DOI:10.2214/AJR.07.2043
AJR 2008; 190:W19-W27
© American Roentgen Ray Society
Comparison of Three Free-Breathing T2-Weighted MRI Sequences in the Evaluation of Focal Liver Lesions
Bong Soo Kim1,
Jung Hoon Kim2,
Guk Myung Choi1,
Seung Hyoung Kim1,
Ji Kang Park1,
Byung-Cheol Song3 and
Weechang Kang4
1 Department of Diagnostic Radiology, Cheju National University Hospital, Cheju
National University College of Medicine, 154, 3-do 2-dong, Jeju City, Jeju-Do,
690-716, Korea.
2 Department of Diagnostic Radiology, Soonchunhyang University Hospital, Seoul,
Korea.
3 Department of Internal Medicine, Cheju National University Hospital, Cheju
National University College of Medicine, Jeju, Korea.
4 Department of Information and Statistics, Daejeon University, Daejeon,
Korea.
Received February 13, 2007;
accepted after revision August 22, 2007.
WEB This is a Web exclusive article.
Address correspondence to B. S. Kim
(67kbs{at}medimail.co.kr).
Abstract
OBJECTIVE. The purpose of this study was to compare three
free-breathing T2-weighted MRI sequences in the evaluation of focal liver
lesions.
MATERIALS AND METHODS. Forty-nine patients with 86 focal liver
lesions (56 malignant, 30 benign) underwent liver MRI with free-breathing
sequences: turbo spin-echo (TSE) with navigator-triggered prospective
acquisition correction (PACE), respiration-triggered TSE, and HASTE with
navigator-triggered PACE. The images were retrospectively reviewed by two
independent observers. Diagnostic performance was evaluated with receiver
operating characteristics and sensitivity. The images were assessed
quantitatively by measurement of the liver signal-to-noise ratio (SNR) and the
lesion-to-liver contrast-to-noise ratio (CNR).
RESULTS. The PACE TSE sequence had better receiver operating
characteristic curves for lesion detection and characterization than did the
respiration-triggered TSE sequence, but the difference was not statistically
significant (p > 0.05). The PACE TSE sequence had a significantly
greater area under the curve for lesion detection (p < 0.01) and
lesion characterization (p < 0.001) than did the PACE HASTE
sequence. The composite sensitivity of the PACE TSE sequence for lesion
detection was significantly higher than that of respiration-triggered TSE
(p < 0.05) and PACE HASTE (p < 0.01). The mean
signal-to-noise ratio for liver and the contrast-to-noise ratio for hepatic
lesions were higher with the PACE HASTE than with the other sequences.
CONCLUSION. The navigator-triggered PACE technique is a valid method
for T2-weighted MRI of the liver and may replace conventional
respiration-triggered techniques.
Keywords: comparative studies • liver neoplasms • MRI • pulse sequences
Introduction
T2-weighted MRI of the liver has been essential for both detection
and characterization of focal liver lesions. With recent advances in the
development of high-performance gradient coils and phased-array torso coils
and the evolution of software, numerous pulse sequences have become available
for T2-weighted hepatic imaging. Artifacts caused by respiratory motion are
one of the major problems with these pulse sequences because the artifacts can
produce image blurring, ghosting, loss of signal intensity, and
misregistration, thereby obscuring important anatomic structures and
lesions.
Various techniques have been used to reduce respiratory artifacts
[1-5].
A straightforward strategy is to use fast imaging. Because the typical
breathing cycle of adult humans lasts 4-5 seconds, respiratory motion is
essentially frozen if all of the k-space data can be acquired faster than that
[6-8].
However, although fast-imaging pulse sequences such as breath-hold turbo
spin-echo (TSE) and single-shot sequences can effectively freeze respiratory
motion, spatial resolution of the resultant images usually is poor, and
artifacts inherent to fast imaging often become troublesome. Another strategy
for addressing respiratory motion is the respiration-triggering method.
Several investigators have reported that respiratory triggering in T2-weighted
imaging allows extension of the acquisition time. The longer acquisition time
increases spatial resolution and signal-to-noise ratio (SNR), improving
liver-lesion contrast and detection of focal liver lesions
[9-12].
