Yonago Acta medica 1996;39:155–162

Three-Dimensional Gd-DTPA Enhanced MR Angiography (MRA):
Comparison of the Visualization of Portal Branches by MRA using
Magnetization Transfer Contrast Pulses and Fat Saturation Pulse
Yuji Suto, Masayuki Kamba, Takashi Kato, Shuji Sugihara, Kotaro Yoshida
and Yoshio Ohta
Department of Radiology, Faculty of Medicine, Tottori University, Yonago 683, JapanTo evaluate the visualization of portal branches of the liver, we compared threedimensional (3D) gadopentetate dimeglumine (Gd-DTPA) enhanced magnetic resonanceangiography (MRA) using magnetization transfer contrast pulses (MTC) with MRA
using fat saturation pulse (FAT-SAT). The subjects were 10 healthy volunteers and 15
patients with liver tumors. MRA was reconstructed from the data obtained by 3D-fast
low angle shot sequences(FLASH) with MTC after intravenous injection of Gd-DTPA
during breath-holding. MRA was performed again on another day by 3D-FLASH with
FAT-SAT. The depictabilities of the portal trunk to the 4th-order intrahepatic portal
branches of MRA using both methods were compared among healthy volunteers. The
depictabilities of the tumor and the contour of the liver were compared in patients withliver tumor. The visualization of the portal trunk was significantly better by the FATSAT-MRA. The 1st-order to 2nd-order portal branches were clearly visualized byboth MRA sequences, but the depictabilities of the third-order and fourth-orderbranches were significantly better by the MTC-MRA. The visualization of the contourof the liver was significantly better by the FAT-SAT-MRA, and that of the tumor was
significantly better by the MTC-MRA. In conclusion, complementary use of the 2techniques is recommended in liver MRA.
Key words: magnetization transfer contrast; MR angiography; portal vein

Methods such as two-dimensional (2D)-timeof-flight (TOF) (Edelman et al., 1989a, 1989b;
Finn et al., 1991), three-dimensional (3D)-TOF(Lewin et al., 1991; Lewin, 1992; Smith and
Bakke, 1993), and 3D-phase contrast angiography (PCA) (Dumoulin et al., 1990; Hausmann
et al.,1991; Vock et al., 1991) have been used
for abdominal magnetic resonance angiography(MRA), and each method has been suggested tohave its own limitations. In 2D-TOF, the visu-

alization of vessels flowing in the slice is reduced, and the image is deteriorated especially inthe abdominal region by phase discrepancy due
to multiple breath-holding maneuvers(Bosmans et al., 1992; Suto et al., 1994a). In
3D-TOF, signals are reduced due to saturationof blood flow spins in the imaging slab (Lewin,
1992; Bosmans et al., 1992; Suto et al., 1994b).
In 3D-PCA, the length of time needed for scanning and image processing was a problem (Suto

Abbreviations: 2D, two-dimensional; 3D, three-dimensional; FA, flip angle; FAT-SAT, fat saturation pulse;
FLASH, fast low angle shot sequences; FOV, field of view; Gd-DTPA, gadopentetate dimeglumine; Hf, protons ina free motion state; Hr, protons in a restricted motion state; MIP, maximum intensity projection; Mo, normalized SI
obtained without MTC; Mo', normalized SI obtained without FAT-SAT; Mp, mean SI of a phantom obtained with
MTC; Mp', mean SI of a phantom obtained with FAT-SAT; MR, magnetic resonance; MRA, MR angiography;
MRI, MR imaging; Ms, normalized SI obtained with MTC; Ms', normalized SI obtained with FAT-SAT; MTC,
magnetization transfer contrast pulse; PCA, phase contrast angiography; ROI, region of interest; SI, signal
intensity; TE, echo time; TOF, time-of-flight; TR, repetition time155

