AJR 2002; 178:343-348
© American Roentgen Ray Society
Intraportal Venous Flow Distribution
Evaluation with Single Breath-Hold ECG-Triggered Three-Dimensional Half-Fourier Fast Spin-Echo MR Imaging and a Selective Inversion-Recovery Tagging Pulse
Katsuyoshi Ito1,
Shinji Koike1,
Chisaki Jo2,
Ayame Shimizu1,
Hitoshi Kanazawa2,
Mitsue Miyazaki2,
Shuichi Yamauchi1 and
Naofumi Matsunaga1
1
Department of Radiology, Yamaguchi University School of Medicine, 1-1-1 Minami
Kogushi, Ube, Yamaguchi 755-8505, Japan.
2
Toshiba Medical Engineering Center, 1385 Shimoishigami, Otawara, Tochigi
324-8550, Japan.
Received May 14, 2001;
accepted after revision August 9, 2001.
Address correspondence to K. Ito.
Abstract
OBJECTIVE. The purpose of this study was to evaluate the intraportal
blood flow distribution from splenic and superior mesenteric veins with an
unenhanced MR angiographic technique using single breath-hold ECG-triggered
three-dimensional (3D) half-Fourier fast spin-echo sequence and selective
inversion-recovery tagging pulse.
SUBJECTS AND METHODS. Seventeen healthy volunteers were included in
this prospective study. After obtaining regular single breath-hold
ECG-triggered 3D half-Fourier fast spin-echo images without applying a tagging
pulse, we placed the selective inversion-recovery tagging pulse on the
superior mesenteric vein (TAG-A), the splenic vein (TAG-B), or on both (TAG-C)
to study the inflow correlation of tagged or marked blood into the portal
vein. MR images were evaluated subjectively by three reviewers.
RESULTS. On MR images obtained using the TAG-A pulse to suppress the
signal flow from the superior mesenteric vein into the portal vein, the most
common pattern of signal loss was observed on the right half of the main
portal vein (8/17 subjects). Conversely, on the MR images obtained using the
TAG-B pulse, signal loss of the left half of the main portal vein was the most
common pattern (11/17 subjects). Signal reduction from the splenic venous flow
in the left portal vein was significantly greater than that from the superior
mesenteric venous flow (p<0.05).
CONCLUSION. The unenhanced MR angiographic technique using single
breath-hold ECG-triggered 3D half-Fourier fast spin echo with selective
inversion-recovery tagging pulse has the potential to assess the intraportal
blood flow distribution from the splenic and superior mesenteric veins.
Introduction
The portal vein mainly receives blood flow from the splenic and the
superior mesenteric veins, which are laden with the products of digestion. The
distribution of the blood flow from each vein to the portal vein and the
liver, however, is still not clear in healthy subjects and in patients with
abnormal conditions. In patients with cirrhosis, the alteration of portal flow
distribution may be related to the lobar or segmental morphologic change of
cirrhotic livers.
In general, phase-contrast MR angiography has been applied in the study of
portal flow measurement. However, the long acquisition time of this technique
sometimes hampers its clinical use and research application for portal venous
flow studies. Recently, an ECG-triggered three-dimensional (3D) half-Fourier
fast spin-echo technique that uses T2 blurring and near-the-center-of-k-space
acquisition has been introduced for the examination of breath-hold unenhanced
MR angiography [1]. This
technique can show slow blood flow such as portal venous flow as high signal
intensity without the use of a gadolinium-based contrast agent. Additionally,
we have combined the unenhanced MR angiographic technique with a selective
inversion-recovery pulse [2,
3] to evaluate blood flow from
the splenic and the superior mesenteric veins. The selective
inversion-recovery tagging pulse is placed on the superior mesenteric vein,
the splenic vein, or both, to study the inflow correlation of tagged blood
into the portal vein. To our knowledge, no report has evaluated the
intraportal venous flow distribution using MR angiographic techniques. The
purpose of this study was to evaluate the intraportal blood flow distribution
from the splenic and superior mesenteric veins with an unenhanced MR
angiographic technique using a single breath-hold ECG-triggered 3D
half-Fourier fast spinecho sequence with a selective inversion-recovery
tagging pulse.
Subjects and Methods
Study Population
The study population included 17 healthy volunteers (11 men, six women; age
range, 21-43 years) who did not have a history of hepatic or pancreatobiliary
disease. The institutional review boards approved the study and informed
consent was obtained from all participants. Subjects were required to fast for
at least 5 hr before the MR examination.
