Avaliação Ultrassonográfica Do Músculo Genio-Hióideo e Osso Hióide Durante A Deglutição em Adultos Jovens PDF

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The Laryngoscope
C 2015 The American Laryngological,
V
Rhinological and Otological Society, Inc.

Ultrasonographic Evaluation of Geniohyoid Muscle and Hyoid Bone


During Swallowing in Young Adults

Xin Feng, MD, PhD; Michael S. Cartwright, MD, MS; Francis O. Walker, MD; Jessica H. Bargoil, BS;
Yunping Hu, MD, PhD; Susan G. Butler, PhD

Objectives/Hypothesis: The geniohyoid muscle plays an important role in hyoid bone movement. Adequate hyoid bone
movement during swallowing is important for effective bolus flow and pharyngeal clearing. The aim of this study was to esti-
mate the relationship between the geniohyoid muscle size and function and hyoid bone movement during swallowing in
healthy young adults, as measured via ultrasound, in different body positions.
Study Design: Cross-sectional study.
Methods: Forty young (20–40 years old) adults (20 male and 20 female) participated. The cross-sectional area of the
geniohyoid muscle at rest (seated position), the geniohyoid muscle contraction velocity, and the hyoid bone displacement dur-
ing swallowing 10 mL of mineral water were measured by ultrasound in seated, supine, and right lateral decubitus positions.
Results: The size of the geniohyoid muscle correlated with body height. Males had larger geniohyoid cross-sectional
area than females and greater maximal and anterior hyoid displacement during swallowing than females, and maximal and
anterior hyoid bone displacement during swallowing correlated with the size of geniohyoid muscle only when the body was
in the supine position; these two movements were positively correlated to each other.
Conclusions: Genders vary in hyoid bone movement during swallowing, and the correlation between geniohyoid muscle
size and hyoid bone displacement varies among different body positions during swallowing. This investigation also illumi-
nates the use of ultrasound in providing quantitative measures of geniohyoid muscle and hyoid bone displacement during
swallowing.
Key Words: Ultrasonography, geniohyoid muscle, muscle contraction, hyoid bone, swallowing, body position.
Level of Evidence: 2c.
Laryngoscope, 125:1886–1891, 2015

INTRODUCTION risk and pharyngeal residue in dysphagia and aging.3–6


The hyoid bone is a suspended bone that connects Our previous study found that a more posterior position
to the thyroid cartilage and mandible bone through liga- of the hyoid bone at rest is associated with advanced age
ments and muscles (e.g., mylohyoid, geniohyoid, digas- and is correlated with aspiration in older people.7 The
trics, hyoglossus).1 The excursion of the hyoid bone due suprahyoid muscles have a major role in hyoid bone
to the contraction of the attached skeletal muscles helps movement during swallowing. Among these muscles, the
drive tongue and laryngeal movements during swallow- geniohyoid muscle has the most potential to move the
ing. Upward displacement of the hyoid bone during hyoid in the anterior direction, and the mylohyoid has
swallowing is related primarily to events in the oral cav- the greatest ability to move the hyoid in the superior
ity, whereas anterior displacement of the hyoid is related direction.8 Disrupted hyoid bone movement in the ante-
to the opening of the upper esophageal sphincter during rior direction is particularly problematic to swallowing.3
the pharyngeal processes of swallowing.2 Reduced range It has also been noted that age-related geniohyoid mus-
of hyoid movement has been associated with aspiration cle atrophy is related to aspiration status in healthy
older adults.9 A kinematic study to estimate the direct
relationship between the geniohyoid muscle size and
From the Department of Otolaryngology (X.F., S.G.B.), Department function and hyoid bone movement during swallowing is
of Neurology (M.S.C., F.O.W., J.H.B.), and Department of Neurosurgery lacking.
(Y.H.), Wake Forest School of Medicine, Winston-Salem, North Carolina,
U.S.A Although video fluoroscopy, computed tomography
Editor’s Note: This Manuscript was accepted for publication (CT), and dynamic magnetic resonance imaging (MRI)
January 28, 2015. have been used to evaluate hyoid bone movement during
This work was supported by the Department of Otolaryngology swallowing,10–13 their disadvantages of radiation expo-
and Department of Neurology, Wake Forest School of Medicine and
NINDS grant 1K23NS062892 (M.S.C.) sure (video fluoroscopy and CT) and high cost (MRI)
The authors have no other funding, financial relationships, or con- limit their benefits as regular techniques in both basic
flicts of interest to disclose.
Send correspondence to Xin Feng, MD, PhD, Assistant Professor,
research and clinic application. In addition, video fluo-
Department of Otolaryngology, Wake Forest School of Medicine, Medical roscopy is limited in its ability to quantify muscle size
Center Boulevard, Winston-Salem, NC 27157. and contraction activity during swallowing, which are
Email: xfeng@wakehealth.edu
also difficult to assess with CT and MRI. Ultrasound,
DOI: 10.1002/lary.25224 a technique with low cost, portability, and without