In the navigator-triggered prospective acquisition correction (PACE)
technique, virtual respiratory monitoring with navigator echoes is used to
trace the superoinferior movement of the diaphragm during the respiratory
cycle. In the conventional respiration-triggering method, changes in the
anteroposterior diameter of the chest cavity are measured with pressure
transducers
[13-15].
The PACE technique is a real-time gradient-recalled echo fast low-angle shot
navigator sequence for monitoring diaphragmatic movement. Sampling data about
the respiratory cycle are used to synchronize data acquisition to the
underlying MRI sequence. The purpose of our study was to compare the efficacy
of the following three sequences in the detection and characterization of
focal liver lesions: TSE performed with navigator-triggered PACE,
respiration-triggered TSE, and HASTE performed with navigator-triggered
PACE.
Materials and Methods
Patients
Our institutional review board approved this retrospective study, and
patient informed consent was not required. From September 2004 to July 2005,
60 consecutively registered patients with findings suggestive of focal liver
lesions on previous sonography (n = 20), contrast-enhanced CT
(n = 28), or both (n = 12) underwent MRI examination of the
liver. Eleven patients were excluded for the following reasons: final
diagnosis not established (n = 6), more than 10 lesions (n =
4), and respiratory monitoring impossible because of severe lack of
cooperation and motion restriction (n = 1). Therefore, a total of 49
patients (32 male and 17 female patients; mean age, 59 years; range, 15-77
years) were included in the study.
The 49 study patients had a total of 86 focal liver lesions. The final
diagnoses (Table 1) were based
on histologic findings, clinical evidence, typical CT and MRI findings, and
laboratory findings. Eleven patients had two kinds of diagnoses. Histologic
specimens were obtained with surgical biopsy or percutaneous needle biopsy.
The clinical evidence of malignant tumors was obtained with follow-up iodized
oil-enhanced CT after transcatheter arterial chemoembolization in patients
with hepatocellular carcinoma or on the basis of an increase in size and
number of tumors over time on serial follow-up contrast-enhanced CT
examinations of patients with metastasis. The clinical diagnosis of liver
abscess was based on a decrease in size and number of lesions over time on
serial follow-up imaging studies after antibiotic therapy.
MRI Technique
MRI was performed on a 1.5-T system (Magnetom Sonata Maestro, Siemens
Medical Solutions) with high-performance gradients (maximum gradient strength,
40 mT/m; peak slew rate, 200 mT/m/ms). A dedicated 12-element surface-coil
array was used as the radiofrequency receiver. The section thickness was 5 mm
with a 1.5-mm interslice gap for all T2-weighted sequences. All T2-weighted
images were acquired in the axial plane with parallel imaging. A generalized
autocalibrating partially parallel acquisitions algorithm was used with an
acceleration factor of two and 34 extra reference lines. The imaging range
covered the entire liver in all subjects. The phase-encoding direction was
anterior to posterior. Fat suppression was not applied. The protocol was
composed of a free-breathing T2-weighted TSE sequence with navigator-triggered
PACE, a respiration-triggered T2-weighted TSE sequence, and a HASTE sequence
with navigator-triggered PACE. The technical parameters are listed in
Table 2.
PACE is a 2D navigator-based technique in which the position of the
diaphragm is repeatedly measured. The coronal 2D gradient-echo fast low-angle
shot sequence was performed with the following parameters: TR/TE, 7.1/3.4;
slice thickness, 10 mm; field of view, 256 x 512 mm; bandwidth, 260
Hz/pixel; flip angle, 3°; matrix size, 256 x 12. Measurement of the
position of the diaphragm was repeated every 150 milliseconds so that a
continuous curve of the position was generated. Within each navigator image, a
window (96 x 32 mm2) was moved in the readout direction
within a search range (± 100 mm) relative to a similar window in the
reference image. With the technique, the position of the diaphragm before
measurement of a new image stack was compared with the position in the first
acquired image stack. The position of the following measurements was
prospectively corrected. The TR was 1 multiplied by the respiratory cycle.
In the respiration-triggered T2-weighted TSE sequence, the respiratory
bellows signal is used to generate a respiratory trigger. The trigger point
within the respiratory cycle can be selected. We chose a trigger point just
before end expiration with a threshold of 20% so that data acquisition would
occur during a period of reduced respiratory motion. The mean acquisition
times of the PACE TSE, respiration-triggered TSE, and PACE HASTE sequences
were 3.18, 6.17, and 3.17 minutes, respectively.