MR Imaging Technique
All examinations were performed with the patient in the standard supine
position using a 1.5-T clinical imager (VISART/EX; Toshiba, Tokyo, Japan),
equipped with a body flex array coil. Before the tagging study, an ECG-prep
scan using a two-dimensional half-Fourier fast spin-echo sequence that
acquires a single slice in multiple cardiac phases was obtained to determine
the appropriate ECG triggering delay time to show the abdominal aorta in
reduced signal intensity or "black blood." ECG-prep scans were
obtained using the following parameters: TR, 2 or 3 R-R intervals;
TEeff, 60 min; echo-train spacing, 5 msec; imaging matrix, 128
x 256; slice thickness, 40 mm; field of view, 38 x 38 cm; and a
total acquisition time of about 20 sec.
After the ECG-prep scan, the appropriate delay time was selected. An
appropriately timed breath-hold ECG-triggered 3D half-Fourier fast spin-echo
acquisition was then performed. At first, regular breath-hold ECG-triggered 3D
half-Fourier fast spin-echo images without applying a tagging pulse were
obtained to depict the portal, superior mesenteric, and splenic veins as
control images in the coronal plane. We used the following imaging parameters
with a single breath-hold technique: TR, 2 or 3 R-R intervals;
TEeff, 60 msec; echo-train spacing, 5 msec; inversion time, 180
msec; matrix, 256 x 256; field of view, 35 x 35 cm; slice
thickness, 3.5 mm; slice sections, 16. Then, the selective inversion-recovery
tagging pulse was placed on the superior mesenteric vein (TAG-A), the splenic
vein (TAG-B), or both (TAG-C), to study the inflow correlation of tagged blood
into the portal vein (Fig.
1A,1B,1C)
using the same 3D fast spin-echo sequence. An inversion time of about 600 msec
was applied to tag selectively or suppress inflow blood of the superior
mesenteric and splenic veins. A 20-cm width tagging pulse was placed at
approximately 15 mm distal to the confluence of the superior mesenteric and
the splenic veins for TAG-A and TAG-B, respectively, and placed to cover
completely both the superior mesenteric and splenic veins for TAG-C (Fig.
1A,1B,1C).
Tagged blood is expected to move into the portal vein during 660 msec
(TEeff, 60; inversion time, 600 msec). Mean flow velocities of the
splenic and the superior mesenteric veins have been reported to be 19 cm/sec
and 21 cm/sec, respectively
[4]. Therefore, a 20-cm width
tagging pulse was considered sufficient for showing the inflow effect of
splenic and superior mesenteric blood into the portal vein. The second
inversion-recovery pulse with a delay time of 180 msec was applied to suppress
fat and background signals. Interpolation in the slice direction was performed
to improve the apparent resolution, and then the 3D data were processed with
maximum-intensity processing.
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Fig. 1A. —39-year-old healthy man who underwent unenhanced MR
angiography of portal venous system performed with regular breath-hold
ECG-triggered three-dimensional half-Fourier fast spin-echo sequence with no
tagging pulse. Placement of selective inversion-recovery tagging pulse on
maximum-intensity-projection image was obtained with regular three-dimensional
fast spin-echo sequence. Selective inversion-recovery tagging pulse (TAG-A) is
placed on superior mesenteric vein to suppress inflow blood signal into portal
vein.
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Fig. 1B. —39-year-old healthy man who underwent unenhanced MR
angiography of portal venous system performed with regular breath-hold
ECG-triggered three-dimensional half-Fourier fast spin-echo sequence with no
tagging pulse. Placement of selective inversion-recovery tagging pulse on
maximum-intensity-projection image was obtained with regular three-dimensional
fast spin-echo sequence. Selective inversion-recovery tagging pulse (TAG-B) is
placed on splenic vein to suppress inflow blood signal into portal vein.
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Fig. 1C. —39-year-old healthy man who underwent unenhanced MR
angiography of portal venous system performed with regular breath-hold
ECG-triggered three-dimensional half-Fourier fast spin-echo sequence with no
tagging pulse. Placement of selective inversion-recovery tagging pulse on
maximum-intensity-projection image was obtained with regular three-dimensional
fast spin-echo sequence. Selective inversion-recovery tagging pulse (TAG-C) is
placed on both superior mesenteric and splenic veins to suppress inflow blood
signal into portal vein.
