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Method for detection of aspiration based on B-mode video ultrasonography

Article  in  Radiological Physics and Technology · April 2014

DOI: 10.1007/s12194-014-0264-3 · Source: PubMed

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Radiol Phys Technol (2014) 7:290–295
DOI 10.1007/s12194-014-0264-3
Method for detection of aspiration based on B-mode video
ultrasonography
Yuka Miura • Gojiro Nakagami • Koichi Yabunaka
Haruka Tohara • Ryoko Murayama •
Hiroshi Noguchi • Taketoshi Mori • Hiromi Sanada
Received: 14 January 2014 / Revised: 20 March 2014 / Accepted: 24 March 2014 / Published online: 10 April 2014
Ó Japanese Society of Radiological Technology and Japan Society of Medical Physics 2014
Abstract In this study, we aimed to develop a new method
for detection of aspiration based on B-mode video ultraso-
nography and to evaluate its performance. To detect aspi-
rated boluses by B-mode video ultrasonography in patients
with dysphagia, we placed a linear array transducer above the
thyroid cartilage and observed the area around the vocal
folds. Forty-two ultrasonographic measurements were
obtained from 17 patients with dysphagia who also under-
went videofluoroscopy or videoendoscopy measurements at
the same time. Aspirated boluses were observed in B-mode
Y. Miura
G. Nakagami
H. Sanada (&)
Department of Gerontological Nursing/Wound Care
Management, Graduate School of Medicine, The University of
Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
e-mail: hsanada-tky@umin.ac.jp
Y. Miura
Japan Society for the Promotion of Science, 5-3-1 Kojimachi,
Chiyoda-ku, Tokyo 102-0083, Japan
K. Yabunaka
Department of Ultrasound, Katsuragi Hospital, 2-33-1 Habu-cho,
Kishiwada, Osaka 596-0825, Japan
H. Tohara
Gerodontology and Oral Rehabilitation, Department of
Gerontology and Gerodontology, Graduate School of Medical
and Dental Sciences, Tokyo Medical and Dental University,
1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8549, Japan
R. Murayama
Department of Advanced Nursing Technology, Graduate School
of Medicine, The University of Tokyo, 7-3-1 Hongo,
Bunkyo-ku, Tokyo 113-0033, Japan
H. Noguchi
T. Mori
Department of Life Support Technology (Molten), Graduate
School of Medicine, The University of Tokyo, 7-3-1 Hongo,
Bunkyo-ku, Tokyo 113-0033, Japan
•
video ultrasonographic images as hyperechoic, long, narrow
objects that passed through the vocal folds beneath the
anterior wall of the trachea, with movement different from
that of the surrounding structure. The sensitivity of aspiration
detection was 0.64, and the specificity was 0.84. This newly
developed detection method will enable patients with dys-
phagia to receive appropriate daily swallowing care.
Keywords Aspiration pneumonia
Deglutition
disorders
Sensitivity and specificity
Ultrasound
1 Introduction
Pneumonia is the third leading cause of death in Japan, and
aspiration pneumonia accounts for 90 % of cases, which
predominantly occurs in elderly people [1]. Aspiration is
defined as passage of material below the vocal folds [2].
With repeated aspiration, bacteria within food or saliva are
often introduced into the lungs, where they can cause
aspiration pneumonia [3]. Most aspiration pneumonia is
caused by silent aspiration without producing a reflexive
cough [4]. Therefore, a timely detection method for aspi-
ration, including silent aspiration, is needed for preventing
pneumonia in elderly people.
Convenient screening tests for dysphagia are often used
at the bedside, such as the repetitive saliva swallowing test
[5], water swallowing test [6], and food test [7]. However,
these tests use clinical signs such as coughing as an indi-
cator of the presence of aspiration, and they cannot detect
silent aspiration. A cough test, which uses an induced
cough reflex by citric acid particle inhalation as a surrogate
indicator of silent aspiration, has been proposed as a useful
screening test for silent aspiration [8]. Although this test
shows high sensitivity and specificity, clinicians cannot
Method for detection of aspiration
directly observe silent aspiration. In other words, clinicians
cannot know the appropriate viscosity of the bolus and the
effective swallowing posture that prevent aspiration. Apart
from these screening tests, the development of a method of
direct detection of aspiration, including silent aspiration,
would also be effective for daily swallowing care. Patients
would be able to receive appropriate care according to the
detection of aspiration.
Videofluoroscopy (VF) and videoendoscopy (VE) are
considered to be the most appropriate detection methods
for silent aspiration because we can directly observe the
passage of a bolus into the trachea [9, 10]. However, these
procedures for detection of silent aspiration in patients with