Qualitative Image Analysis
MR images were retrospectively analyzed by two experienced radiologists
with 6 years of experience in abdominal MRI. The reviewers were blinded to
patient identification, clinical history, biopsy results, and other imaging
findings. Image review was separated into three sessions at 4-week intervals.
Images with only one of the three free-breathing T2-weighted sequences were
reviewed at each session and were independently assessed by the two
reviewers.
Image Quality
The reviewers graded the overall image quality of each T2-weighted sequence
using the following 5-point scale: 1, unacceptable; 2, poor; 3, fair; 4, good;
5, excellent. The presence of artifacts such as respiratory ghosting, vascular
pulsation, peristalsis, and susceptibility was graded 1, severe; 2, moderate;
3, mild; 4, minimal; 5, absent. Depiction of the intrahepatic vessels was
assessed with the following criteria: 1, unacceptable (invisible main portal
vein); 2, poor (only main portal vein visible); 3, fair (only main branch of
portal vein visible); 4, good (peripheral portal vein sometimes visible); 5,
excellent (clearly visible peripheral portal vein). Image sharpness was graded
1, unacceptable; 2, poor; 3, fair; 4, good; 5, excellent.
Lesion Detection and Characterization
Both reviewers independently evaluated the overall number of hepatic
lesions per sequence on a segment-by-segment basis. For each pulse sequence,
the reviewers recorded the location of visible abnormalities and then assigned
one of five confidence levels: 1, definitely absent; 2, probably absent; 3,
possibly present; 4, probably present; 5, definitely present. The reviewers
then characterized each detected lesion using a 5-point scale: 1, definitely
benign; 2, probably benign; 3, indeterminate; 4, probably malignant; 5,
definitely malignant.
Quantitative Analysis
Quantitative image analysis was performed by an abdominal radiologist who
measured the signal intensity of the liver and the focal liver lesion and the
SD of the background noise using operator-defined regions of interest for each
image. This radiologist did not participate in the qualitative image analysis.
Signal intensity in the liver was measured in the same location in each
sequence and in areas devoid of a large intrahepatic vessel or prominent
artifacts. For all measurements, the size of the region of interest was
identical in all three sequences. The SD of the background noise was measured
in the largest possible region of interest positioned in the phase-encoding
direction outside the abdominal wall. For measurement of the focal liver
lesions, the region of interest was positioned to avoid necrotic foci. For
small hepatic lesions, the image was magnified to place a region of interest.
Liver SNR (SIliver/SDnoise) and lesion-to-liver
contrast-to-noise ratio (CNR) ([SIlesion -
SIliver]/SDnoise), where SI is signal intensity, were
calculated.
Statistical Analysis
The statistical significance of the data from the qualitative analysis for
image quality was determined with Friedman two-way analysis of variance by
ranks (SPSS version 12.0 for Windows, SPSS). Receiver operating characteristic
curve analysis was performed to evaluate lesion detection and characterization
for the reference standard
[16]. In interpretation of
each imaging sequence, each reviewer's performance and a composite performance
that combined the performances of all reviewers were evaluated by means of
calculation of the area under the receiver operating characteristics curve
(Az) with MedCalc software version 8.1 for Windows (MedCalc). The
relative sensitivity of lesion detection and differentiation of malignant from
benign tumors was calculated for lesions allocated a rating of 3 or higher.
The individual and composite sensitivities that combined the performance of
all reviewers were compared by use of the generalized linear mixed models in
SAS 8.02 for Windows (SAS Institute).
To assess interobserver variability in interpreting the images, the
weighted kappa statistics of SAS version 8.02 were used to measure the degree
of agreement between the two interpreters
[17]. A kappa value up to 0.40
indicated positive but poor agreement, a value of 0.41-0.75 indicated good
agreement, and a value greater than 0.75 indicated excellent agreement. The
liver SNR and lesion-to-liver CNR data were compared for each sequence by use
of the linear mixed models of SAS version 8.02. A value of p <
0.05 indicated a statistically significant difference.
Results
Qualitative Analysis
Image quality—For overall image quality, the PACE TSE and
respiration-triggered TSE sequences were superior to the PACE HASTE sequence.