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Image Interpretation
MR images were interpreted independently by three radiologists experienced
in abdominal MR imaging. Instances of disagreement among the reviewers were
resolved by majority opinion. The source images and the 3D reconstructions
were reviewed on hard copy. At first, MR images obtained by regular 3D fast
spin echo without a tagging pulse were evaluated for the visibility of the
main portal vein and the first-order intrahepatic portal vein by use of a
4-point scale (0, not visible; 1, poor; 2, good; 3, excellent). The definition
of the rating was as follows: 3, excellent, if the vessel was clearly seen as
a high-intensity structure; 2, good if the vessel was seen with moderate
visibility (between excellent and poor); 1, poor, if the vessel was visible
but the image of the vessel was blurred; 0, if the vessel was not seen.
Regarding the tag study, we reviewed all MR images for the presence and
location of the signal loss of blood flow in the main portal vein and the
first-order intrahepatic portal vein, compared with reference images obtained
by regular 3D half-Fourier fast spin-echo imaging without a tagging pulse. The
pattern of signal loss in the portal vein was categorized as central part,
left half or right half of the vessel, heterogeneous, or entire reduction. The
severity of signal loss was also recorded using the following 3-point severity
scale: 3, severe if the signal intensity of the affected vessel was markedly
less than that of the liver; 2, moderate if the signal intensity of the
affected vessel was equal to or slightly greater than that of the liver; 1,
mild if the signal intensity of the affected vessel was greater than that of
the liver but less than that of the vessel on the reference images obtained
without a tagging pulse. The findings were recorded on standardized data
sheets.
Interobserver agreement was calculated to determine the presence or absence
of signal loss in the portal vein and for localization of signal loss using
the weighted kappa statistics
[5]. The level of agreement was
defined as follows: kappa value of less than 0.40 for poor agreement, kappa
value of 0.40-0.75 for good agreement, and kappa value greater than 0.75 for
excellent agreement.
Results
In the analysis of interobserver variability for the reviewers, the kappa
values indicated good or excellent agreement for the rating of visibility of
the portal veins in the nontag studies (0.65-0.79) and for the findings in the
tag studies (0.54-0.70).
The regular 3D fast spin-echo images without the tagging pulse showed the
main portal vein, the first-order intrahepatic portal veins, the superior
mesenteric vein, and the splenic vein with high signal intensity in all
subjects (Fig.
2A,2B).
The average ratings of visibility of the main portal vein, the right portal
vein, and the left portal vein by three independent observers were 2.8
± 0.4, 2.9 ± 0.3, and 2.9 ± 0.3 (mean ± standard
deviation [SD]), respectively. Satisfactory visualization (average ratings of
two or higher) was achieved in all branches.
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Fig. 2A. —39-year-old healthy man who underwent unenhanced MR
angiography of portal venous system performed with regular breath-hold
ECG-triggered three-dimensional half-Fourier fast spin-echo sequence with no
tagging pulse (same subject as in Fig.
1A,1B,1C).
Maximum-intensity-projection image shows main portal vein, first-order
intrahepatic portal veins, superior mesenteric vein, and splenic vein with
high signal intensity.
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Fig. 2B. —39-year-old healthy man who underwent unenhanced MR
angiography of portal venous system performed with regular breath-hold
ECG-triggered three-dimensional half-Fourier fast spin-echo sequence with no
tagging pulse (same subject as in Fig.
1A,1B,1C).
Source image shows right portal vein and main portal vein.
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The presence and pattern of the signal loss in the portal branches in the
tag study are summarized in the tables. On the MR images obtained using TAG-A
to suppress the signal flow from the superior mesenteric vein into the portal
vein (Table 1), signal loss was
observed in the main portal vein in all subjects. The most common pattern of
signal loss was observed on the right half of the main portal vein (8/17
subjects) (Fig.
3A,3B),
followed by entire signal loss (6/17 subjects). Signal loss in the right and
left portal veins was observed in 14 (82%) and nine subjects (53%),
respectively. Central signal loss was the most common pattern in both the
right and left portal veins.
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Fig. 3A. —39-year-old healthy man who underwent unenhanced MR
angiography performed with breath-hold ECG-triggered three-dimensional
half-Fourier fast spin-echo sequence using selective inversion-recovery
tagging pulse (TAG-A) to suppress signal flow from superior mesenteric vein
into portal vein (same subject as Fig.
1A,1B,1C).
Maximum-intensity-projection image shows signal reduction (arrows) on
right half of main portal vein. Compare with
Figure 2A.
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Fig. 3B. —39-year-old healthy man who underwent unenhanced MR
angiography performed with breath-hold ECG-triggered three-dimensional
half-Fourier fast spin-echo sequence using selective inversion-recovery
tagging pulse (TAG-A) to suppress signal flow from superior mesenteric vein
into portal vein (same subject as Fig.
1A,1B,1C).