dysphagia are sometimes not common in clinical settings
because they are invasive and complicated. Therefore, a
new noninvasive method for detection of aspiration in a
patient’s daily feeding is required.
B-mode video ultrasonography (BV-US) appears to be an
ideal method for detection of silent aspiration because it is
noninvasive and performed in real time. However, passage
of a bolus into the trachea has not been detected by BV-US.
The trachea contains air, which causes ultrasound attenua-
tion [11]; thus, most researchers believe that it is difficult to
detect material in the trachea by BV-US. There are a few
reports on US measurement of hyoid bone or geniohyoid
muscle movements during swallowing [12–14]. It is difficult
to modify food viscosity or change the swallowing posture
based on these movements; hence, a new technique for
detecting material in the trachea by US is needed. Several
reports have included US images of the bolus in the oral
cavity during the different phases of oral and pharyngeal
swallowing [15–17]. There are some amounts of air present
in the oral cavity and the pharynx; therefore, we focused on
the region around the vocal folds when imaging aspirated
boluses because ultrasound attenuation by air would be
minimal in this location. US observation of the vocal folds
indicated that the trachea was sufficiently narrow at the
vocal folds for visualization of a bolus in the trachea [18].
We hypothesized that an aspirated bolus in the trachea
would be observed as a hyperechoic object-like bolus in the
oral cavity. In this study, we aimed to develop a new method
for detection of aspiration based on BV-US and to evaluate
its performance in a clinical setting by comparing the results
with those of VF or VE examination.
2 Methods
2.1 Patients and setting
This was a cross-sectional observational study conducted
from June to November 2012. All data were collected at the
dysphagia outpatient clinic of a general hospital in Chiba
291
prefecture, Japan. Individuals[60 years old who underwent
VF or VE examinations were included. Patients who could
not undergo BV-US examination at the same time with VF or
VE examination were excluded. Age, sex, and disease his-
tory were collected from the medical records. Items related
to examinations, including type of test food, patient’s pos-
ture, aspiration, and cough reflex, were recorded at each
examination. The study protocol was approved by the Ethics
Committee of the Graduate School of Medicine, The Uni-
versity of Tokyo (#3260). Written informed consent was
obtained from all patients or their proxies.
2.2 BV-US examination
BV-US examination was performed at the same time as VF
or VE examinations by the same operator for all patients.
An examination consisted of more than one measurement,
and the test food for each measurement was modified
during the examination. The test foods consisted of three
types as follows: thin liquid, thick liquid, and solid food.
The examples of thin liquids are water, milk, and soup.
They often cause aspiration, and it is more difficult for
patients with dysphagia to swallow such thin liquids
compared with thick liquids. Thick liquids represent an
increased consistency to allow patients with dysphagia to
swallow easily. They are less easy to pour and drizzle from
a cup or bowl like honey. Solid foods hold their shape.
They cannot be poured and are generally consumed with a
spoon. They are easier to swallow than liquids. The solid
food was served by an experienced speech-language-
hearing therapist (ST) with a spoon to adjust the amount to
the patient’s swallowing ability. Thin and thick liquids
were also served by a ST with a cup or a syringe. We did
not take into account the amount of the test food to analyze
the data because the ability of visualization of aspirated
boluses in BV-US movies did not appear to be based on
their initial sizes, but on their swallowed sizes. The
amounts of the aspirated boluses were not different
between each VF and VE image. Bedside US (M-Turbo;
Sonosite, Bothwell, WA, USA) was performed with use of
a 6–15 MHz (HFL509) linear array transducer. The head
and neck positions of the patients were not fixed, to
facilitate swallowing in their most comfortable posture.
The transducer for the longitudinal scan was placed above
the thyroid cartilage (Fig. 1a). The patient was asked to
speak for detection of vibrations of the vocal folds on the
display screen for determining the landmark during swal-
lowing (Fig. 1b). Before each measurement, the transducer
was placed at the vocal folds shown in the middle of the
display screen, with the cranial side on the left. The images
were captured on a hard disk. The operator held the
transducer to keep the initial location during swallowing
and ensured that the swallowing movements were not
292 Y. Miura et al.

