Yonago Acta medica 1996;39:73–81

Evaluation of Fast Gradient System Breath-Hold FLASH Imaging in the
Examination of Liver Tumors: Comparison with Conventional Spin-Echo
Pulse Sequences
Kotaro Yoshida, Yuji Suto, Takashi Kato, Shuji Sugihara and Naoto Ohmura
Department of Radiology, Faculty of Medicine, Tottori University, Yonago 683, Japan
Forty one patients with various types of focal liver tumors were imaged with a multisection fast low-angle shot (FLASH) gradient echo sequence using a fast gradient MR
system. We compared the T1-weighted images of the liver with the multisection FLASHand conventional spin-echo (SE) pulse sequences in order to determine whether FLASH
images could replace SE images. The multisection FLASH sequence provided a significantly higher signal-to-noise ratio (SNR), liver-spleen contrast, liver-spleen contrastto-noise ratio (CNR), liver-nodule CNR (P < 0.01) and liver-tumor contrast (P < 0.05)
than did the T1-weighted SE sequence. The overall image quality of the multisection
FLASH sequence was superior to that of the T1-weighted SE sequence (P < 0.05). The
signal intensity features of liver tumors with both sequences were almost the same.
There was a statistically mutual correlation in the signal intensity between hepatocellular
carcinomas and metastases. The detectability of liver tumors in FLASH sequences was
superior to that in SE sequences. These findings suggest that multisection FLASH
sequence imaging can replace T1-weighted SE sequence imaging.
Key words: breath-hold FLASH; fast gradient; MRI; liver tumor

quence (Haase et al., 1986), one of the fastest
imaging methods available, has improved thepossibility of clear imaging as compared withthat of the conventional low and slow gradientsystem.
In our present study, the breath-hold multisection FLASH imaging using the fast gradient
MR system was compared with the conventional SE imaging, quantitatively and qualitatively, and tumor detectability of each method
was evaluated, with computed tomography(CT) during arterial portography (CTAP) as thegolden standard, in order to determine whether
the FLASH method could replace the conventional SE method.

Magnetic resonance imaging (MRI) has an excellent contrast resolution, and its usefulness indetecting tumorous lesions of the liver and in its
diagnosis has been reported (Li et al., 1988;
Matsui et al., 1989; Rammeny et al., 1989;
Kadoya et al., 1992). In previous clinical evaluation of liver tumors, the spin-echo (SE) method
has been used. However, it has some drawbacks
in that the image deteriorates due to breathing
during the examination, and the time it takes toperform is too long (Felmlee and Ehman, 1987;
Edelmann et al., 1988; Mitchell et al., 1988).
With the recent installation of the fast gradient MR system, the image quality of the T1weighted fast low-angle shot (FLASH) se-

Abbreviations: CNR, contrast-to-noise ratio; CT, computed tomography; CTAP, CT during arterial portography; FLASH, fast low-angle shot; MRI, magnetic resonance imaging; Nstat, mean SI of background in thefrequency-encoding direction (statistical noise without ghosting artifacts); N sys, mean SI of background in thephase-encoding direction (large region of interest anterior to the abdomen, including ghosting artifacts); SE,
spin-echo; SI, signal intensity; SIbackground, SI of background; SIliver, SI of the liver; SIspleen, SI of the spleen,
SNR, signal-to-noise ratio; TE, echo time; TR, repetition time.

