinewitha3.5MHzcurvilineartrans-
ducer. (b) Technique for holding the transducer. The thumb should be placed at the mandible angle and the index finger at
the mental protuberance. The transducer is held in thevertical midsagittal plane using the third and fourth digits. (c) Sub-
mental midsagittal ultrasonography image with acoustic shadows behind the hyoid bone (white arrow) and the mandible
(black arrow); between them is the suprahyoid muscles (between the black arrowheads). The bolus is held in front of the
tongue (between the white arrowheads). The palate is also visible (asterisk).
2Ultrasound in Medicine and BiologyVolume -, Number -, 2012
instructed to hold their head steady when swallowing.
Each participant swallowed 5 mL of water for each
attempt. Their tongue motion and hyoid bone movement
when swallowing was recorded. The recorded images
were analyzed in single frames to determine the
maximum change in tongue thickness and hyoid bone
Figure 1c shows the structures observed in the sub-
mental midsagittal ultrasonography images. Mandible
and hyoid bones appear as two hyperechoic areas with
acoustic shadows. To measure tongue thickness, we bi-
sected the angle formed by the acoustic shadows of the
hyoid and mandible, before measuring tongue thickness
images and changes in tongue thickness were calculated.
The mandible was used as the reference point to
calculate the hyoid bone displacement (Fig. 2b). Using
a two-axis coordinate system, the position of the hyoid
bone in relation to the mandible in each frame was repre-
sented as coordinate pairs. The distance between two
coordinates before and during swallowing denote the
hyoid bone displacement (Fig. 2c).
The software employed in this study was developed
using MATLAB (v. 7.5.0, R2007b; The MathWorks, Inc.,
Boston, MA). The measurements were repeated 3 times
for every participant, to obtain mean values for statistical
Videofluoroscopic swallowing study
eofluoroscopic swallowing study (VFSS). VFSSs were
conducted at our institute using fluoroscopic equipment
with a remote control (Medix; Hitachi Medical Corp,
Tokyo, Japan) and a high-resolution super-VHS recorder
(VC BR 1200; Victor Co. of Japan, Yokohama, Japan) at
a frame rate of 30 frames per second. Participants main-
tained good posture by sitting on a specially designed
chair (VFES chair; Vess Chairs Inc., Milwaukee, WI,
USA). During the examination, participants swallowed
5 mL of thin barium sulfate (suspension of 340 g of
E-Z-HD [E-Z-HDT; Bracco Diagnostics Inc., Princeton,
NJ, USA] and 65 mL of water). The anterior superior
margin of the fourth cervical vertebral body was used as
the reference point for calculating hyoid bone displace-
ment. The initial position of the hyoid bone was marked
and the displacement relative to the reference point was
calculated in single frames to determine the maximum
hyoid bone displacement when swallowing.
(SPSS Statistics 12.0; SPSS Inc., Chicago, IL, USA).
Fig. 2. Calculation of tongue thickness change and hyoid bone displacement. (a) Tongue thickness was measured at the
central plane bisecting the angle formed by the acoustic shadows of the hyoid and mandible. (b) The position of the
mandible (black arrow) and the hyoid bone (white arrow) was determined by the intersection of the acoustic shadows
(dash lines) and suprahyoid muscles. Using a two-axis coordinate system, and the mandible as the reference point, the
hyoid bone was designated a pair of coordinates (X1,Y1). (c) During swallowing, the hyoid bone moves upward and
forward into a new position (arrow) designated by (X2, Y2), with the mandible as the reference point. The distance
between the two coordinates before and after swallowing denote the hyoid bone displacement (thin arrow).
Ultrasonography in assessing oropharyngeal dysphagia d M.-Y. HSIAO et al.3
A Mann-Whitney test was used to analyze the results and
bone displacement differed significantly among the tube-
feeding-dependent group, oral feeding group and control
group. A probability value less than .05 indicated statis-
The intra-rater and inter-rater reliability of the
submental ultrasonography measurements of changes in
tongue thickness and hyoid bone displacement were
assessed by determining the intraclass correlation coef-
ficient (ICC) for 10 healthy participants. Hyoid bone
displacement among stroke patients, measuredusing sub-
mental ultrasonography and VFSS, was also compared
with determining their ICC. An ICC of ,0.4 indicated
poor reproducibility. An ICC between 0.4 and 0.75 indi-
cated fair-to-good reproducibility. An ICC of .0.75 indi-
cated excellent reproducibility.
Of the 60 stroke patients (42 men, 18 women, mean age
66 6 11), 41 had an ischemic stroke and 19 had a hemor-
16–177 days). No statistically significant differences ex-
to ultrasonographic examination between the groups
(p . 0.05).