Y. Suto et al.

et al., 1996). To overcome these problems,
MRA utilizing the T1-shortening effect ofgadopentetate dimeglumine (Gd-DTPA)(Weinmann et al., 1984; Niendorf et al., 1991)
has been evaluated and reported to be useful(Creasy et al., 1990; Prince et al., 1993; Prince,
1994; Suto et al., 1994b, 1996).
We previously reported MRA by bolus intravenous injection of Gd-DTPA and by scanningwith a single breath hold (Suto et al., 1994b).
This method is free from image deterioration
due to phase discrepancy caused by multiple
breath holds such as that observed by 2D-TOF; italso allows suppression in the saturation of bloodflow spins in the imaging slab such as that observed in 3D-TOF, and can be performed withina short time because it requires only one breath
holding period (scanning time about 20 s).
However, the greatest disadvantage of Gdenhanced MRA is a decrease in the vessel-liver
contrast due to contrast enhancement also of thehepatic parenchyma by Gd (Suto et al., 1994b,
1996).
In this study, we added magnetization transfer contrast pulses (MTC) (Wolff and Balban,
1989; Balban and Ceckler, 1992) or fat saturation pulses (FAT-SAT) (Rosen et al., 1984;
Frahm et al., 1985) to contrast-enhanced 3D
MRA sequences as measures to increase thecontrast between vessels and surrounding tissues and compared the usefulness of the 2
methods. These pulses have been used in MRIof the heart (Li et al., 1993), but they have notoften been used in breath-holding imaging of
the abdominal region, and there have been nocomparative studies of MRA using 2 pulses.

Subjects and Methods

Subjects
The subjects were 10 normal male volunteers(aged 30–40 years, mean 36 years) and 15
patients who underwent MRI for liver tumors(aged 30–60 years, mean 48 years). The liver
tumors were hepatocellular carcinoma in 6,
metastatic liver cancer in 2 (primary lesion
located in the colon and pancreas in 1 each), andliver hemangioma in 2. Normal volunteers were
examined in advance by ultrasonography andblood biochemical tests, and those who did nothave fatty liver were selected. Liver tumor patients who showed no abnormalities on electrocardiography or chest radiography and exhibited mild or no fat infiltration on blood biochemical tests were selected. Prior to the start of eachstudy, informed consent was obtained fromeach subject.

MTC-MRAMR imagings were implemented on a 1.5 Tesla
whole body MR imaging system using a bodyphased array coil with 25 mTesla/m maximum
gradient amplitude and 1200 µs rise time. The
imaging pulses were 3D-fast low angle shot
image (FLASH) (Haase et al., 1986) with theaddition of 4 MTC [Gaussian waveform, pulse
duration 8 ms, interval 5 ms, off-resonance 1.5
kHz, band 250 Hz, radio-frequency (RF) pulse
intensity 12.1 × 10–6 Tesla]. The 4 serial MTC
correspond to 16 phase encode lines in the slab
direction. Centric reordering was made forphase encoding in the slab direction so that the
information impressed by RF before data collection would be reflected in the image. The
parameters of imaging were as follows:
repetition time (TR), 10 ms; echo time (TE), 4
ms; flip angle (FA), 15˚; field of view (FOV),
350 × 350 mm; imaging matrix, 128 (number ofphase encodings in the plane) × 256; slab
thickness, 80 mm; 16 partitions; signal averaging, 1; and scanning time 23 s. Using this imaging sequence, oblique coronal shots were obtained with breath holding 75 s after rapid intravenous injection of 0.1 mmol/kg of Gd, and
MRA was reconstructed from obtained image
data by a maximum-intensity projection (MIP)
algorithm (Laub, 1990). A series of projection
images were generated with viewing anglesof –45˚ to +45˚ from the coronal plane at fixed
5˚ intervals.