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Fig. 1. Diagram for measuring cross-
sectional area of the geniohyoid muscle
in the coronal plane with ultrasound. (a)
The marker for ultrasonic transducer
placement. (b) Ultrasonographic image
showing the outlines of geniohyoid
(GH) and anterior diagastric (D)
muscles when the transducer was
placed at the marker placement for
measurements. The scale for the x/y-
axis is in centimeters.

radiation has been used for hyoid bone movement the inferior border of the mandible bone and the hyoid was
assessment during swallowing,14–18 with high reliabil- measured, and the skin was marked at a position one-third
ity.15,19 Most importantly, ultrasound can assess muscle (Fig. 1a) posterior to the inferior border of the mandible bone.
contraction and activity,20,21 and geniohyoid muscle The transducer was placed at the marker to measure the cross-
sectional area of the geniohyoid muscle (Fig. 1b). Resolution
movement during swallowing.22
was to one-tenth of a millimeter. The measurement took about
One of our research aims is to determine if genio- 15 to 30 seconds, and the participants were instructed not to
hyoid muscle sarcopenia in aging or other muscular dis- swallow during this measure.
eases reduces hyoid bone movement during swallowing Contraction velocity of geniohyoid muscle during
and contributes to aspiration or other swallowing prob- swallowing at three different body positions. Three differ-
lems. This study is the first step toward making that ent body positions (seated, supine, and right lateral decubitus)
determination and then targeting rehabilitative thera- were used to identify the gravity effects on the muscle contrac-
pies. We used ultrasound in healthy young adults to tion and hyoid bone movement during swallowing. Pillows (20 3
assess: 1) geniohyoid muscle size at rest, 2) geniohyoid 26 3 4 in) as needed (depending on the distance from neck to
muscle contraction during swallowing, 3) hyoid bone shoulder in each participant) were used to lift the head to keep
the neck straight and in line with the body and keep each of the
movement during swallowing, 4) the correlation coeffi-
body positions consistent among all the subjects. The transducer
cient between the geniohyoid muscle size and function was placed in the medial submental region longitudinally, and
during swallowing, and 5) the correlation between genio- ultrasonography of the geniohyoid muscle was performed in M
hyoid muscle size and hyoid bone movement during mode (Fig. 2). The scan line was set at the position of the thick-
swallowing. In addition, in consideration of gravity being est point in the geniohyoid muscle in each participant (Fig. 2a).
a confounder in the geniohyoid muscle and hyoid activity The participant was instructed to take 10 mL of mineral water
during swallowing among different body positions, we through a straw to avoid head movement, and the water was
did all of our assessments in three different body posi- held in the mouth until the ultrasonographer said “swallow.” The
tions: seated, supine, and right lateral decubitus. chin was held by the tester to avoid head movement during swal-
lowing. Ultrasonography of the geniohyoid muscle movement
was performed in M mode (Fig. 2b). “A” was the maximal con-
MATERIALS AND METHODS tractional distance of the geniohyoid muscle and “B” was the
duration of the geniohyoid muscle contraction (from resting to
Participants maximal contraction) during swallowing. The velocity (V) of the
Forty healthy young adults (20–40 years old) comprised of geniohyoid muscle contraction during swallowing was calculated
20 females and 20 males participated in this study. The study as V 5A/B. This test was repeated five times, with a 40-second
was approved by the Wake Forest University Health Sciences interval between swallows. Results from all five tests were aver-
Institutional Review Board, and participants provided written aged for data analysis. The amount of water, repetitions, and
consent. Participants reported no history of swallowing, speech, duration of intervals between swallowing used was the same as
or respiratory disorders, and no neurologic, muscular, or otola- those used in previous studies.16,19,22
ryngologic trauma/disorders. Hyoid bone movement during swallowing in three
different body positions. The transducer was placed slightly
posterior to the position described above, so that the hyoid bone
Apparatus signal at the midsagittal plane could be shown in the scan (Fig.
A Biosound MyLab25 ultrasound device (Esaote Group, 3a). Images of hyoid bone movement from rest to the maximal
Genoa, Italy), with an 18-MHz linear array transducer was used. excursion during each bolus swallow was recorded and saved.
The moving images were reviewed, and frozen frames at rest
and the maximal displacement during swallowing were ana-
Data Collection lyzed (Fig. 3b; x-axis horizontal migration, y-axis perpendicular
Cross-sectional area of geniohyoid muscle. The partic- migration). The maximal hyoid excursion distance (A–B), ante-
ipants were instructed to sit in a chair in an upright position to rior displacement (A–C) at the x-axis, and superior displace-
control body movement during measures. The distance between ment (A–D) at the y-axis were measured and analyzed.

