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1 All authors: Department of Radiology, Tsukuba University Hospital, 2-1-1 Amakubo, Tsukuba, Ibaraki, 305-8576 Japan.
Received March 6, 2000;
accepted after revision May 4, 2000.
Address correspondence to K. Mori.
Abstract
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SUBJECTS AND METHODS. Ten arterioportal shunts in eight patients, including four tumorous and six nontumorous arterioportal shunts, were evaluated on T2-weighted turbo spin-echo and T2*-weighted gradient-echo sequences before and after administration of superparamagnetic iron oxide. Qualitatively, the relative signal intensity of the arterioportal shunt compared with that of the surrounding liver parenchyma was categorized into three grades: high, slightly high, and not detected. Quantitatively, signal-to-noise ratio, contrast-to-noise ratio, lesion-to-liver contrast, and percentage enhancement were calculated and compared between tumorous and nontumorous arterioportal shunts by a nonparametric statistical test (Mann-Whitney test).
RESULTS. Qualitatively, all four tumorous arterioportal shunts appeared as areas of slightly high or high intensity without and with superparamagnetic iron oxide on T2-weighted turbo spin-echo images and changed from isointensity to high intensity after the administration of superparamagnetic iron oxide on T2*-weighted gradient-echo images. All nontumorous arterioportal shunts except one could not be recognized without or with superparamagnetic iron oxide on either sequence. Quantitatively, with superparamagnetic iron oxide the contrast-to-noise ratio and the lesion-to-liver contrast of the tumorous arterioportal shunts were significantly higher than those of the nontumorous arterioportal shunts.
CONCLUSION. Tumorous arterioportal shunts are seen as areas of reduced signal loss, whereas most nontumorous arterioportal shunts are seen as areas of normal signal loss, like the normal liver parenchyma. The difference is more marked on T2*-weighted gradient-echo images than on T2-weighted turbo spin-echo images.
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In the cirrhotic liver, a nontumorous arterioportal shunt can sometimes mimic a hepatocellular carcinoma on dynamic CT [15] or dynamic MR imaging. The nontumorous arterioportal shunt is detected as a hyperenhancing focus during the arterial dominant phase on dynamic studies and as a portal venous perfusion defect similar to hepatocellular carcinoma on CT during arterioportography. When the shape of the nontumorous arterioportal shunt is almost round, differentiating the arterioportal shunt from a hepatocellular carcinoma becomes more difficult. When a tumorous arterioportal shunt occurs adjacent to a hepatocellular carcinoma, it is sometimes difficult to detect small lesions in the arterioportal shunt because the whole area of the arterioportal shunt is enhanced during the arterial dominant phase on dynamic studies.
In these situations with arterioportal shunts, MR imaging with superparamagnetic iron oxide is expected to be useful for detecting focal liver lesions because both nontumorous and tumorous arterioportal shunts are part of the liver parenchyma and include Kupffer's cells, regardless of the extent to which the portal venous flow is diminished. However, in a 1998 study comparing superparamagnetic iron oxide—enhanced MR imaging with CT during arterioportography in noncirrhotic patients, Sharf et al. [16] found that 12 of 14 tumor-associated perfusion defects seen on CT during arterioportography appeared as areas of reduced signal loss on the superparamagnetic iron oxide—enhanced T1-weighted gradient-echo images, whereas two non—tumor-associated perfusion defects were not visible. These researchers concluded that impaired portal perfusion decreased the uptake of superparamagnetic iron oxide in histopathologically normal regions of the liver parenchyma.
The purpose of our study was to identify the superparamagnetic iron oxide—enhanced MR features of arterioportal shunts in patients with cirrhosis and to evaluate the differences between tumorous and nontumorous arterioportal shunts on superparamagnetic iron oxide—enhanced MR imaging.
In our study, the term "arterioportal shunt" was used to indicate the geographic region of hyperenhancement caused by the arterioportal shunt, which is not the vascular shunt itself but its effect on regional tissue density or intensity.