Fig. 1 a Setting of the

transducer during scanning of
swallowing in the sagittal plane.
b Ultrasonographic image of the
vocal folds. The cranial side is
the left side, and the skin surface
is the upper side

Fig. 2 a Image of an aspirated

bolus by ultrasonographic (US)
examination. b An image of an
aspirated bolus by
videofluoroscopic examination
that was obtained
simultaneously with US
examination

disturbed. An operator obtained BV-US movies of swal-
lowing within 6–30 s at a rate of 30 frames per second. We
decided to use this frame rate to correspond to the VF and
VE examination. Image acquisition settings for the ultra-
sound machine, such as focus, frequency, and zoom, were
maintained for all measurements for standardization of the
image quality. We had to focus on a trachea that was
located above the esophagus to detect aspirated boluses.
The esophagus was always visualized within 4 cm from the
contact surface with a probe in BV-US images. Therefore,
we decided on a scanning depth of 4 cm from the skin in
order to visualize all structures of the trachea. The echo
gain and dynamic range were tuned to a proper level for
each measurement. The US operator evaluated the aspira-
tion without referring to the VF or VE results to avoid any
bias. Aspiration on BV-US was interpreted as passage of a
hyperechoic object through the vocal folds beneath the
tracheal anterior wall, with the movement different from
that of the surrounding structure (Fig. 2a). Twenty BV-US
measurements were obtained at the same time as VF, and
the remaining 31 BV-US measurements were obtained with
VE. Two patients (six measurements) were excluded
because a tracheostomy hole or a labored cough caused
difficulty in placement of the transducer at an appropriate
position during the examination. In addition, three mea-
surements were excluded after a discussion with an expe-
rienced sonographer because of high attenuation caused by
air between the transducer and skin. Finally, 42 measure-
ments from 17 patients were analyzed.
2.3 VF and VE examinations
All patients received VF (DI Station ADR-1000A; Toshiba
Medical Systems, Tokyo, Japan) or VE (FNL-10RBS;
PENTAX MEDICAL, Ontario, Canada) assessment of
swallowing simultaneously with BV-US by experienced
dentists (Fig. 2b). We used barium sulfate for VF exam-
inations as a contrast medium, and we used a coloring
agent for VE examinations. Both additives are commonly
used in these examinations, and both methods are widely
used as gold standards in clinical settings. In particular,
previous studies revealed that there was a good agreement
between these two methods in terms of detection of aspi-
ration [9, 19]. The dentists decided on the examination
protocol and the number of measurements that should be
performed. They changed the test food viscosity and
measurements if necessary. An experienced dentist evalu-
ated aspiration in each VF and VE measurement.
2.4 Data analysis
For comparing demographic data, patients who aspirated at
least once during the examination were classified into the
‘‘aspiration’’ group, whereas others were classified into the
Method for detection of aspiration 293

