Yonago Acta medica 1996;39:163–170

Assessment of the Image Quality and Tumor Detectability of BreathHold T2-Weighted Imaging of Liver Tumors using a Fast Gradient MR
SystemKotaro Yoshida, Yuji Suto, Shuji Sugihara and Yukiko Tokuda
Department of Radiology, Faculty of Medicine, Tottori University, Yonago 683, Japan
Fourteen patients with various types of focal liver tumors were imaged with turbo spinecho (TSE), breath-hold TSE (BH-TSE) and half-Fourier single-shot TSE (HASTE)
pulse sequences using a fast gradient magnetic resonance imaging (MRI) system. We
compared the T2-weighted images of the liver with the TSE, BH-TSE, HASTE andconventional spin-echo (SE) pulse sequences in order to determine whether those fast
T2-weighted images, including fat suppressed images, could replace SE images. In
quantitative and qualitative analysis, the fast T2-weighted images were slightly superior
to the SE images, but they were inferior in the conspicuousness of liver tumor to the SE
images. These findings suggest that the fast T2-weighted images can shorten theexamination time of the liver MRI, but cannot replace the T2-weighted SE images
because of the low conspicuousness.
Key words: breath-hold MRI; fast gradient; T2-weighted image; liver tumor

method shortened the time needed for theexamination and was more useful than the SE
method for detection and diagnosis of liver
tumors (Yoshida et al., 1996).
In this study, we quantitatively and qualitatively compared the image quality and thedetectability of liver tumors by images of theT2-weighted SE (SET2) and various fast sequences. The fast sequences were the turbo SE(TSE) method with breathing at rest, breathhold TSE method (BH-TSE) and half-Fourier
single-shot TSE method (HASTE) with a fasterexamination speed and heavier T2-weighted
image than ordinary TSE (Hening et al., 1986;
Fujii, 1994). We also compared their fat
saturation (fs) images with those by SET2 andexamined whether these breath-hold T2weighted imaging techniques can replace
SET2.

Magnetic resonance imaging (MRI), especiallyin T2-weighted images, has been reported tohave an excellent contrast resolution and to be
useful in detection and diagnosis of tumorous
lesions of the liver (Rammeny et al., 1989;
Egglin et al., 1990). However, by the conventional spin-echo (SE) method, a long examination time is needed for scanning, and deterioration of the image quality due to various artifacts
including respiratory artifacts has been aproblem (Wood et al., 1988). Recently, however, whole liver imaging with breath-holding
has become possible by both T1-weighted andT2-weighted images due to the development ofvarious fast imaging methods and increased
availability of the fast gradient MRI systems(Winkler et al., 1989; Siewert et al., 1994).
We previously reported that the breath-holdT1-weighted imaging by the gradient-echo

Abbreviations: BH-TSE, breath-hold TSE; CNR, contrast-to-noise ratio; CNRSP, spleen-liver CNR; CNRT,
tumor-liver CNR; FOV, field of view; fs, fat saturation; HASTE, half-Fourier single-shot TSE; MRI,
magnetic resonance imaging; MTC, magnetization transfer contrast; ROI, regions of interest; SE, spin-echo;
SET2, T2-weighted SE; SI, signal intensity; SDBKG , SD of background; SIL, SI of the liver; SI SP, SI of thespleen; SIT, SI of the tumor; SNR, signal-to-noise ratio; TE, echo time; TR, repetition time; TSE, turbo SE

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Table 1. Imaging parameters of each pulse sequence
Parameter

Sequence
SET2

TSE

BH-TSE

HASTE

Repetition time (ms)
1800
3500
4500
10.9
Echo time (ms)
80
99
138
87
Echo train length
11
29
128
No. of acquisitions
2
5
1
1
Matrix size
157 × 256
176 × 256116 × 256
128 × 256
Imaging time
9 min 28 s
4 min 43 s
23 s
12 s
BH-TSE, breath-hold TSE; HASTE, half-Fourier single-shot TSE; SET2, conventional T2 weighted spinecho; TSE, turbo spin-echo.