73

K. Yoshida et al.

Table 1. Results of quantitative evaluation
Parameter

Sequence
FLASH

SE

34.15 ± 12.60
13.98 ± 5.89*
0.16 ± 0.05
0.09 ± 0.07*
0.10 ± 0.08
0.08 ± 0.11**
CNR
9.44 ± 4.62
2.52 ± 1.98*
7.23 ± 7.22
2.06 ± 2.29*
Nsys/N stat
1.78 ± 2.37
5.12 ± 4.51*
CNR, contrast-to-noise ratio; Nstat, mean SI of background in the frequency-encoding direction (statisticalnoise without ghosting artifacts); Nsys, mean SI of background in the phase-encoding direction (large regionof interest anterior to the abdomen, including ghosting artifacts); Nsys /Nstat, ratio between systematic noiseand statistical noise; SI, signal intensity; SNR, signal-to-noise ratio at the liver.
Measurements obtained from the multisection fast low-angle shot (FLASH) images are significantly larger
than those obtained from conventional T1-weighted spin-echo (SE) images (*P < 0.01, **P < 0.05).
Liver SNR
Contrast

Liver-spleen
Liver-tumor (all nodes)
Liver-spleen
Liver-tumor (all nodes)

Subjects and Methods

262 ms and a TE of 4.8 ms, with a flip angle of
65˚. Signal averaging was 1 time. Imaging of
the entire liver was performed (imaging time 26s) with one breath held. The imaging matrix
was 100 × 256 and field of view 350 mm with afrequency band of 130 Hz/pixel. With theconventional low gradient 1.5 T MRI system,
the band width under nearly the same imaging
conditions was 300 Hz/pixel.
The 2 imaging methods were compared intumor detectability, with CTAP as the golden
standard. CTAP was performed at the time ofangiography which was performed 1 to 2 weeks
after MRI. The apparatus used was Somatom
Plus S (Siemens). Operating conditions were: 1
rotation/s, continuous 30 rotations, X-ray beamwidth 5 mm, and moving speed of the table at 5mm/rotation. One hundred milliliters of Iohexol
in concentration of 140 mgI/mL (Omnipaque140, Daiichi Seiyaku, Tokyo, Japan) was injected at a speed of 2.5 mL/s, and imaging by spiralscan was started 30 s after the injection was
begun.

The subjects were 41 patients (35 males and 6
females, ages ranging from 33 to 83 years withan average of 63.5 years) with tumorous lesionsof the liver who underwent MRI from
September 1994 to July 1995. None of thesepatients had a previous history of abdominal
operation.
Diagnosis of hepatic tumorous lesions wasmade based on the clinical findings, image
findings and histological findings. There were
27 patients with 74 nodes of hepatocellular
carcinoma, 8 patients with 65 nodes of metastatic liver tumor, 2 patients with 5 nodes of bile
duct carcinoma, 1 patient with 1 node of adenomatous hyperplasia, 4 patients with 10 nodes ofcavernous hemangioma and 2 patients with 13
nodes of liver cyst, the total number of nodes
being 174.
We used a 1.5 T fast gradient superconducting
MRI system (Magnetom Vision: Siemens,
Erlangen, Germany; gradient magnetic field
intensity 25 mT/m). In SE imaging, T1weighted images were obtained with a repetition time (TR) of 600 ms and an echo time (TE)of 17 ms, with 4 signal averagings. The imaging time was 4 min and 58 s. Slice thickness
was 10 mm, imaging matrix 123 × 256 and fieldof view 350 mm with a frequency band of 130
Hz/pixel.
In multisection FLASH imaging, T1weighted images were obtained with a TR of

Image analysis
Quantitative evaluation
In each image with FLASH and SE, mean
signal intensities (SIs) of liver (SIliver), spleen(SIspleen) and background (SIbackground) (outsideof the abdomen in the phase-encoding direction, including ghosting artifacts of both a74

Breath-hold FLASH imaging of liver tumors

Table 2. Results of quantitative evaluation of liver-tumor CNR and contrast
Parameter

Sequence
FLASH

SE

Hepatocellular carcinoma
0.07 ± 0.08
0.03 ± 0.12**
Metastasis0.13 ± 0.07
0.12 ± 0.08
Bile duct carcinoma
0.19 ± 0.07
0.22 ± 0.12
Hemangioma
0.11 ± 0.08
0.05 ± 0.05
Cyst
0.19 ± 0.06
0.16 ± 0.06
CNR
Hepatocellular carcinoma
3.49 ± 5.58
0.96 ± 2.25*
Metastasis9.56 ± 7.19
2.92 ± 1.73*
Bile duct carcinoma
14.92 ± 6.10
4.49 ± 0.61**
Hemangioma
6.85 ± 5.57
1.40 ± 1.25**
Cyst
11.83 ± 4.60
4.21 ± 3.16**
CNR, contrast-to-noise ratio.
Measurements from the multisection fast low-angle shot (FLASH) images are significantly larger thanthose from conventional T1-weighted spin-echo (SE) imaging (*P <0.01, **P < 0.05).