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Fig. 2. Real-time imaging of geniohyoid muscle. (a) B-mode; a sagittal view of the geniohyoid muscle at rest (the arrow indicates the scan
line). (b) M-mode; arrows indicate the start (1), peak (2), and end (3) of the geniohyoid muscle movement during a bolus swallow. Maximal
contractional distance of geniohyoid muscle from baseline to the peak of muscle movement is measured as the letter A. The duration
needed for the geniohyoid muscle to move from rest to maximal contraction during a bolus swallow is measured as the letter B. The GH
abbreviation is the geniohyoid muscle. The scale for the y-axis is in centimeters.

Data Analyses Males had significantly larger geniohyoid muscle size


Data are reported as mean 6 standard deviation. An inde- (i.e., cross-sectional area) than females (P <.05, Table I).
pendent samples t test was used to determine gender differen- However, there were no gender differences in the genio-
ces in age, weight, height, body mass index (BMI), and cross- hyoid muscle contraction velocity in all three body posi-
sectional area of geniohyoid muscle. A multivariate general lin- tions (P >.05, Table I), and the geniohyoid muscle
ear model was used to assess the differences in measures of contraction velocity did not correlate with muscle size
muscle size, contraction velocity, and hyoid bone movement as a (seated, r 5 0.07, P 5.72; supine, r 5 20.05, P 5.87; right
function of gender and body position. Linear regression was lateral decubitus, r 5 0.27, P 5.33) during swallowing. The
used to analyze the relationship of muscle size and contraction different body positions did not affect the geniohyoid mus-
velocity and hyoid bone movement. Statistical analysis was per-
cle contraction velocity in males and females (P >.05).
formed using SPSS 10.0 statistical software (IBM, Armonk,
There were no differences in hyoid bone movement
NY). All significance tests were two tailed, and P <.05 was con-
during swallowing among the three different body posi-
sidered significant.
tions (P >.05, Table II). However, males had greater
maximal and anterior hyoid bone displacement during
RESULTS swallowing in each of the different body positions com-
The cross-sectional area of the geniohyoid muscle pared to females (P <.05). Maximal and anterior hyoid
correlated positively with height (r 5 0.62, P <.001, Fig. displacement during swallowing correlated with the size
4). The geniohyoid muscle size did not correlate with of the geniohyoid muscle only in the supine position
body weight (r 5 20.02, P >.05) or BMI (r 5 0.17, (Fig. 5a: maximal, r 5 0.45, P 5.004; Fig. 5b: anterior,
P >.05). The measurements of muscle size, contraction r 5 0.43, P 5.006). The maximal hyoid displacement dur-
velocity, and hyoid bone movement were then adjusted ing swallowing correlated positively with the anterior
by height and are summarized in Tables I and II. displacement (Fig. 5c: r 5 0.45, P 5.001).