Subjects and Methods
The subjects were 14 patients with 42 tumorous
lesions of the liver (11 males and 3 females
ranging in age from 33 to 83 years, mean 63.5
years) who underwent MRI between June, 1995
and March, 1996. The lesions were 31 nodes ofhepatocellular carcinoma, 6 nodes of metastatic
liver tumor, and 5 nodes of liver cysts diagnosed on the basis of the clinical findings andimage findings. Quantitative evaluation wasmade in 26 nodes detected by SET2, TSE, BHTSE, HASTE and their fs images, and qualitative evaluation was made in 42 nodes detectedby anyone of these imaging methods. The
masses were 0.6–10.5 cm (mean 3.8 cm) in diameter.
A 1.5 T fast gradient superconducting MRI
system (Magnetom Vision: Siemens, Erlangen,Germany, maximum gradient magnetic field
intensity 25 mT/m) was used. A phased arraycoil was used in all patients. Table 1 shows imaging conditions. The fs images were obtainedwith the same parameters using frequencyselective saturation pulses (Haase et al., 1985;
Hata and Tada, 1994). Transaxial images at aslice thickness of 10 mm, a gap of 1 mm and afield of view (FOV) of 35–42 cm were obtained. A rectangular FOV with a 6/8 of 7/8 phase
encode reduction was used depending on thebody, and a presaturation pulse was impressedat the upper and lower ends of the imaging
region.
Quantitative evaluation was made by determining the region-of-interest (ROI) over theliver, spleen and solid part of the tumor as
widely as possible and by avoiding blood vessels
in each imaging method. Also, ROI was determined as widely as possible over the background on the abdominal side of each patient,which was the phase encoding direction. Each
ROI was 35 pixels or wider, and the mean
signal intensity (SI) and SD per pixel of liver(SI L), spleen (SI SP), tumor (SI T) and background (SDBKG) were calculated. The signalto-noise ratio (SNR) of the liver, spleen-liver
contrast-to-noise ratio (CNRSP) and tumor-liver
contrast-to-noise ratio (CNRT) were calculated
as follows: SNR = SIL/SDBKG, CNRSP = (SISP –SIL)/SDBKG, CNR T = (SI T – SIL)/SDBKG. The
results of SET2 and fast imaging methods werecompared with Student’s t-test when thevariance was equal and by Welch’s t-test whenthe variance was unequal.
Qualitatively, each image was evaluated by
the following 6 items: i) motion artifacts bybreathing and vascular pulsation, ii) liverspleen and liver-tumor contrast, iii) visibility of
intrahepatic vessels, iv) visibility of tumor
structures (margin, septum, capsule), v) sharpness of the liver margin and vi) overall image
quality, taking into consideration the assessments in i) to vi). The assessments done by 3
radiologists were numerically represented in
the following 5 grades and numerical rating:poor (1 point); fair (2 points); moderate (3points); good (4 points); or excellent (5 points).
Based on this numerical rating, comparativeevaluation of the quality of each image wasmade with the Wilcoxon matched-pairs signedrank test. In addition, the number of nodes

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Breath-hold T2 weighted imaging of liver

visualized by each image was compared according to the diameter of the nodes (less than 1 cm,
1 cm or larger, less than 2 cm, 2 cm or larger,
less than 3 cm and 3 cm or larger).

Results
Table 2 shows the results of the quantitativeevaluation. The SNR of the liver was significantly higher in TSEfs (P < 0.05) and HASTE(P < 0.01) than in SET2 or TSE. No significant
differences were observed among the other fast
imaging techniques. The CNR SP showed nosignificant difference be tween SET2 and fast
imaging methods with and without breathholding. The CNRT was significantly higher in
HASTE (P < 0.05) and HASTEfs (P < 0.01) thanin SET2 and in TSEfs (P < 0.01). It was alsosignificantly higher in HASTE (P < 0.05), and
HASTEfs (P < 0.01) than in TSE.
Figure 1 shows the results of the qualitative
image evaluation. Respiratory artifacts weregreater in TSE (P < 0.05) but were significantly
smaller in TSEfs (P < 0.05), HASTE (P < 0.01)
and HASTEfs (P < 0.05) than in SET2. Vascular
artifacts were greater in BH-TSEfs (P < 0.05)
but were significantly smaller in TSEfs (P < 0.05),
HASTE (P < 0.05) and HASTEfs (P < 0.05).
Liver-tumor contrast was significantly better in
TSEfs (P < 0.01) and BH-TSEfs (P < 0.05), andliver-spleen contrast was significantly better in
TSEfs (P < 0.01). In the visibility of tumor

structures, the information concerning thecapsule and the internal structure such as themosaic structure was richer in TSE (P < 0.05),
TSEfs (P < 0.01), BH-TSEfs (P < 0.05) andHASTEfs (P < 0.05). The visibility of intrahepatic vessels was inferior in TSEfs (P < 0.05).
The sharpness of the liver margin was superior
in TSE (P < 0.05), and BH-TSE and BH-TSEfs(P < 0.01). The overall image quality was better in TSEfs (P < 0.05) than in SET2 but was not
significantly different in other methods. Figure
2 shows a case of hepatocellular carcinoma in
the left hepatic lobe.
Table 3 compares the number of tumors detected by each image. Tumors of all sizes weredetected most clearly in SET2 except that ahepatocellular carcinoma of 3.5 cm in diameter
located in the lower margin of the liver was not
visible.