On source image, signal loss (arrows) is clearly observed on right
half of main portal and right portal veins. Compare with
Figure 2B.
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On MR images obtained using TAG-B to suppress the signal flow from the
splenic vein into the portal vein (Table
2), signal loss in the main portal vein was observed in all
subjects. Signal loss on the left half of the main portal vein was the most
common pattern (11/17 subjects) (Fig.
4A,4B),
followed by heterogeneous (4/17), probably caused by turbulent flow. Signal
loss in the right and in the left portal veins was observed in 14 (82%) and 12
subjects (71%), respectively. Central signal loss was most commonly seen in
both the right and the left portal veins.
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Fig. 4A. —39-year-old healthy man who underwent unenhanced MR
angiography performed with breath-hold ECG-triggered three-dimensional
half-Fourier fast spin-echo sequence using selective inversion-recovery
tagging pulse (TAG-B) to suppress signal flow from splenic vein into portal
vein (same subject as in Fig.
1A,1B,1C).
Maximum-intensity-projection image shows signal reduction (arrows) on
left half of main portal vein. Compare with
Figure 2A.
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Fig. 4B. —39-year-old healthy man who underwent unenhanced MR
angiography performed with breath-hold ECG-triggered three-dimensional
half-Fourier fast spin-echo sequence using selective inversion-recovery
tagging pulse (TAG-B) to suppress signal flow from splenic vein into portal
vein (same subject as in Fig.
1A,1B,1C).
On source image, signal loss (arrows) is clearly observed on left
half of main portal and right portal veins. Compare with
Figure 2B.
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When comparing MR images obtained with TAG-A and with TAG-B, we found that
the most common combination of the signal-reduction pattern in the main portal
vein, seen in seven subjects, was at the right half in the TAG-A study and at
the left half in the TAG-B study.
Regarding the severity of signal loss in the vessel, we found no
significant difference in the averaged severity scores in the main portal vein
between the TAG-A study and the TAG-B study (2.4 ± 0.5 vs 2.5 ±
0.6, mean ± SD). The averaged severity scores of the left portal vein
in the TAG-B study (2.4 ± 0.5) were significantly higher than those in
the TAG-A study (1.7 ± 0.7) (p = 0.048), suggesting the
predominant blood flow from the splenic vein into the left portal vein. The
averaged severity scores in the right portal vein tended to be greater in the
TAG-B study (2.4 ± 0.6) than in the TAG-A study (1.9 ± 0.8),
although these differences were not statistically significant (p =
0.068).
Table 3 shows the frequency
and pattern of signal loss on MR images obtained using the TAG-C to suppress
signal flow from both superior mesenteric and splenic veins. Signal loss in
the main portal vein was observed in all subjects. In 16 of the 17 subjects,
entire signal reduction was shown (Fig.
5A,5B).
Signal loss in the right and left portal veins was observed in 16 subjects
(94%).
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TABLE 3 Number of Cases of Signal Loss Within Portal Branches on MR Images
Tagged on Both Superior Mesenteric and Splenic Veins
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Fig. 5A. —39-year-old healthy man who underwent unenhanced MR
angiography performed with breath-hold ECG-triggered three-dimensional
half-Fourier fast spin-echo sequence using selective inversion-recovery
tagging pulse (TAG-C) to suppress signal flow from both superior mesenteric
and splenic veins into portal vein (same subject as in Fig.
1A,1B,1C).
Maximum-intensity-projection image shows entire signal reduction
(arrow) in main portal vein. Compare with
Figure 2A.
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Fig. 5B. —39-year-old healthy man who underwent unenhanced MR
angiography performed with breath-hold ECG-triggered three-dimensional
half-Fourier fast spin-echo sequence using selective inversion-recovery
tagging pulse (TAG-C) to suppress signal flow from both superior mesenteric
and splenic veins into portal vein (same subject as in Fig.
1A,1B,1C).
On source image, entire signal loss (arrows) is clearly observed in
main portal and right portal veins. Compare with
Figure 2B.
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Discussion
The distribution of splenic and superior mesenteric blood flow to the
portal vein and to the liver is not fully understood. Some previous studies
have shown the selective distribution of the portal blood in the liver due to
the portal streamlining by which splenic blood is largely sent to the left
lobe and superior mesenteric blood to the right lobe of the liver
[6,
7]. Conversely, other
investigators have reported no consistent pattern of selective distribution to
the liver of splenic and superior mesenteric blood flow
[8,9,10,11].