Fig. 3. Sonogram of the hyoid bone at


rest (a) and during swallowing (b). The
letter A is the hyoid bone at rest. The
letter B is the hyoid bone at maximal
movement during a bolus swallow.
The maximal hyoid excursion distance
(A–B), the anterior distance (A–C) at the
x-axis, and the superior distance (A–D)
at the y-axis are shown. The GH abbre-
viation was the geniohyoid muscle. The
scale for the x-axis and y-axis is in
centimeters.

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DISCUSSION
In this study, the geniohyoid muscle size at rest,
geniohyoid muscle activity, and hyoid bone movement
during swallowing were evaluated by ultrasound in
healthy young adults. Our main findings were as fol-
lows: 1) the size of the geniohyoid muscle correlated
with body height, and males had greater geniohyoid
muscle size compared to females; 2) males had greater
maximal and anterior hyoid displacement during swal-
lowing than females; 3) maximal and anterior hyoid dis-
placement during swallowing correlated with the size of
the geniohyoid muscle only when the body was in the
supine position, and these two movements positively cor-
related with each other.
The size of the geniohyoid muscle was larger in the
males compared to females, which is consistent with our
previous study.9 However, no differences were found in
the contraction velocity of the geniohyoid muscle
between genders or in the three different body positions.
No correlation was found between the size of the genio-
Fig. 4. Bivariate scatterplot for positive correlation between the hyoid muscle and contraction velocity. That is, muscle
cross-sectional area of geniohyoid muscle and height at rest. size and body positions do not affect geniohyoid function
during swallowing in healthy young adults. This is simi-
TABLE I. lar to the previous finding that geniohyoid muscle activ-
Characteristics of Study Participants. ity was not significantly affected by body position during
swallowing.23,24 It has been reported that hyolaryngeal
Gender
muscles (including geniohyoid) activation and muscles
Parameter Female Male P Value
size can be increased by swallowing exercises in the
healthy subjects.25,26 We did not evaluate the strength of
No. of participants 20 20 the geniohyoid muscle and its correlation with muscle
Age, yr 30 6 7.4 32 6 6.1 .095 size in this study. However, our previous study found
Weight, lb 136.5 6 22.6 172.7 6 28.7 .349 that geniohyoid muscle atrophy was associated with
Height, in 64.6 6 2.0 69.9 6 3.0 .270 aging and correlated to aspiration status in older
BMI, Ib/in2 23.0 6 3.5 24.8 6 2.9 .360
adults.9 Replication of this study is needed in healthy
older adults and patients with dysphagia, as advanced
CSA of geniohyoid 1.4 6 0.3 2.3 6 0.5* .039
muscle, cm2 age and myopathic diseases may induce loss of muscle
size and strength, which may in turn affect muscle func-
*P <.05 vs. female. tion and contribute to swallowing deficits. Ultrasound
BMI 5 body mass index; CSA 5 cross-sectional area.

TABLE II.
Geniohyoid Muscle Contraction Velocity and Hyoid Bone Movement in Different Body Positions During Swallowing.*
Gender

Parameter Body Position Female Male P Value

Contraction velocity of geniohyoid muscle, mm/s Seated 18.82 6 6.63 19.32 6 10.26 .822
Supine 19.22 6 9.12 23.39 6 13.83 .240
Right lateral decubitus 18.21 6 8.84 25.69 6 17.23 .084
Maximal displacement of hyoid bone, cm Seated 1.43 6 0.28 1.67 6 0.37† .031
Supine 1.39 6 0.32 1.72 6 0.47† .015
Right lateral decubitus 1.42 6 0.37 1.80 6 0.32† .001
Anterior displacement of hyoid bone, cm Seated 1.23 6 0.29 1.46 6 0.38† .041
Supine 1.22 6 0.31 1.56 6 0.49† .013
Right lateral decubitus 1.25 6 0.34 1.60 6 0.36† .003
Superior displacement of hyoid bone, cm Seated 0.69 6 0.20 0.79 6 0.26 .224
Supine 0.66 6 0.22 0.70 6 0.26 .596
Right lateral decubitus 0.66 6 0.24 0.80 6 0.28 .125

*Adjusted by height.