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The gold standard to distinguish arterioportal shunts from tumors was the combination of findings of dynamic CT, dynamic MR imaging, angiography, or a combination of these modalities. On the dynamic studies, the arterioportal shunts were recognized not only as areas of hyperenhancement during the arterial dominant phase, but also as areas of isodensity and isointensity to surrounding liver parenchyma during the other phases including before enhancement. On the angiographic studies and during the arterial dominant phase of dynamic studies, the diagnosis of the arterioportal shunt was made when the strong enhancement of the intrahepatic portal venous branch was seen within the areas of wedge- or fan-shaped staining or enhancement.
In our study, arterioportal shunts were classified into the following two types: tumorous and nontumorous. Tumorous arterioportal shunts were defined as arterioportal shunts adjacent to tumors, especially peripheral to tumors, whereas nontumorous arterioportal shunts were defined as arterioportal shunts without any relationship to tumors. Ten arterioportal shunts were identified: four tumorous arterioportal shunts in four patients and six nontumorous arterioportal shunts in five patients, because one patient had two nontumorous arterioportal shunts, and another patient had both tumorous and nontumorous arterioportal shunts.
To confirm the diagnosis of arterioportal shunt, we performed MR imaging using superparamagnetic iron oxide in all eight patients within 4 weeks after the last imaging examination by which the diagnosis had been made. MR imaging was performed on a 1.5-T unit (GYROSCAN ACS-NT; Philips Medical Systems, Best, The Netherlands) with the following two sequences performed both before and after IV administration of superparamagnetic iron oxide. The first was a T2-weighted turbo spin-echo sequence with a TR of 1800 msec and a TE of 90-100 msec (number of signal acquisitions, 4-6; slice thickness, 8-10 mm; interslice gap, 2 mm; field of view, 320-380 mm; matrix, 179-200 x 256). The second was a T2*-weighted breath-hold gradient-echo sequence with a TR of 120-180 msec, a TE of 4.6-4.8 msec, and a flip angle of 30° (number of signal acquisitions, 1; slice thickness, 8-10 mm; inter-slice gap, 2 mm; field of view, 320-380 mm; matrix, 179-192 x 256-512).
After undergoing the unenhanced scanning, the patients received IV superparamagnetic iron oxide at a dose of 0.56 mg Fe/kg of body weight that was diluted in 100 mL of a 5% glucose solution (Feridex; Eiken Kagaku, Tokyo, Japan) over 30 min. The contrast-enhanced study was performed 30-60 min after the end of the infusion.
Qualitative image analysis was performed by two experienced radiologists. The relative signal intensities of the arterioportal shunts to surrounding liver parenchyma were categorized using the following three grades: high, slightly high, and not detected. The conclusions were made by consensus.
Quantitative analysis was performed by region-of-interest analysis. Signal intensities of the arterioportal shunt and of the surrounding liver parenchyma were measured on both unenhanced and contrast-enhanced images. Regions of interest were placed at the same anatomic level in the lesion and in the liver excluding bigger vascular structures in each sequence. The largest possible region of interest was chosen according to the lesion size, at least 120 mm2 in area. If a lesion was not visible on either unenhanced or enhanced MR imaging, a region of interest of adequate size and shape was placed in the same anatomic location as in the dynamic CT or MR imaging. The standard deviation of background intensities was also measured in the phase-encoding direction, avoiding areas of motion artifact. The following four quantitative parameters were calculated as described by Poeckler-Schoeniger et al. [11].