Themeanchangeintonguethickness was1.1 cmfor
and 0.9 cm forthe tube-feeding stroke patients. No differ-
ence existed between the control and the oral intake
group, whereas significant differences were observed
among the tube-feeding-dependent group, the oral intake
group and the control group (Table 2) (Fig. 3a). A tongue
thickness change of less than 1.0 cm as the cut-off point
(criteria1) for detecting
dysphagia (FOIS 1–3) indicated a sensitivity and speci-
ficity of 70.0% and 66.7%, respectively.
encewas observed between the control and the oral intake
group; however, significant differences existed among the
tube-feeding-dependent group, the oral intake group and
ment below 1.5 cm as the cut-off point (criteria 2) for
detecting tube-feeding-dependent dysphagia (FOIS 1–3)
indicated a sensitivity and specificity of 73.3% and
66.7%, respectively. If both criteria were required, the
sensitivity was 63.3% and the specificity was 93.3%. If
only one criterion was required, the sensitivity was
86.7% and the specificity was 40%.
The intra-rater ICC of hyoid bone displacement of
the two examiners was 0.927 and 0.842, respectively;
the inter-rater ICC value between the two examiners
was 0.806. For measurements of changes in tongue thick-
ness, the intra-rater ICC values were 0.758 and 0.661,
respectively, and the inter-rater ICC value was 0.685.
For measurements of hyoid bone displacement, no signif-
icant difference existed between the results provided by
submental ultrasonography and those by VFSS, with
a p value of 0.266 and an ICC value of 0.804.
The results demonstrate that submental ultrasonog-
raphy can aid in bedside assessments of swallowing func-
tion among stroke patients by directly visualizing bolus
Table 1. Basic demographic data*
Group 1 FOIS 1–3
(N 5 30)
Group 2 FOIS 4–7
(N 5 30)
Group 3 normal subjects
(N 5 30)p value
Stroke onset to
67 6 12y(40–85) 64 6 10y(44–82) 63 6 9 (47–78) 0.171
69 6 46 (17–177)45 6 24 (16–110)0.052
FOIS 5 functional oral intake scale.
* Data are presented as mean 6 standard deviation and range (bracket). Statistics were obtained using a Mann-Whitney test for numerical data and
a Fisher’s exact test (c2test) for categorical data (group 1 vs. group 2).
yp . .05 vs. group 3.
4 Ultrasound in Medicine and BiologyVolume -, Number -, 2012
bone displacement in the pharyngeal stage. Severely dys-
icantly low changes in tongue thickness and hyoid bone
displacement. Most of the tube-feeding-dependent stroke
and a tongue thickness change of less than 1.0 cm.
Whether a dysphagic stroke patient can be free of
clinical concern. Swallowing is a complex process and
multifaceted factors on the safety and efficiency of oral
intake must be considered. Extensive clinical experience
is often required for a proper evaluation and management
of dysphagia. Moreover, most of the clinical evaluations
ments. Submental ultrasonography, a readily accessible
clinicians obtain the whole picture of the swallowing
function of a patient. Adequate larynx elevation can
reduce the risk of aspiration and good bolus handling
reduced hyoid bone displacement and tongue thickness
change, which indicate severely impaired swallowing
function. Stroke patients with hyoid bone displacement
exceeding 1.5 cm and a tongue thickness change
exceeding 1.0 cm have substantial potential to be free
from tube feeding.
In addition to presenting no radiation and being
noninvasive, ultrasonography is portable and can be used
at the bedside for bedridden patients. Another advantage
of ultrasonographic examination is the use of real food
in swallowing assessments, in contrast to the barium
meal in VFSS. This facilitates a more physiological eval-
uation of the swallowing function. In addition, other
abnormalities in the oral stage, such as premature oral
leakage, impaired tongue propulsion and repeated swal-
Although VFSS provides a more comprehensive eval-
uation of the physiology and anatomy of swallowing,
submental ultrasonography can complement VFSS as
Table 2. Changes in tongue thickness and hyoid bone
displacement when swallowing 5 mL of water (cm)*
Tongue thickness change
Hyoid bone displacement
SD 5 standard deviation; FOIS 5 functional oral intake scale.
* Statistics were obtained using a Mann-Whitney test.
yp value 5 .002 (group 1 vs. group 2), ,.001 (group 1 vs. group 3),
.061 (group 2 vs. group 3).
zPercentage of change 5 tongue thickness change/resting tongue
thickness 3 100%. p value 5 .012 (group 1 vs. group 2), ,.001 (group
1 vs. group 3), .014 (group 2 vs. group 3).
xp value 5 .001 (group 1 vs. group 2), ,.001 (group 1 vs. group 3),
.22 (group 2 vs. group 3).
Fig. 3. A box plot for the results of each group (cm). The rectangle represents the values of the two central quartiles, and
the lines represent the tenth to ninetieth quartiles. The horizontal lines inside the rectangles represent the median values.