‘‘without-aspiration’’ group. A t test or Fisher’s exact test Table 1 Demographic data

was used for comparison of the patient characteristics Aspiration Without aspiration p value
between the ‘‘aspiration’’ and ‘‘without-aspiration’’ groups. N=8 N=9
We used the results of the VF or VE examinations as the
Age (years), mean ± SD 71 ± 9.2 69 ± 6.2 0.583a
reference to calculate the sensitivity and specificity of
aspiration detection for each BV-US measurement. It was Male, n (%) 8 (100) 8 (88.9) 0.307b
important to evaluate aspiration for each measurement Disease, n (%)
rather than for each patient because the operators changed Stroke 5 (62.5) 4 (44.4) 0.637b
the test food for the patients between measurements. Pneumonia 0 (0.0) 2 (22.2) 0.471b
Therefore, the performance of aspiration detection by BV- Head and neck cancer 0 (0.0) 2 (22.2) 0.471b
US on a measurement basis was evaluated. Two separate Others 3 (37.5) 1 (11.1) 0.294a
measurements were obtained from all patients at an interval Silent aspiration 6 (75.0) – –
of 1 month. The repeatability of the aspiration detection a
t test
method was assessed by calculation of the kappa coeffi- b
Fisher’s exact test
cient for the two measurements for each patient. The sta-
tistical significance level was set at p \ 0.05. Statistical
Analysis System software version 9.2 (SAS Institute, Cary, Table 2 Results of the aspiration detection method based on BV-US
NC, USA) was used for all statistical analyses.
N = 42 (measurements) VF/VE
Aspirated Not aspirated
3 Results
BV-US Aspirated 7 5
Not aspirated 4 26
This study included 17 patients (16 males), with an average
age of 70 ± 7.6 years. There were no differences in the VF Videofluoroscopy, VE videoendoscopy, BV-US B-mode video
patient characteristics between the aspiration and without- ultrasonography
aspiration groups. All of the 8 subjects in the aspiration
group were males. They had the following diseases: Five detection method based on BV-US were 0.64 and 0.84,
had a stroke, two had Parkinson’s disease, and one had respectively. The kappa coefficient was 0.66.
amyotrophic lateral sclerosis. Six patients had silent aspi-
ration at least once during the examination (Table 1).
Eleven BV-US measurements were diagnosed as aspi- 4 Discussion
ration with reference to the VF/VE measurements. Among
the seven measurements that were detected correctly as This is the first study to show that an aspirated bolus in the
aspiration by BV-US measurements, five were obtained trachea was observed as a hyperechoic, long, narrow object
from stroke patients and one each was obtained from a moving along the trachea wall by BV-US examination. In
patient with Parkinson’s disease and a patient with amyo- addition, this is the first study to use comparisons with
trophic lateral sclerosis. Among the four measurements that reference test findings to confirm the usefulness of BV-US
were not detected correctly as aspiration by BV-US mea- examination findings.
surements, two were obtained from stroke patients and one We focused directly on the vocal folds to observe
each was obtained from a patient with Parkinson’s disease aspirated boluses. There were no marked differences in the
and a patient with amyotrophic lateral sclerosis. All of the location of the vocal folds and the characteristics of the
measurements that were not detected as aspiration by BV- surrounding soft tissues among the patients who had vari-
US measurements were obtained with thin-liquid swal- ous diseases, which allowed us to detect aspiration in BV-
lowing. Among the seven measurements that were cor- US images from these patients. A previous method that
rectly detected by BV-US measurements as aspiration, two measured surrounding muscle movement by B-mode US
were obtained from solid food, two were obtained from showed that the extent of the differences varied widely
thick liquid, and three were obtained from thin liquid. between different diseases [20]. Moreover, a sex difference
Among the seven measurements that were detected cor- has been reported in the movement of the surrounding
rectly by US measurements as aspiration, three measure- muscle [13]. Thus, it is difficult to detect abnormal swal-
ments were obtained by VF examination and four were lowing in a variety of patients by movement of the sur-
obtained by VE examination. Table 2 shows the results of rounding structures. In male subjects, it appears to be more
the detection of the aspiration based on BV-US measure- difficult to observe material in the trachea because males
ments. The sensitivity and specificity of the aspiration have a larger laryngeal prominence than female subjects,
294
which causes attenuation of US. In this study, all of the
aspirated patients were male, and the aspirated boluses