In the our study, MR images obtained with the tagging pulse clearly showed
the region of portal blood inflow with decreased signal intensity. In the main
portal vein, the signal loss was frequently seen in the selective half of the
portal vein (the right half on the MR images tagged on the superior mesenteric
vein and the left half on those tagged on the splenic vein), suggesting
unevenly mixed portal blood and the presence of streamlining in the main
portal vein. Atkinson et al.
[12] also found that
streamlining might occur at the origin of the portal vein but suggested that
the separate channels mixed before the blood reached the liver. Heterogeneous
or entire signal loss in the main portal vein was, however, observed in eight
subjects on the TAG-A images and in five subjects on the TAG-B images. This
fact may suggest that turbulent or whirling flow can occur in the main portal
vein.
In our study, signal loss from the splenic and the superior mesenteric
venous flow can be observed in both the right and the left portal veins.
Therefore, it seems unlikely that venous blood from the splenic and the
superior mesenteric veins is selectively distributed to completely different
lobes of the liver. However, our results suggest that there are some
tendencies in distribution patterns of splenic and mesenteric blood flow to
the right and the left portal veins. In the left portal vein, signal loss from
the splenic vein was observed in 71% of the subjects, whereas that from the
superior mesenteric vein was seen in 53% of subjects. Additionally, signal
reduction from the splenic venous flow in the left portal vein was
significantly greater than that from the superior mesenteric venous flow,
suggesting that the left portal vein may be predominantly perfused by the
splenic blood flow. In the right portal vein, signal loss from the splenic
blood flow tended to be greater than that from the superior mesenteric blood
flow, suggesting the predominant flow from the splenic vein, although there
was no significant difference. In our study, the subjects were required to
fast before MR imaging. Predominant splenic flow into the right and the left
portal veins in our subjects may be attributed to the effect of fasting
causing the reduced superior mesenteric venous flow. It has been reported that
the portal venous blood flow increased after food consumption
[13]. Another study reported
that the splenic venous blood flow volume decreased in the face of an increase
of superior mesenteric venous blood flow
[14]. It may be interesting to
evaluate the correlation between the splenic and superior mesenteric venous
flow after fasting and after food intake on the tagging MR studies.
Other studies of the portal flow distribution from splenic and superior
mesenteric blood flow have usually been performed with an interventional
technique using radiopaque dyes or a scintigraphic technique using a
radionuclide
[7,8,9,10,
12,
15,
16]. These techniques,
however, may alter the physiologic state of the portal venous circulation.
Contrast media have a specific gravity considerably higher than that of blood
and will be preferentially distributed to the dependent portion of the liver
[17]. Injection of contrast
material into the portal stream may increase flow volume and velocity, even
though a small amount of material is used. Our technique for unenhanced MR
angiography has advantages over conventional techniques. Our technique does
not require the injection of contrast material into the portal circulation.
Therefore, data from our technique are expected to reflect more accurately the
distribution of the portal blood flow in physiologic conditions. Additionally,
with this technique, the portal flow distribution in the main right and left
portal vein can be directly visualized as the region of signal reduction.
Scintigraphic techniques failed to reveal the movement of intraportal blood
flow.
Lobar or segmental changes of hepatic morphology (e.g., atrophy of the
right hepatic lobe and enlargement of the left lateral segment) are common
appearances seen in advanced cirrhosis
[18]. Segmental liver volume
is related to portal venous blood flow because of various trophic factors in
portal venous blood [19,
20]. Therefore, altered portal
blood flow in liver segments is likely to be attributed to regional changes in
hepatic morphology. Our unenhanced MR angiographic technique may have the
potential for evaluating regional changes of portal inflow distribution from
the splenic and superior mesenteric veins in cirrhotic livers. Another
clinical application of this technique may be to assess the value of selective
mesenteric or splenic inflow occlusion in patients undergoing liver tumor
ablation [21].
A limitation of this study is that biliary tracts are also shown as
high-intensity structures with our technique, often overlapping with the
portal vein. However, 3D reconstructed images facilitate discriminating the
portal venous system from biliary tracts. Another limitation is that the
hepatic parenchymal distribution of the portal blood flow cannot be determined
because of the difficulties in depicting the signal reduction from the tagged
flow in the peripheral portal branches.
In conclusion, our technique for unenhanced MR angiography using a single
breath-hold ECG-triggered 3D half-Fourier fast spin-echo sequence with a
selective inversion-recovery tagging pulse has the potential to assess the
portal blood flow distribution from the splenic and the superior mesenteric
veins. Further modification in our technique may lead to more accurate
evaluation of the intrahepatic and intraportal blood flow distribution.
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Abstract
Introduction