The dots represent the fifth and 95th percentiles. The dash lines represent the cut-off points chosen for detecting tube-
feeding dependent dysphagia (FOIS 1–3). (a) Change in tongue thickness when swallowing 5 mL of water. (b) Hyoid
bone displacement when swallowing 5 mL of water.
Ultrasonography in assessing oropharyngeal dysphagia d M.-Y. HSIAO et al.5
Although previous studies have applied ultrasonog-
raphy for assessing tongue movement, quantitative anal-
ysis and functional correlation was not conducted.
Shawker et al. (1983) first applied ultrasonography for
observing tongue movement and observed decreased
tongue movement in a patient with hypoglossal nerve
palsy. They also identified the motor sequence of the
tongue and hyoid bone movement during swallowing by
applying ultrasonography on healthy people (Shawker
et al. 1984). Stone and Shawker (1986) fixed a pellet to
the tongue surface of six healthy people to record hori-
zontal and vertical tongue movement and found that
major tongue movement correlates with the propulsion
a descriptive scoring system for bolus control and tongue
and hyoid movement and observed decreased movement
in malnourished disabled children. Tongue mobility is
important for preventing premature oral leakage and
enabling bolus preparation and propulsion of the bolus
into the pharynx. Reduced changes in tongue thickness
when swallowing may suggest impaired tongue mobility,
further indicating dangerous and inefficient swallowing,
thereby increasing the possibility of tube feeding, as
shown in this study.
Hyoid bone displacement is a major contributor to
larynx elevation, which is essential for airway protection
during swallowing. Lower hyoid displacement indicates
a higher risk of aspiration; thus, it can be used as an
adjunct predictor of tube-feeding dependency. Previous
studies have used ultrasonography for observing hyoid
bone movement (Sonies et al. 1996). Kuhl et al. (2003)
and Huang et al. (2009) employed ultrasonography to
measure hyoid-larynx approximation, using the result as
a parameter to estimate larynx elevation. Huang et al.
(2009) found that the hyoid-larynx approximation of the
dysphagic stroke patient group was lower than that of
the nondysphagic patient group. Yabunaka et al. (2011)
used ultrasonography to depict the trajectory of hyoid
bone movement during swallowing. They also observed
compared with young participants. This study further
defined diagnostic cut-off values and enabled ultrasonog-
raphy to be used in screening for high-risk patients with
severely impaired tongue movement and larynx elevation
in a more objective manner.
Most previous studies did not consider the trans-
ducer translation to skin when calculating hyoid bone
displacement usingultrasonography.Measurement errors
have been reported because of the movement of the trans-
ducer over the skin (Chi-Fishman 2005). To facilitate
bedside application, the head immobilization instrument
was not applied in this study. Instead, we manually posi-
tioned the transducer developed by Stone (2005) to
reduce the movement of the transducer over the skin.
mandible, which was visible during the entire recording
process of submental ultrasonography, was used as the
reference point. During examinations, the participant’s
head must remain in a neutral position to ensure that
the transducer is vertical to the submental area and in
the midsagittal plane. Under this precaution, the results
of this study showed no significant difference in hyoid
bone displacement between the measurements provided
by submental ultrasonography and by VFSS.
gic stroke patients. However, this study has several limita-
participant cooperation to ensure stable positioning and
transducer placement. Thus, patients with severely
impaired cognition or involuntary movement were unsuit-
sionally, maintaining good skin-transducer contact during
the swallowing examination was difficult in patients with
prominent thyroid cartilage and minimal soft neck tissue.
Placing a water balloon in front of the transducer may
istics. In addition to the amount of hyoid bone displace-
ment, the timing and velocity of hyoid bone movement
are important for airway protection. The timing was not
investigated in this study. The triggering time of the swal-
lowing reflex can be calculated using a timer. Further
studies are required to determine the reliability of
measuring swallowing reflex using submental ultrasonog-
a limited sample size and clinical functional correlation
was used. Further large-scale studies are required to verify
the diagnostic accuracy of submental ultrasonography and
to determine whether the results correlate with aspiration
rate. Finally, a longitudinal follow-up study must be con-
ducted to evaluate the sensitivity to changes in swallowing
raphy among dysphagic stroke patients.
calculatinghyoid bonedisplacement, the
Submental ultrasonography enables visualization of
bolus transporting in the oral stage and reliable measure-
thus, aiding in bedside assessments of swallowing func-
tion among stroke patients. A hyoid bone displacement
less than 1.5 cm and a tongue thickness change of less
than 1.0 cm correlates with a poor swallowing function.
Acknowledgments—The authors thank Mr. Steve Yao for his assistance
in designing the software for the ultrasonography.
6Ultrasound in Medicine and Biology Volume -, Number -, 2012
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