FAT-SAT-MRA
The imaging sequence was 3D-FLASH including a single FAT-SAT (Gaussian waveform,

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3D-Enhanced MRA: MTC versus FAT-SAT

Table 1. Comparison of the visualization of portal branches by FAT-SAT-MRA and MTC-MRA
Vessel†

MTC-MRAFAT-SAT-MRA

P value

Portal vein trunk
4.8 ± 0.2
5.0*First-order branches
5.0
5.0
NS
Second-order branches
5.0
5.0
NS
Third-order branches
4.6 ± 0.5
4.2 ± 0.3**
Fourth-order branches
3.8 ± 0.5
3.0 ± 0.6**
All values are mean gradings (± SD) for 3 observers.
FAT-SAT-MRA, magnetic resonance angiography obtained with fat saturation pulse; MTC-MRA,
magnetic resonance angiography obtained with magnetization transfer contrast pulses; NS, not significant.
† Vessel visualization was graded on a scale of 1 to 5: 1 = vessel not indentified and 5 = vessel clearly
defined.
* P < 0.01.
** P < 0.001.

pulse duration 9.7 ms, off-resonance 250 Hz,
band 100 Hz, RF pulse intensity 2.6 × 10 –6
Tesla), and one FAT-SAT was adjusted to the
16 phase encode lines in the slab direction.
Centric reordering was made similarly to MRA
with MTC.
The parameters of imaging were as follows:
TR, 10 ms; TE, 4 ms; FA, 15˚; FOV, 350 × 350
mm; imaging matrix,128 (number of phase
encodings in the plane) × 256; slab thickness,
80 mm; 16 partitions; signal averaging, 1; andscanning time 19 s. Similar imaging was performed within 1 week after MTC-MRA withimage reconstruction by an MIP algorithm.

(Ms) was divided by Sln obtained by the sequence without MTC pulses (Mo), and Ms/Mo
was calculated for each tissue.
Evaluation of the effect of FAT-SAT

Analysis of MRA

To evaluate the degree of fat suppression by
FAT-SAT, 3D-FLASH with and without FATSAT were performed serially before injectionof the contrast medium in 10 normal volunteers,
ROIs were determined in the liver, muscle,
perirenal fat layer and portal vein, and the mean
SI per pixel was calculated in each tissue. A
phantom filled with copper sulfate solution was
attached to the right flank, and imaging was
made over the area including the phantom. The
mean SI of the phantom was expressed as Mp',
and the mean SI normalized by dividing SI by
Mp' in each tissue was represented by Sln. Sln
obtained by the sequence with FAT-SAT (Ms')
was divided by Sln obtained by the sequence
without FAT-SAT (Mo'), and Ms'/Mo' wascalculated for each tissue.

Evaluation of the effect of MTC

To measure the extent of the effect of MTC
in the imaging sequence, 3D-FLASH with andwithout MTC was performed serially without
Gd injection in 10 healthy volunteers, the region of interests (ROIs) were determined in theliver, muscle, perirenal fat layer and portal vein,and the mean signal intensity (SI) per pixel was
calculated for each tissue. A phantom filledwith a copper sulfate solution was attached to
the right flank of each subject, and imaging was
made in the area including the phantom. The
mean SI of the phantom was expressed as Mp,
and the mean SI normalized by dividing SI ineach tissue by Mp was expressed as Sln. Sln
obtained by the sequence with MTC pulses

Comparison of MRAs with MTC and those with
FAT-SAT157

MRAs obtained by the MIP method werestudied in the cine mode. The visibility of theportal trunk from the 1st-order to the 4th-orderbranches of the portal system was compared
between MRA using MTC and MRA using
FAT-SAT in 10 normal volunteers. Three uninformed radiologists studied the images
individually and assessed the visibility of the

Y. Suto et al.

Table 2. Comparison of the visualization of the tumor and the contour of the liver by FATSAT-MRA and MTC-MRA
MTC-MRAFAT-SAT-MRA