Discussion
Various fast T2-weighted MRI techniques havebeen developed, and the imaging time wasshortened in the central nervous system, headand neck, and pelvic regions (Feinberg andOshio, 1991; Jones et al., 1992; Nghiem et al.,1992). In the abdominal region, however, respiratory artifacts cannot be reduced by shorteningof the imaging time, and the problem of image
deterioration due to respiratory movements hasremained (Stalk et al., 1987). However, T2-

Table 2. Results of quantitative evaluation in each imaging sequence
Sequence

Parameter
Liver SNR

Contrast

CNRT

CNR SP

SET2
10.1 ± 3.6
0.30 ± 0.13
11.3 ± 7.5
14.2 ± 4.4TSE
7.6 ± 3.4
0.37 ± 0.13
8.5 ± 4.4
11.4 ± 5.5
TSEfs
17.0 ± 4.1*††
0.37 ± 0.14
21.8 ± 12.2††
19.4 ± 10.5
BH-TSE6.8 ± 2.7
0.43 ± 0.20
15.7 ± 14.1
12.1 ± 4.5
BH-TSEfs
8.3 ± 2.8
0.45 ± 0.17*
17.2 ± 13.4
14.9 ± 4.5
HASTE
15.4 ± 7.4
0.35 ± 0.21
51.8 ± 55.6*†
14.5 ± 10.7
HASTEfs
24.9 ± 7.3**††0.40 ± 0.20
32.9 ± 18.7**††23.3 ± 16.3
CNRSP, spleen-to-liver contrast-to-noise ratio; CNR T: tumor-to-liver CNR; fs, fat-saturation; SNR, signalto-noise ratio. The other abbreviations are the same as in Table 1.
* P < 0.05, **P < 0.01 to SET2.
† P < 0.05, ††P < 0.01 to TSE.

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K. Yoshida et al.

14

J

J
J

12

E

J
10

J

E

E

E

E
8

E

6

4

2

SET2
0

TSE11
breathingvascular pulsation

contrast-T

contrast-SP
TSE11fs

12

J
10

BH-TSE

J
E

E

E

E

J

E

E

BH-TSEfs
HASTE

8

HASTEfs
6

4

2

0

nodule structure

clarity of liver

overall quality

vesselFig. 1. Qualitative assessment of the image quality on fast, chemical fat-saturation (fs) fast and conventional
T2-weighted spin-echo (SE) magnetic resonance (MR) images (E P < 0.05, J P < 0.01). Respiratory artifacts
were greater in turbo SE (TSE) (P < 0.05) but were significantly smaller in TSEfs (P < 0.05), half-Fourier
single-shot TSE (HASTE) (P < 0.01) and HASTEfs (P < 0.05) than in T2-weighted SE (SET2). Vascular
artifacts were greater in breath-hold TSE fs (BH-TSEfs) (P < 0.05) but were significantly smaller in TSEfs (P< 0.05), HASTE (P < 0.05) and HASTEfs (P < 0.05). Liver-tumor contrast was significantly better in TSEfs(P < 0.01) and BH-TSEfs (P < 0.05), and liver-spleen contrast was significantly better in TSEfs (P < 0.01). In
the visibility of tumor structures, the information concerning the capsule and the internal structure such as themosaic structure was richer in TSE (P < 0.05), TSEfs (P < 0.01), BH-TSEfs (P < 0.05) and HASTEfs (P <0.05). The visibility of intrahepatic vessels was inferior in TSEfs (P < 0.05). The sharpness of the liver
margin was superior in TSE (P < 0.05), and BH-TSE and BH-TSEfs (P < 0.01). The overall image quality
was better in TSEfs (P < 0.05) than in SET2 but was not significantly different in other methods.

weighted imaging methods with breath-holds
such as TSE and HASTE have become possible
due to recent improvements in the instrument(Winkler et al., 1989; de Lange et al., 1994;
Taupitz et al., 1995; Rydberg et al., 1995).

By TSE, T2-weighted images can be obtained in a shorter time than SE by phase-encodingof each echo obtained by several 180 pulses per
excitation pulse. By HASTE, an accelerated
version of TSE, one image can be obtained inFig. 2 (opposite page). MR images for a 76-year-old patient with hepatocellular carcinoma (arrows). The
SET2 (A), TSE (B), TSEfs (C), BH-TSE (D), BH-TSEfs (E), HASTE (F) and HASTEfs (G) images show
hepatocellular carcinoma in the left hepatic lobe. The contrast of tumor in SET2 and TSEfs is better than inother fast images. Respiratory artifacts in TSE images are greater than in SET2 and other fast images.

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K. Yoshida et al.