P <.05 vs. female

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swallowing.27–31 Reduced and abnormal hyoid bone dis-
placement during aging and other neurological diseases
was found to be associated with penetration, vallecular resi-
due, aspiration, and other swallowing deficits.3,4,6,32–35 Def-
icits in the anterior movement of the hyoid bone, especially,
contribute to patients’ swallowing impairment.4 Among the
suprahyoid muscles, the geniohyoid muscle is the key mus-
cle moving the hyoid bone in the anterior direction during
swallowing.8,12 In this study, we found that maximal and
anterior hyoid displacement during swallowing was greater
in males compared to females in all three body positions.
Maximal and anterior hyoid displacements were correlated.
However, there was no difference in the superior displace-
ment between males and females. This suggests a gender
difference in the anterior hyoid displacement during swal-
lowing. In addition, the maximal and anterior displace-
ments were correlated to the geniohyoid muscle size when
the participants were in the supine but not in the seated or
right lateral decubitus positions. This correlation variety
among different positions is not clear. However, we suspect
that hyoid bone displacement during swallowing in the
supine position was more muscle dependent to resist grav-
ity and keep constant movement during swallowing, as it
has been previously demonstrated that neither the position
of the hyoid bone nor its movement during pharyngeal
swallowing changed in relation to position nor gravity.36
Our previous studies revealed that aspiration status was
linked to age-related decrease in geniohyoid muscle size in
older men, and the hyoid bone was moved farther away
from the mandible compared to the young males or older
women.9,37Together with the finding that hyoid excursion
was reduced in older males not females,38 it may suggest
that males experience more geniohyoid muscle atrophy and
less compensation for aging effects on hyoid bone move-
ment. Future studies on the correlation among geniohyoid
muscle size, strength, and hyoid bone movement in older
adults and patients with neuromuscular diseases may pro-
vide valuable information on the physiologic mechanisms
underlying swallowing deficits.
In this study, we did not find differences in genio-
hyoid muscle activity and hyoid bone movement among
different body positions. This suggests that geniohyoid
muscle function and hyoid bone displacement are nor-
mally preserved in different head and body positions
during swallowing. These findings are also similar to
previous reports.23,36,39 Conversely, others have reported
that the hyoid bone position changes with body position
and has a greater amount of anterior displacement while
in the supine position compared to that of the upright
Fig. 5. Bivariate scatterplot for positive correlation between the position.40,41 These different findings from varying stud-
maximal (a)/anterior (b) moving distance of the hyoid bone and
cross-sectional area of the geniohyoid muscle during swallowing in ies may be due to the different materials, bolus volume,
the supine position. (c) Positive correlation between the maximal and assessment technologies. Differences in bolus vol-
and anterior displacements of the hyoid bone during swallowing. ume and viscosity can modulate the pharyngeal swallow
via volume-dependent sensory feedback loops, thus
may prove useful for evaluating geniohyoid muscle func- inducing differences in muscle activity and hyoid bone
tion and swallowing pathology in these diseases. displacement during swallowing.42–46 The findings of
Suprahyoid muscles, including the geniohyoid muscle, this study were from swallowing 10 mL of water; how-
are responsible for hyoid bone displacement during ever, we hypothesize that by using different bolus vol-
swallowing.8 Hyoid bone displacement plays an important umes and viscosities in our future ultrasound studies,
role in glottic closure and upper esophageal sphincter we may find differences in geniohyoid activity and hyoid
opening, which are critical for airway protection during displacement as a function of head position.

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A limitation of this study is that we only assessed 16. Yabunaka K, Sanada H, Sanada S, et al. Sonographic assessment of hyoid
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