P value

Tumor visualization†
3.0 ± 0.3
2.0 ± 0.4*
Coutour of the liver†
2.8 ± 0.4
4.0 ± 0.5**
All values are mean gradings (± SD) for 3 observers.
FAT-SAT-MRA, magnetic resonance angiography obtained with fat saturation pulse; MTC-MRA,
magnetic resonance angiography obtained with magnetization transfer contrast pulses.
† The visualization of the tumor and the liver contour was graded on a scale of 1 to 4 (1 = poor, 2 = fair, 3 =good, 4 = excellent).
* P < 0.01.
**P < 0.001.

hepatic vessels according to the following 5grade scale based on the classification by
Goldberg and colleagues (1993): 1, vessel not
identified; 2, vessel equivocally identified; 3,
vessel identified but poorly defined; 4, vessel
identified and moderately well-defined; 5,vessel clearly defined, allowing definite evaluation of patency.
The results of the 2 MRAs were comparedby Wilcoxon’s signed rank test, and differenceswere considered significant when the P value
was less than 0.05. Portal branches were classified according to the Takayasu Classification(Takayasu et al., 1985). Caudal lobe branches
were excluded, because they are difficult toanatomically identify.
In the 10 patients with liver tumors, thedetectabilities of the tumor and the liver contour
were compared between MRAs with MTC andthose with FAT-SAT. Evaluation was madeFig. 1. Case 1 (hepatocellular carcinoma). A: magnetic resonance angiography obtained with fat saturation
pulse (FAT-SAT-MRA). B: magnetic resonance angiography obtained with magnetization transfer contrast
pulses (MTC-MRA). The depictabilities of the intrahepatic distal portal branches and the tumor (arrows) are
better by MTC- MRA than by FAT-SAT-MRA, except that the visualization of the portal trunk is poor in its
caudal portion (arrowhead). The depictabilities of the portal trunk and the contour of the liver are better by
FAT-SAT-MRA than by MTC- MRA.

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3D-Enhanced MRA: MTC versus FAT-SAT

according to the 4-grade scale of: 1, poor (noliver contour or tumor stain is identified); 2, fair(liver contour and tumor stain are identified but
equivocal); 3, good (liver contour and tumor
stain are identified with moderate clarity); 4,
excellent (liver contour and tumor stain can beclearly identified). The findings in the 2 MRAs
were compared by Wilcoxon signed rank test,
and P values less than 0.05 were considered tobe significant.

Effects of FAT-SAT
The value of Ms/Mo before administration of
the contrast material was 0.56 ± 0.10 for theliver, 0.52 ± 0.11 for the portal vein, 0.16 ± 0.06
for fat, and 0.22 ± 0.08 for muscle. Ms/Mo of
fat was lower than those of other tissues, and the
FAT-SAT was effective.

Comparison of MRAs with MTC andthose with FAT-SAT

Results

Effects of MTC

The visualization of the portal trunk wassignificantly better in FAT-SAT-MRA (P <0.01). The 1st-order and 2nd-order branches ofthe portal vein were clearly visualized by both
MRA sequences, but 3rd-order and 4th-orderbranches were visualized significantly better by
the MTC-MRA (P < 0.001). The visualizationof the liver contour was significantly better by
the FAT-SAT-MRA (P < 0.001), and that of thetumor was significantly better by the MTCMRA (P < 0.01) (Tables 1 and 2, Figs.1 and 2).

The value of Ms/Mo before administration of
the contrast material was 0.70 ± 0.07 (mean ±SD) for the liver, 0.98 ± 0.07 for the portal vein,
0.98 ± 0.06 for fat and 0.65 ± 0.08 for muscle.
Ms/Mo of the portal vein was near 1, but thoseof the liver and muscle were low, and MTC was
effective in this study.

Fig. 2. Case 2 (pancreatic cancer). A: magnetic resonance angiography obtained with fat saturation pulse(FAT-SAT-MRA). B: magnetic resonance angiography obtained with magnetization transfer contrast pulses(MTC-MRA). The depictabilities of the intrahepatic distal portal branches are better by MTC- MRA than by
FAT-SAT-MRA. However, the visualization of the contour (arrows) of the liver is better by FAT-SAT-MRA
than by MTC- MRA. Arrowheads: Portal vein obstruction due to tumor invasion.