Images obtained with the PACE TSE sequence were of slightly better quality
than those obtained with the respiration-triggered TSE sequence, but the
difference was not statistically significant. The PACE HASTE sequence produced
images with fewer artifacts than did the PACE TSE and respiration-triggered
TSE sequences. PACE TSE was the best sequence for depiction of intrahepatic
vessels and image sharpness and was followed by respiration-triggered TSE and
PACE HASTE (Fig. 1A,
1B,
1C and
Table 3).
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Fig. 1A —64-year-old man with hepatic metastasis of colon cancer. MR image
obtained with prospective acquisition correction turbo spin-echo sequence
shows tumor with greater conspicuity, more intrahepatic vessels, and greater
sharpness than do B and C.
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Fig. 1B —64-year-old man with hepatic metastasis of colon cancer.
Respiration-triggered turbo spin-echo MR image shows motion artifacts.
Depiction of tumor is worse than in A but better than in C.
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Lesion detection and characterization— The individual and
mean Az values for the three MRI pulse sequences for
lesion detection and characterization are shown in
Table 4. In lesion detection
the PACE TSE sequence had the highest Az value followed by
the respiration-triggered TSE and PACE HASTE sequences (Fig.
2A,
2B,
2C). There was no statistically
significant difference between PACE TSE and respiration-triggered TSE. The
individual and mean Az values of the PACE TSE sequence
were significantly higher than those of the PACE HASTE sequence. PACE TSE had
the best diagnostic performance for differentiating malignant from benign
lesions and was followed by respiration-triggered TSE and PACE HASTE. There
was no statistically significant difference between PACE TSE and
respiration-triggered TSE. The individual and mean Az
values of the PACE TSE and respiration-triggered TSE sequences were
significantly higher than those of the PACE HASTE sequence.
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TABLE 4: Area Under the Receiver Operating Characteristics Curve for Detection of
Lesions and for Differentiation of Malignant from Benign Lesions
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Fig. 2A —62-year-old man with hepatocellular carcinoma. MR image obtained
with prospective acquisition correction turbo spin-echo sequence clearly
depicts sharpness of contours of liver and hepatic tumor and shows
intrahepatic vessels.
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The sensitivities in detection of lesions and differentiation of malignant
from benign tumors with each pulse sequence are shown in
Table 5. For detecting lesions,
one reviewer had significantly better diagnostic performance with the PACE TSE
sequence than with the respiration-triggered TSE sequence. The composite
sensitivity of the PACE TSE sequence was significantly higher than that of
either the respiration-triggered TSE or the PACE HASTE sequence (Figs.
3A,
3B,
3C and
4A,
4B,
4C). For the two reviewers,
the individual sensitivity with PACE TSE was significantly higher than that
with PACE HASTE. In differentiating malignant from benign tumors, one reviewer
had significantly better diagnostic performance with PACE TSE than with
respiration-triggered TSE. The composite sensitivity of PACE TSE was higher
than that of respiration-triggered TSE, but the difference was not
statistically significant. For the two reviewers, the individual sensitivity
of PACE TSE was significantly higher than that of PACE HASTE. The kappa values
for the two reviewers, which were calculated on the basis of each
interpreter's confidence level in detection and characterization in the
receiver operating characteristics analysis, ranged from 0.728 to 0.929
(Table 6). Interobserver
agreement for the two reviewers was good and excellent with regard to the
presence and characterization, respectively, of lesions.
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Fig. 3A —58-year-old woman with complex cyst and pseudolesion. All three
sequences clearly show hyperintense cyst (arrow) in right anterior
superior segment. MR image obtained with prospective acquisition correction
turbo spin-echo sequence shows ghosting artifacts more prominently than does
C and clearly shows hepatic vein (arrowhead), which appears as
pseudolesion in C.
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Fig. 3B —58-year-old woman with complex cyst and pseudolesion. All three
sequences clearly show hyperintense cyst (arrow) in right anterior
superior segment. Respiration-triggered turbo spin-echo MR image shows
ghosting artifacts more prominently than does C.
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Fig. 3C —58-year-old woman with complex cyst and pseudolesion. All three
sequences clearly show hyperintense cyst (arrow) in right anterior
superior segment. MR image obtained with prospective acquisition correction
HASTE sequence shows hyperintense pseudolesion (arrowhead) in
anteromedial position in relation to complex cyst. One of two reviewers
misinterpreted lesion as tumor.