Contrast

points). Based on this numerical rating, comparative evaluation of the quality of FLASHand SE images was made with the Wilcoxon
matched-pairs signed-rank test. The following
5 items were checked: i) artifacts due to breathing and vascular pulsation, ii) contrast (liverspleen, liver-tumor), iii) capability to visualize
blood vessels, iv) clarity around the border ofthe liver and v) overall image quality, taking
into consideration the assessments in i) to iv).
In addition, SI in liver tumors was evaluatedusing the following 5 grades through consultation among the 3 radiologists: low, mild low,
iso, mild high and high. Based on the criteria,
comparison was made between FLASH and SE
images. To determine tumor detectability, CTAP
images and the images in each of the MRIs were
sorted into groups according to the size of thetumors, and a comparative evaluation was madein each method, and then on the overall detection rate.

respiratory and vascular nature) were determined with standard region-of-interest measurements. In addition, the signal-to-noise ratio(SNR) at the liver (SI liver/SI background ), liverspleen contrast [(SI liver – SI spleen )/(SIliver +SI spleen)] and contrast-to-noise ratio (CNR)[(SI liver – SIspleen)/SI background] were calculated.
The tumor contrast and CNR were also
calculated in the same manner. Contrast was ameasure for the differentiation of 2 tissues
without weighting. Furthermore, the mean SIsof background in the phase-encoding direction(large region of interest anterior to the abdomen, including ghosting artifacts) (N sys) and in
the frequency-encoding direction (statisticalnoise without ghosting artifacts) (N stat) were
determined with standard region-of-interest
measurements. In addition, the ratio between
systematic noise and statistical noise (N sys/Nstat)
was calculated as a measure for the intensity of
motion artifacts in each imaging method. In thestatistical analysis, Student’s t-test was used,with P < 0.05 as significant.

Results

Qualitative evaluation
Quantitative evaluation

Through consultation among 3 radiologists
with experience of 5 years or more in MRI,
images were evaluated in the following 4
grades and numerical rating: poor (1 point), fair
(2 points), good (3 points) and excellent (4The results of quantitative evaluation are shownin Tables 1 and 2. In Table 1, FLASH was significantly superior to SE in all items of evaluation as in the following: SNR, 144% increase75

K. Yoshida et al.

FLASH pulse sequence
0%

10%

20%

30%

40%

50%

60%

70%

80%

90%

100%

Motion artifact: breathing
Motion artifact: vascular pulsation
excellent
good
fair
poor

Contrast: liver-spleenContrast: liver-tumor
Visibility of intrahepatic vessels
Sharpness of hepatic margin
Overall image quality

SE pulse sequence
0%

10%

20%

30%

40%

50%

60%

70%

80%

90% 100%

Motion artifact: breathing
Motion artifact: vascular pulsation
Contrast: liver-spleenexcellent
good
fair
poor

Contrast: liver-tumor
Visibility of intrahepatic vessels
Sharpness of hepatic margin
Overall image quality

Fig. 1. Results of qualitative evaluation of image quality for 41 patients who underwent multisection fast
low-angle shot (FLASH) and spin-echo (SE) imagings. FLASH images were significantly superior (P < 0.05)
in each item of evaluation.