The first quantitative parameter was the signal-to-noise ratio (S/N) for the lesions and livers both before and after contrast enhancement, as defined by the following formula:
S/N = SI of lesion or liver / noise,
where SI is defined as the signal intensity and noise is the standard deviation of the background intensity. The second parameter was the contrast-to-noise ratio (C/N) for the lesions both before and after contrast enhancement, as calculated by the following formula:
C/N = (SI of the lesion — SI of the liver) / noise,
where SI is the signal intensity. The third parameter was the lesion-to-liver contrast for lesions both before and after contrast enhancement, as obtained by the following formula:
lesion-to-liver contrast = (SI of the lesion — SI of the liver) / (SI of the lesion + SI of the liver),
where SI is the signal intensity; possible values for this parameter ranged from -1 to +1. The last parameter was the percentage of enhancement after superparamagnetic iron oxide injection for the lesions and the livers as determined by the following formula:
percentage of enhancement = [(S/Npost — S/Npre) / S/Npre] x 100,
where S/Npre and S/Npost are defined as signal-to-noise ratio before contrast enhancement and signal-to-noise ratio after contrast enhancement, respectively.
In addition, the maximum diameter of the arterioportal shunt was measured. All these parameters were compared between tumorous arterioportal shunts and nontumorous arterioportal shunts. Statistical significance was determined using a nonparametric statistical test (Mann-Whitney test). Differences were considered to be significant if the p value was less than 0.05.
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The results of quantitative analyses were as follows. For signal-to-noise ratios, no significant difference was seen between tumorous and nontumorous arterioportal shunts. The contrast-to-noise values of the tumorous arterioportal shunts were significantly higher than those of nontumorous arterioportal shunts on both T2-weighted turbo spin-echo images and T2*-weighted gradient-echo images with superparamagnetic iron oxide (p < 0.05) (Table 2). The lesion-to-liver contrasts of the tumorous arterioportal shunts were significantly higher than those of nontumorous arterioportal shunts on both sequences with superparamagnetic iron oxide (p < 0.05) (Table 3). There were no significant differences of the contrast-to-noise values or the lesion-to-liver contrast on either sequence without superparamagnetic iron oxide. The differences of percentage of enhancement after administration of superparamagnetic iron oxide were also not significant on either sequence. The maximum diameter of tumorous and nontumorous arterioportal shunts ranged from 4.8 to 10.8 cm (mean, 8.6 cm) and from 3 to 9.8 cm (mean, 5.6 cm), respectively. The difference between the maximum diameters was not significant.
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Our results showed definitive differences between the features of tumorous arterioportal shunts and those of nontumorous arterioportal shunts on superparamagnetic iron oxide—enhanced MR imaging. In the qualitative analysis of the T2-weighted turbo spin-echo sequence, all tumorous arterioportal shunts were shown as areas of slightly high or high intensity without and with superparamagnetic iron oxide, whereas all nontumorous arterioportal shunts but one were undetectable before and after superparamagnetic iron oxide infusion. On the T2*-weighted gradient-echo sequence, the relative signal intensities of all tumorous arterioportal shunts to liver parenchyma changed from isointensity to high intensity after administration of superparamagnetic iron oxide, whereas no changes were seen in all nontumorous arterioportal shunts but one. Therefore, the difference in the effect of superparamagnetic iron oxide between tumorous and nontumorous arterioportal shunts was more marked on the T2*-weighted gradient-echo images than on T2-weighted turbo spin-echo images.
In the quantitative analyses, however, the contrast-to-noise ratio and the lesion-to-liver contrast of the tumorous arterioportal shunts were significantly higher than in those of the nontumorous arterioportal shunts on both sequences performed with superparamagnetic iron oxide. The practical meaning of the quantitative data was that the tumorous and the nontumorous arterioportal shunts were distinguishable from each other on superparamagnetic iron oxide—enhanced MR imaging. Because of the small study size, we could not prove whether the degree of superparamagnetic iron oxide accumulation in the nontumorous arterioportal shunts was equal to that in the surrounding liver parenchyma. However, owing to the proved difference between the two types of arterioportal shunts, it was certain that the accumulation of superparamagnetic iron oxide in the tumorous arterioportal shunts was significantly decreased and resulted in the qualitative finding of relative high intensity.