159

Y. Suto et al.

Discussion
FAT-SAT is a technique to selectively reduce
the signals of adipose tissue by impressing
selective excitation pulses with a resonancefrequency of fat (Rosen et al., 1984; Frahm etal., 1985 ). In this study, the Ms'/Mo' ratio of fat
was reduced below those of other tissues, andsignals of the adipose tissue around the liver
were reduced. Combined with the enhancement of the SI by the administration of the contrast medium, the contour of the liver tissue wasrepresented more clearly. The portal trunk,
which is also surrounded by adipose tissue, wasclearly visualized.
MTC is a method to utilize the interaction ofmagnetization between protons in a free motion
state (Hf) and those in a restricted motion state(Hr) (Wolff and Balban, 1989; Balban and
Ceckler, 1992) and is useful as a method forcontrast enhancement in MRA (Edelman et al.,
1992; Pike et al., 1992).
Effects of MTC vary widely depending on
the tissue. Since macromolecules are abundantly present in the liver, Hr and Hs are exchanged
well. Therefore, MTC are expected to be effective in the liver (Outwater et al., 1992; Loesberg
et al., 1993; Kahn et al., 1993; Suto et al., 1996).
However, they are hardly effective in adipose
tissues not containing Hf (Wolff and Balban,
1989; Balban and Ceckler, 1992). Consequently, MTC makes adipose tissue stand out as ahigh signal area relative to the liver tissue.
The MIP algorithm is used widely for image
processing in MRA (Laub, 1990). By thismethod, the maximum SI is determined on the
pixels of the projected surface. If there are perivascular signals such as those of fat, visualization of vessels is often reduced within MIP
images. As mentioned previously, MTC is
hardly effective in adipose tissue. While thedecrease in the SI due to MTC is minimal inperivascular tissues in the portal trunk surrounded by adipose tissue, the SI is reduced inperivascular adipose tissue by FAT-SAT,
resulting in improvements in the visualizationof the portal trunk. On the other hand, visuali-zation of the intrahepatic portal system andtumor stain were better by the MTC-MRA thanthe FAT-SAT-MRA.
There are reports that the SI in the liver ismarkedly reduced by FAT-SAT in patients whoshow moderate to severe fat infiltration(Mitchell, 1992). In the subjects of this study,
fat infiltration was absent or mild, so that theamount of intrahepatic adipose tissue aroundthe vessel or the tumor is considered to havebeen smaller than that around the portal trunk.
Therefore, the increase in the contrast between
the vessel and surrounding liver tissue wassmall even with impression of FAT-SAT. On
the other hand, MTC decreases the SI in livertissues around the vessels or the tumor, and the
SI of the vessels and tumor is increased by thecontrast medium, resulting in relative increases
in the vessel-liver and tumor-liver contrast.
In contrast, in subjects with marked fat
infiltration, the SI of the liver parenchyma ishardly reduced, because MTC has little effect inadipose tissue. In such cases, FAT-SAT-MRA
may be more effective. Therefore, MTC-MRA
is advantageous for visualization of the distal
intrahepatic portal system and the tumor, but
FAT-SAT-MRA is advantageous for visualization of the contour of the portal trunk or theliver, which are directly surrounded by adipose
tissue, in individuals with mild or no fat infiltration.
Although, concurrent use of both methods isthe best, the use of both methods means prolongation of the scanning time with the present
system. As a result, imaging with breathholding becomes impossible, and the inevitable
deterioration of the image quality prevents
simultaneous application of both techniques tothe upper abdominal region. Therefore, complementary use of the 2 techniques is recommended in liver MRA.

160

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(Received August 19, Accepted September14, 1996)

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