Table 3. Detectability of tumorous lesions on fast, chemical fat-saturation fast andconventional T2-weighted spin-echo MR images
Sequence
1 cm <≤ 1-2 cm <Tumor size (cm)
≤ 2-3 cm <

SET2
4 (3)
9 (1)
11 (1)
TSE
5 (1)
8 (1)
10 (1)
TSEfs
4 (1)
8 (1)
10 (1)
BH-TSE2 (1)6 (1)10 (1)
BH-TSEfs
2 (1)
5 (1)
10 (1)
HASTE
4 (1)
9 (1)
7 (1)
HASTEfs
4 (1)
9 (1)
7 (1)
( ), cyst.
The abbreviations are the same as in Tables 1 and 2.

about 1 s by producing 180 pulses 128 times pereach excitation pulse and phase-encoding ofeach echo (Hening et al., 1986; Fujii, 1994).
However, TSE has been reported to differ fromSE in that it is affected markedly by the magnetization transfer contrast (MTC) effect, that thesusceptibility effect is small, and that edge enhancement effect is obtained (Wolf and Balaban,
1989; Melki and Mulkem, 1992). The contrast
of TSE images is also reported to be altered bychanges in the number of echo factors. In
HASTE, also, echoes near the end of the pulse
series are weakened in tissues with short T2 due
to attenuation of T2 during data accumulation,and the resolution in the phase-encoding direction
is reduced (Catasca and Mirowitz, 1994; Outwater
et al., 1994).
In quantitative evaluation, the liver SNR
was slightly lower in TSE and BH-TSEfs
images, but was similar to or higher in othermethods than in SET2. Especially, the SNR
was significantly higher in TSEfs, the CNR T
was significantly higher in HASTE, and both
SNR and CNRT were significantly higher in
HASTEfs than in SET2. In TSE, the signals of
adipose tissue are higher in SET2 so that artifacts of the abdominal wall associated withrespiratory motions are stronger, and the noise
is greater. This is probably why the SNR of theliver was slightly lower. In TSEfs, noise was
reduced by fs, and liver signals were higher
than in SET2 because of 5 signal acquisitions.
Therefore, the SNR of the liver was significantly higher than in SET2, unlike TSE. Also, the≤ 3 cm

Total

9
10
9
10
10
10
10

33 (5)
33 (3)
31 (3)
28 (3)
27 (3)
30 (3)
30 (3)CNRT was significantly higher in TSEfs images
than in TSE images, probably because tumorliver contrast was increased by fs with a resultant decrease in noise.
In BH-TSE with only 1 signal average, theMTC effect was increased with a boost in thenumber of echo factors, and fat signals wereintensified in relative terms as compared with
TSE, hence low liver signals. In addition, it
required 23-s breath holding, and the images
were markedly deteriorated if breath-holding
was insufficient. However, repetition time(TR) and effective echo time (TE) were sufficiently longer than in SET2 with resultant
enhancement of T2-weighting. Therefore, the
SNR of the liver was lower, but the CNRT was
higher than in SET2 although the differenceswere not significant.
In HASTE, the imaging time was 14 s (1 s/shot) so that sufficient breath-holding was
possible in nearly all patients. Therefore, no
deterioration of the image quality due to respiratory artifact was observed, and backgroundnoise was low. Since T2 relaxation has nearly
been complete in most tissues in the latter partof the echo train, intense T2-weighted images
can be obtained. Also, as each slice is obtained
as a single shot by this method, the MTC effect ofneighboring slices can be ignored. For thesereasons, the CNRT was significantly higher in
HASTE, and the SNR of the liver and CNRT
were significantly higher in HASTEfs than in
SET2 or TSE.

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Breath-hold T2 weighted imaging of liver

The results of the qualitative evaluation
generally reflected those of the quantitativeevaluation. In TSE, respiratory artifacts weresignificantly higher, but the TR and effective
TE were longer, so that the visibility of thetumor was excellent. TSEfs, in which respiratory artifacts are reduced by fs, were superior to
SET2 in all evaluation items except for the
sharpness of the liver margin. Of the breathhold imaging techniques, artifacts were small,and visualization of the tumors and sharpness of
the liver were excellent in BH-TSE, and HASTE
was better in some items than SET2 due tosmall artifacts. However, no significant difference as compared with SET2 was observed inoverall quality because of the low contrast resolution of the tumor due to the MTC effect in
BH-TSE and because of the low spatial resolution in HASTE.
Concerning the detectability of tumors,
SET2 was better than the fast imaging methods.
But one node in the lower margin of the liver,where respiratory movement is prominent, was
not visualized. Because of the strong respiratory
artifacts in TSE, the low contrast resolution of
the tumor due to the MTC effect in BH-TSE,
and the low spatial resolution in HASTE, thedetectability of the fast imaging methods werelow.

Conclusion
Fast T2-weighted MRI of liver tumors including breath-hold scanning techniques is inferior
to SET2 in the detectability of tumors and is notconsidered to replace completely SET2 as adiagnostic procedure despite its quantitativeand qualitative advantages.

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(Received August 19, Accepted September 26, 1996)

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