On the other hand, in our study one of six nontumorous arterioportal shunts showed the reduced signal loss, and in the study by Scharf et al. [16] two of 14 tumor-associated perfusion defects did not show the reduced signal loss on CT during arterioportography. This discrepancy means that, although perhaps rare, there are some overlaps of the findings for the two types of arterioportal shunts on superparamagnetic iron oxide—enhanced MR imaging. A further study of a larger population will be necessary to confirm our results. No association between the size of the arterioportal shunt and the impaired uptake of superparamagnetic iron oxide was proved in our study.
Portal venous obstruction is one of the known causes of the lobar or segmental signal intensity difference on unenhanced MR imaging. In 1986 and 1988, Itai et al. [17, 18] reported that a lobar or segmental wedge-shaped high-intensity area was observed in the affected region of diminished portal flow on T2-weighted images, and these researchers speculated that a possible cause was edema caused by a nutritional effect and arterioportal shunt. In agreement with the results of their studies, the results of our series indicated that the impaired uptake of superparamagnetic iron oxide closely corresponded to the injury of the liver parenchyma, which was shown on T2-weighted turbo spin-echo imaging.
The main morphologic difference between tumorous and nontumorous arterioportal shunts is whether the associated portal branch is affected by tumors. In tumorous arterioportal shunts, the proximal portal venous flow of the affected area is stopped or decreased because of the tumor invasion or compression of the proximal portal branch. Functionally the reduction or depletion of portal flow occurs in both tumorous and nontumorous arterioportal shunts, as revealed by portal perfusion defects on CT during arterioportography. In the arterial dominant phase of dynamic studies or on CT hepatic arteriography, both arterioportal shunts are shown as focal enhanced areas due to a compensated increase of hepatic arterial flow [19]. However, in nontumorous arterioportal shunts, the degree of portal-flow reduction can be changed by the pressure and by the volume of arterial and portal flow, because the vascular space of the associated portal branch is patent. Tochio et al. [20] recently reported the effect of diet on the regional portal flow in nontumorous arterioportal shunts. By performing color Doppler sonography, these researchers found that in four cirrhotic patients with nontumorous arterioportal shunts, the associated portal venous flow changed from hepatofugal to hepatopetal after a meal. Their results showed that the portal-flow volume approximately doubles when fasting is followed by eating. In our patients, color Doppler sonography was not performed before and after eating. The reversibility of the portal flow in nontumorous arterioportal shunts was therefore not proved. Itai et al. [19] have speculated that insufficient compensation of hepatic arterial flow to reduction of portal flow results in various injuries to the liver parenchyma, including edema, depletion of hepatocytes, and fibrosis.
In 1998, Akaki et al. [21] reported an interesting study using Technetium-99m—diethylene-triamine pentaacetic acid—galactosyl human serum albumin (99mTc-DTPA-GSA), which is a hepatocyte-oriented radioligand accumulated by normally functioning hepatocytes. These researchers evaluated the accumulation of 99mTc-DTPA-GSA due to arterioportal shunts and due to decreases in the portal venous flow by liver scintigraphy. The arterioportal shunts in their study were considered to be nontumorous, although the basis for the judgment was not described in their report, because conventional MR imaging showed no signal intensity difference and because enhancement during the arterial phase in the dynamic study was the only finding. In their series, none of seven patients with arterioportal shunts showed decreased accumulation, whereas six of the seven patients with a decrease in portal venous flow revealed decreased accumulation. On the basis of their results, we can speculate that the Kupffer's cells and hepatocytes are injured in tumorous arterioportal shunts in which the associated portal branches are obstructed, whereas Kupffer's cells and hepatocytes are not injured in the nontumorous arterioportal shunts.
In conclusion, superparamagnetic iron oxide—enhanced MR imaging is clinically useful for differentiating most nontumorous arterioportal shunts from hypervascular tumors, and it is also useful for distinguishing tumorous arterioportal shunts from nontumorous arterioportal shunts, especially on T2*-weighted gradient-echo images. However, it is necessary to pay attention to the overlaps between the two types of arterioportal shunts.
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