were detected successfully in the BV-US images. There-
fore, it appears that this aspiration detection method can be
applied to both males and females.
In previous studies, the sensitivity and specificity of a
repetitive saliva swallowing test were 0.28 and 0.76,
respectively [5]; the sensitivity and specificity of a 100-ml
water swallowing test using choking or a wet-hoarse voice
as the sole factor for predicting the presence of aspiration
were 0.48 and 0.92, respectively; [6], and the sensitivity
and specificity of a food test were 0.72 and 0.62, respec-
tively [7]. In this study, the BV-US-based aspiration
detection method gave a sensitivity of 0.64 and a speci-
ficity of 0.84 when we interpreted a hyperechoic, long,
narrow object moving along the tracheal wall in the BV-US
images as an indicator of the presence of aspiration. We
believe that the good results for sensitivity and specificity
were achieved by direct observation of the bolus in the
trachea. We correctly detected aspirated boluses in four of
the seven images that were obtained from silent aspiration
cases.
We consider that the scanning methods we used were
appropriate, but the reduction in the sensitivity occurred by
the aspiration of thin liquids. When we separately ran the
analysis for thin liquids, the sensitivity and specificity were
0.43 and 0.81, respectively. On the other hand, the sensi-
tivity and specificity for detecting aspirated thick liquid or
solid food by BV-US were 1.00 and 0.81, respectively.
These results indicate that this scanning method is optimal
at least for swallowing of thick liquid and solid food. Four
images were not detected as aspiration by the BV-US
method. The reason is related to the speed of the bolus
when it passes through the larynx, which differs according
to the grade of bolus viscosity [21]. All of the measure-
ments in which we could not detect aspiration from the
BV-US images were caused by swallowing of thin liquid. It
was difficult to detect such boluses from the BV-US
measurements because the duration of the thin-liquid pas-
sage through the BV-US scan area was relatively short. The
objects that we could detect as aspirated boluses in the BV-
US measurements had characteristic movements and
shapes. Therefore, if we can identify quantitative charac-
teristics of the object, we will be able to develop some
image-processing method that helps our evaluation in the
BV-US measurements. In future studies, we hope to
develop an image-processing method that can improve the
sensitivity and specificity of the BV-US measurements.
The results of this study suggest that the newly
developed noninvasive detection method would help
clinicians provide daily appropriate swallowing care.
BV-US measurements performed simultaneously with
VE measurements could detect bolus aspiration. The
Y. Miura et al.
BV-US performance of aspirated bolus detection was not
different between the measurements obtained by VF and
those obtained by VE. Thus, special test foods such as
barium liquid are not required for the BV-US-based
method. Patients can undergo examination for detection
of aspiration in their hospital room with their usual
feeding. Consequently, clinicians will be able to detect
aspirations that have been overlooked by lack of timely
detection methods and silent aspirations that have been
overlooked by bedside screening tests.
The limitation of this study was that the performance of
evaluation was based on BV-US measurements obtained by
one operator. The BV-US operation technique has an influ-
ence on the evaluation of measurements. Future studies are
required for establishment of the necessary training in the
BV-US operation technique that can assure reproducible
detection of aspiration among various clinicians.
5 Conclusion
In this study, a new method based on BV-US for detection
of aspiration, including silent aspiration, was developed.
The sensitivity and specificity of the aspiration detection
method were 0.64 and 0.84, respectively, when we inter-
preted a hyperechoic long, narrow object moving along the
tracheal wall in the images as an indicator of an aspirated
bolus.
Acknowledgments This study was funded by a grant-in-aid for
Challenging Exploratory Research from the Japan Society for the
Promotion of Science to Hiromi Sanada (Grant No. 23659999). We
thank the director of the Katsuragi Hospital, Dr. Mutsumi Ohue, who
provided advice and assistance during the study. Furthermore, we
would like to express our sincere thanks to all of the dysphagia
patients who participated in this study, and to the clinical staff who
supported the data collection.
Conflict of interest The authors declare that they had no conflicts
of interest related to this study.
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