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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
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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.
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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.
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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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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.
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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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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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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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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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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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