(P < 0.01); liver-spleen, increases of 77% in
contrast and 275% in CNR (P < 0.01); livertumor, increases of 25% in contrast (P < 0.05)
and 251% in CNR (P < 0.01); and Nsys/N stat, adecrease of 65% (P < 0.01).
Table 2 shows the results of evaluation bytype of tumor (excluding 1 patient with 1 nodeof adenomatous hyperplasia). In CNR, significant increases were observed with FLASHin all types of liver tumor: P < 0.01 in hepatocellular carcinoma and metastatic liver tumor,and P < 0.05 in bile duct carcinoma, hemangioma and liver cyst. As regards contrast, significant increases (P < 0.05) were observed inhepatocellular carcinoma. However, in othertypes of tumor, no significant differences wereseen.

Qualitative evaluation
Visual evaluation of images: Figure 1 shows
the results of visual evaluation by the 3 radiologists. FLASH images were significantly superior (P < 0.05) in each item of evaluation. Figure 2 shows a case of hepatocellular carcinoma
in which high signal intensity was actually observed.

76

Breath-hold FLASH imaging of liver tumors

Fig. 2. MR images for a 70-year-old patient with hepatocellular carcinoma (arrows). Upper images are froma multisection fast low-angle shot (FLASH) sequence, and lower images are from a spin-echo (SE) sequence.
The node on multisection FLASH sequences is of higher intensity and more distinct than on SE sequences.

all types. Included in these were 8 nodes whichwere indistinguishable as nodes in the liver.
These results were put into a two-by-fivecontingency table, and statistical comparison
was made approximately by χ2 test. As a result,a significant correlation was observed in SI
characteristics between hepatocellular carcinoma (P < 0.05) and metastatic liver tumor (P <0.05). In other types of tumor, however, no significant correlation was seen.
Evaluation of tumor detectability, by size oftumor, with FLASH and SE methods in comparison with CTAP is shown in Table 4. The 17
nodes smaller than 1 cm detected with CTAP inhepatocellular carcinoma and liver cyst were
not detectable with FLASH or SE. In detectionof tumors of 1 cm or larger, the detection rate
was greater for FLASH than for SE. With thedetection rate of CTAP as 100%, the detection
rate of FLASH and SE was 79.9% and 73.6%,
respectively.

Comparison in SI characteristics in hepatic tumor and tumor detectability: SI characteristics in liver tumors with FLASH and SE are
shown in Table 3. In 31 nodes of hepatocellular
carcinoma, 64 nodes of metastatic liver tumor,
4 nodes of hemengioma and in all of the nodesof bile duct carcinoma and liver cyst, a lower
signal was observed as compared with thesignal of nontumorous liver tissue. Of thenodes of hepatocellular carcinoma, 14 nodes
showed a high signal. Seven nodes of hepatocellular carcinoma and 1 node of metastatic
liver tumor showed iso SI to nontumorous livertissue. In these types of tumor, the sametendency was observed with both FLASH and
SE in SI characteristics (129 nodes/139 nodes).
In 6 nodes of hepatocellular carcinoma, 3nodes of hemangioma and 1 node of adenomatous hyperplasia, the SI varied depending on theimaging method (10 nodes/139 nodes). In thesetypes of tumor, no specific tendency was observed in SI with FLASH. With SE, however,the SI was equal to nontumorous liver tissue in77

K. Yoshida et al.

Table 3. SI features of liver tumors in multisection FLASH and SE images
FLASH
image

Hepatocellular carcinoma**

Metastasis**

Bile duct carcinoma

Low

Mild
low

High
Mild highIso
Mild low
Low

7
8

8
8

High
Mild highIso
Mild low
Low

4
44

1
15

High
Mild highIso
Mild lowLow

2

1

SE image
Iso
1†
4
7
1
1

Mild
high

High

2
7

1
4

1

High
Mild highHemangioma and cyst
Iso
Mild low
1‡
1
2
Low
3‡
3
1
FLASH, fast low-angle shot; SE, spin-echo; SI, signal intensity.
† Adenomatous hyperplasia.
‡ Cyst.
** A significant correlation is observed in SI characteristics between FLASH and SE in hepatocellular
carcinoma (P < 0.05) and metastatic liver tumor (P < 0.05).