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Fig. 4A —59-year-old man with hepatocellular carcinoma. MR image obtained
with prospective acquisition correction turbo spin-echo sequence shows
slightly hyperintense nodule (arrow) more clearly than do B
and C.
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TABLE 6: Interobserver Agreement for Detection of Lesions and for Differentiation
of Malignant from Benign Lesions
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Quantitative Analysis
The quantitative results of assessments of the mean liver SNR and
lesion-to-liver CNR with each pulse sequence are shown in
Table 7. The mean liver SNR and
lesion-to-liver CNR were highest with the PACE HASTE sequence, followed by the
respiration-triggered TSE and PACE TSE sequences. The SNR with the PACE HASTE
sequence was significantly higher than that with either the PACE TSE or the
respiration-triggered TSE sequence. For benign lesions, the mean
lesion-to-liver CNR with the PACE HASTE sequence was significantly higher than
that with the PACE TSE sequence and was slightly higher than that with
respiration-triggered TSE but not statistically significantly so. For
malignant lesions, there was no statistically significant difference in mean
lesion-to-liver CNR in any of the three sequences.
Discussion
Artifacts produced by physiologic motion are a challenge to the use of MRI
for abdominal imaging [18].
Various types of T2-weighted imaging have been developed to improve image
quality. Breath-hold TSE T2-weighted sequences are commonly used because they
effectively eliminate respiratory motion artifacts because of their short
acquisition time, good image quality, and high diagnostic performance
[6-8,
19]. Nevertheless, some
patients cannot hold their breath efficiently. Patients referred for hepatic
MRI are often in poor general condition because of underlying malignant
disease and pain. Limiting the number of slices and the section thickness
because of a restricted breath-hold yields lower-resolution images, which can
be a limitation to detection of small hepatic lesions
[11,
20]. The use of multiple
refocusing pulses in breath-hold TSE T2-weighted imaging causes a decrease in
the signal intensity of solid liver tumors because of the magnetization
transfer effect, which can result in low conspicuity of malignant tumors
[21,
22].
Respiratory monitoring is a previously described technique
[10,
23,
24] used in an attempt to
prospectively avoid motion artifacts by use of respiratory signals to control
image acquisition. Various techniques have been used to monitor respiration,
including registration with bellows systems in combination with a strain
gauge, application of elastic breathing belts, temperature monitoring with a
face mask, and navigator echoes. These free-breathing techniques of
respiratory monitoring allow extension of the acquisition time and potentiate
an increase in the crucial parameters, which can lead to sharper anatomic
details, equal or less phase ghosting, and improvement in lesion-liver
contrast [10]. Use of a larger
matrix size and thin sections in free-breathing techniques with respiratory
monitoring can enhance the detectability of small-diameter hepatic lesions
[11,
12].
The navigator-triggered PACE technique is a new method of respiratory
monitoring that does not require additional hardware. The examination is not
interrupted owing to dislocation of the monitoring device and is free of
susceptibility to artifacts due to additional hardware
[15]. Monitoring of
respiratory motion is done with navigator echoes that repeatedly acquire MR
signals from the right diaphragmatic dome as it moves during respiration. The
respiratory trace sampled with the navigator portion of the sequence is used
to synchronize data acquisition according to the patient's respiratory cycle.
As soon as the series of detected diaphragmatic positions fulfills the trigger
condition during the quiet phase near end expiration, the sequences stop
repeating, and the navigator executes the anatomic imaging sequences and
acquires a predefined number of slices.
The results of our study show that PACE TSE is superior to
respiration-triggered TSE for most qualitative evaluations. The PACE TSE
sequence was superior to the respiration-triggered TSE sequence in both lesion
detection and characterization. Our findings suggest that the PACE technique
enables more accurate positioning of image stacks because a spatial profile of
the right diaphragm is displayed for changing the vertical dimension of the
chest cavity, as in an actual respiratory waveform. In the
respiration-triggering method, however, the signal is processed to produce a
linear relation between signal amplitude and circumferential changes, that is,
anterior and posterior movement, of the body wall. Therefore, use of the PACE
TSE sequence reduced respiratory artifacts and improved detection and the
ability to make a differential diagnosis of intrahepatic lesions. Because the
respiratory cycle is displayed during acquisition, the technician can identify
incoherent respiration early and has clear feedback on whether the patient is
following respiratory instructions. We used an echo-train length of 13 for
PACE TSE. As Low et al. [25]
reported, the use of this echo-train length may decrease blurring compared
with the echo-train length of 17 used for respiration-triggered TSE, and
better diagnostic performance may be achieved. In addition, the PACE TSE
sequence used in our study yielded a time saving of nearly 50% compared with
the duration of respiration-triggered TSE.