angle suitable for obtaining a T1-weighted
image of good quality, when it was suggested
that FLASH images could replace SE images(Unger et al., 1988).
In the comparison between the T1-weighted
breath-hold FLASH image not using a presaturation pulse and the T1-weighted SE image,Taupitz and colleagues (1992) reported that although FLASH was superior in quantity to in
SNR and CNR, it was slightly inferior in its
capability to visualize intrahepatic blood vessels in image evaluation, and therefore, the 2
methods were equal to each other as a whole.
However, since the quality of FLASH images is
not as stable as that of SE images clinically,
FLASH has previously been used only as anespecial method, for example in dynamic
studies (Kato et al., 1990; Inoue et al., 1994).

Discussion
There are various methods of obtaining fast andultrafast MRI sequences, and these are selectedaccording to the characteristics of each method
such as imaging time, contrast resolution andspatial resolution. Generally these fast imaging
methods are superior to the SE method in time
resolution when used in examination of the uper
abdomen. However, they tend to be inferior incontrast resolution. Besides, there is one drawback in that the shorter the imaging time, thelower the SNR, with a resultant decrease inspatial resolution.
Of these methods, FLASH is comparatively
good in contrast and SNR. In fact, we had previously been studying a TR, a TE and a flip
78

Breath-hold FLASH imaging of liver tumors

Table 4. Tumor detectability with FLASH, SE and CTAP images
1<

≤1–2<

Tumor size (cm)
≤2–3<

≤3

Total

CTAP
17
41
46
74
174
Multisection FLASH pulse sequence
0 (0)31 (75.6)
41 (89.1)
67 (90.5)139 (79.9)
SE pulse sequence
0 (0)31 (75.6)
37 (80.4)
60 (81.1)
128 (73.6)( ), %.
CTAP, computed tomography during arterial portography; FLASH, fast low-angle shot; SE, spin echo.

As for recent systems, the fast gradientsystem is coming into wide use. With the fast
gradient system, the building up of a gradient
field is quick, which makes it possible to further
shorten the imaging time in various methodsof fast imaging. Formerly, with an apparatus of
10 mT/m, it was necessary to hold the breath for
34 s in FLASH imaging of the entire liver without using a presaturation pulse. Even in imaging with the same parameters, it is possible tooperate at a narrow band width. Therefore, the
SNR, which is in inverse proportion to thesquare of the band width, increases in spatial
resolution. In our present quantitative evaluation, the liver SNR, liver-spleen and livertumor CNRs and tumor type-wise CNR weresignificantly higher with FLASH than with SE.
Each of these is the ratio of SI difference
against background noise. Since motion artifacts due to breathing and vascular pulsation are
few with breath-hold FLASH, it is quite naturalthat FLASH was superior to SE. As comparedwith FLASH having the ordinary gradientmagnetic field intensity, the breath holding time
was shortened by 8 s, which means less burden
on the patient. As a result, it has become possible to image the entire liver with one breathholding even for a patient in unfavorable
general condition, and to obtain images withless artifacts. Decrease in artifacts resulting
from vascular pulsation due to presaturation
pulse also contributed to decreasing noise.
The contrast in FLASH images was significantly higher than that of SE in both liverspleen and liver-tumor. Among the tumors examined, a significant difference in liver-tumor
contrast was observed only in hepatocellular
carcinoma. In imaging by gradient echo, themagnetic field inhomogeneities and the presence of any magnetic substance decrease the
SI (Ohtomo, 1993). Since much iron, which is amagnetic substance, is contained in the spleen,
the SI decreases with FLASH. This may be
why it was easier to produce a contrast of thespleen with the liver (Minami et al., 1989;
Sagoh et al., 1989). Also, signal decrease in theliver and tumor due to artifacts was small with
FLASH, and consequently, contrast with thetumor was higher than in imaging with SE.
Hemangioma, cysts and metastatic liver
tumor are types of tumors in which sufficient
contrast with the liver can be obtained evenwith SE, and therefore, scarcely any difference
was observed in comparison with FLASH. In
hepatocellular carcinoma, on the other hand,various degrees of intensity—low, high and iso
signals—are seen, and its degree varies depending on fat and copper content (Ebara et al.,
1991; Kitagawa et al., 1991). Therefore, as already mentioned above, decrease in SI is smallin FLASH. This presumably made it possible
to obtain images with higher contrast in FLASH
which now has a higher spatial resolution in thefast gradient magnetic field.
In qualitative evaluation, the results ofquantitative study were directly reflected. With
increased spatial resolution, the drawback of aslightly weak capability to visualize bloodvessels has been improved, leading to the above
results of our image evaluation. In comparison
to SI characteristics, FLASH visually showednearly the same tendency in many cases of liver
tumor as SE, which is superior in contrast resolution, and therefore, no great differences wereobserved. Statistically, a significant correlation
was seen only between hepatocellular carci79