The results of our qualitative analysis regarding lesion detection and
characterization with the PACE TSE and respiration-triggered TSE sequences
were superior to those with PACE HASTE. In PACE HASTE, as in previously
documented single-shot TSE sequences, lesions of intermediate T2-weighted
signal intensity in which there are few protons in macromolecules and their
associated bound water can be obscured
[21,
22] and image quality
degraded. In addition, in our study the PACE HASTE sequence was performed with
a small matrix size compared with those of the PACE TSE and
respiration-triggered TSE sequences.
Our study also showed that the PACE HASTE sequence is superior to PACE TSE
and respiration-triggered TSE for quantitative evaluation, including
measurement of SNR of the liver and lesion-to-liver CNR. These results may be
attributed to the decrease in image noise related to the low amount of motion
artifact and to the wide receiver bandwidth of 475 Hz/pixel in the PACE HASTE
sequence, as opposed to 260 Hz in PACE TSE and 210 Hz in respiration-triggered
TSE. The mean liver SNR and lesion-to-liver CNR were lowest in the PACE TSE
sequence. However, the mean lesion-to-liver CNR of solid malignant tumors on
PACE TSE images was equal to or slightly lower than that on images obtained
with the other sequences. The mean lesion-to-liver CNR of benign nonsolid
lesions was distinctly lower. We believe the short echotrain length of the
PACE TSE sequence may cause a smaller magnetization transfer effect, which may
explain the increase in mean lesion-to-liver CNR of solid lesions
[21,
22] relative to that of
nonsolid liver lesions.
There are advantages to the use of a fat-suppression technique in liver
imaging. Fat suppression can increase the lesion-to-liver CNR because normal
liver usually contains fat. Fat suppression also decreases ghosting artifacts
[26,
27], which are caused by the
high signal intensity from fat
[28] and the near-field
effect. However, fat saturation was not performed in the three free-breathing
techniques in our study. The reasons were the need for increased imaging time,
unsatisfactory image quality due to incomplete suppression of fat in areas
close to the body array coil
[29], obscuring of
hepatocellular carcinoma with fatty metamorphosis
[30], and decreased definition
of the margins of extrahepatic organs.
We recognize that our study had limitations. First, our reference standard
was suboptimal for lesion detection and characterization. However, a more
rigorous standard, such as pathologic confirmation, would have been impossible
for all patients, especially those with benign lesions. Second, recall bias
was unavoidable in cases with a distinct appearance. We tried to minimize
recall bias by allowing a 4-week interval between reviewing sessions. Third,
the PACE HASTE images were acquired with a matrix setting of 256, whereas the
PACE TSE and respiration-triggered TSE images had a matrix setting of 384. The
different settings for this examination parameter were chosen because
increasing the matrix size in the PACE HASTE sequence decreases image quality
and lesion conspicuity owing to an increase in echo-train length. Therefore,
selection of different values may be justified, although a comparison with
similar values would have been more appropriate. A fourth limitation was that
our study population was relatively small. Definite statistical differences
might have been shown in the qualitative analysis of the PACE TSE and
respiration-triggered TSE sequences. We believe large prospective studies are
needed to support the utility of PACE TSE in T2-weighted imaging of focal
liver lesions.
In our study the PACE TSE sequence had better diagnostic performance for
lesion detection and characterization than did the other free-breathing
techniques. The PACE HASTE sequence, however, had the best mean liver SNR and
lesion-to-liver CNR. The navigator-triggered PACE technique is a valid method
of T2-weighted imaging of focal liver lesions and may replace conventional
respiration-triggering techniques.
Acknowledgments
We thank Tae Kyoung Kim, Department of Medical Imaging, University Health
Network, University of Toronto, Toronto, Ontario, Canada, for reviewing the
manuscript and for providing useful suggestions. We thank Bonnie Hami for
editorial assistance in preparing the manuscript. We also extend our
appreciation to Chang Gil Hyun and Jang Sik Oh for contributions to the
study.
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Abstract
Introduction