K. Yoshida et al.

noma and metastatic liver tumor. As regards
liver tumors with evidently different SI, whichwere indistinguishable with SE from the liver
parenchyma because of artifacts, etc., a clear
distinction was obtained with FLASH as tumorsof low signal in the high intensity area. Thus, inthese tumors, FLASH exhibited excellent
contrast resolution.
In the evaluation of tumor detectability with
CTAP as the golden standard, the detection ratewith FLASH was 79.9%, which was higher than
the rate with SE reported in the past. The detection rate was nearly equal to the rate obtainedby spiral scan in dynamic CT of the entire liver,about which there have been many reports (Kimet al., 1995; Matsuda et al., 1995; Uchida et al.,1995). In picking up tumors smaller than 1 cm,
FLASH has a problem. However, since it has
no difference in imaging time, its performanceis considered satisfactory in screening tumors,considering that no contrast medium is used.
As for its shortcomings, FLASH is easily
affected by magnetic field inhomogeneities.
Therefore, where magnetic substances such as
metal coil are kept in, the resulting artifact
makes it difficult to make proper evaluation. In
the case of severe liver cirrhosis, where there
are many regenerated nodes, there may be many
pseudotumors, making it difficult to detect real
tumors (Murakami et al., 1989; Ohtomo et al.,1990). When a patient is unable to hold thebreath firmly, a strong artifact is likely to occur.
As a result, it becomes difficult to read theimage. In such a case, it is better to use SE,
since SE is less affected by the patient’s condition. T1-weighted FLASH images with the fast
gradient system are excellent in time, spatial
and contrast resolutions, and the tumor detection rate with FLASH is equal to or better thanthat with SE. Therefore, it is possible for
FLASH to replace SE as a method for detecting
tumors in the liver.

and tumor detectability than the SE images inpatients with hepatocelllular carcinomas.
Therefore, it seems that the FLASH images areuseful for diagnosis of hepatocellular carcinomas. In other tumors examined, the FLASH
images are also excellent in spatial and contrast
resolution. Using the fast gradient MRI system
makes it possible to shorten the imaging time inbreath-hold multisection FLASH. It is considered that FLASH with the fast gradient MRI
system can replace SE images for evaluation ofliver tumors.

Acknowledgments: The authors wish to express theirsincere gratitude to Prof. Yoshio Ohta, Dept. ofRadiology, Faculty of Medicine, Tottori Univ., for
his helpful suggestions and reading of the manuscript, and would like to thank very much Prof.
Keiichi Ichihara, Second Dept. of Pathology, Faculty of Medicine, Tottori Univ. and Prof. Hironaka
Kawasaki, Second Dept. of Internal Medicine, Faculty of Medicine, Tottori Univ., for many helpful
discussions.
The abstract of this paper was presented at the23th Congress of Japanese Magnetic Resonance in
Medicine held in 1995.

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