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Vascular and Interventional Radiology |
1 From the Departments of Radiology (L.K., J.R., R.V., U.F., B. Renner, E.G.) and Transplantation Surgery (T.L., B. Ringe), Georg-August-University Göttingen, Robert-Koch-Strasse 40, 37075 Göttingen, Germany, and Siemens Medical Systems, Hamburg, Germany (J.G.). From the 1997 RSNA scientific assembly. Received May 27, 1998; revision requested July 21; revision received August 11; accepted October 6. Address reprint requests to L.K.
| Abstract |
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MATERIALS AND METHODS: Dual phase 3D MR angiography of the hepatic arteries and portal vein was performed in 140 patients. In 80 patients, the value of fat saturation, digital image subtraction, an anticholinergic agent, and a high-caloric meal were evaluated. In the next 60 patients, MR angiographic and digital subtraction angiographic (DSA) image quality and diagnostic value were compared.
RESULTS: Fat-saturated images were of significantly better quality (P < .01) than nonfat-saturated images. Digital image subtraction was useful in only 23 of 40 patients. The injection of an anticholinergic agent was superfluous, whereas administration of a high-caloric meal helped in demonstration of the superior mesenteric artery and portal vein. Classification on MR angiograms of the arterial blood supply was correct in 57 of 60 patients. All arterial and portal venous lesions were seen on MR angiograms, and MR angiograms had a significantly higher subjective image-quality ranking than did DSA images in the evaluation of the portal vein (P < .05).
CONCLUSION: Fat saturation and use of a high-caloric meal improve the results of MR angiography of hepatic vessels. MR angiography was comparable to DSA for evaluation of the arterial system and was superior for demonstration of the portal vein; therefore, MR angiography could replace intraarterial DSA.
Index terms: Liver, blood supply, 761.12117, 761.12143, 761.92 Liver, MR, 761.12117, 761.121412, 761.121415, 761.12142, 761.12143 Magnetic resonance (MR), comparative studies, 761.12142, 761.124 Magnetic resonance (MR), vascular studies, 761.12142
| Introduction |
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Visualization of the arterial system is especially difficult to achieve with MR angiography (5,6). Evident limitations are in-plane saturation, phase dispersion, and long acquisition times, which prevent the performance of an examination during respiratory arrest in a patient. This results in limited image quality and difficulties in the detection of vascular anatomy and pathologic conditions. The evaluation of the portal venous system has been reported (3,711) to be sufficient with time-of-flight and phase-contrast techniques. The authors of early studies (6,12) with contrast material enhancement and single image sections also described the visualization of the portal vein. The use of three-dimensional (3D) breath-hold contrast materialenhanced MR angiography by Prince et al (13) in 1995 enabled the acquisition of a large-volume data set in a coronal plane within a single breath hold during the first vascular pass of the contrast material. The value of this technique for different vascular regions in the thorax and abdomen had already been shown (1417).
The protocols for MR angiography of the abdominal vessels are still not standardized and are subject to continuous change. The purpose of this study was to evaluate the usefulness of a fat-saturated MR sequence, the role of retrospective digital image subtraction, the prior injection of an anticholinergic agent, and the oral administration of a high-caloric liquid meal for improving image quality at contrast-enhanced 3D MR angiography of the arterial and portal venous blood supply of the liver in the dual phase of the hepatic vascular supply. The results of a dual phase contrast-enhanced MR angiographic protocol were compared with the results of intraarterial digital subtraction angiography (DSA), which is the current standard of reference.
| MATERIALS AND METHODS |
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The MR angiographic data from the first 80 consecutive patients were used to optimize the MR protocol for dual-phase hepatic MR angiography (study part 1). After evaluation of these results, the next 60 consecutive patients underwent MR angiography with an optimized MR protocol and intraarterial DSA, which was used as the standard of reference.
MR Imaging Technique
All examinations were performed with a 1.5-T MR imaging system (Magnetom Vision; Siemens Medical Systems, Erlangen, Germany) with a maximum gradient strength of 25 mT/m by using a four-channel body phased-array coil. In all cases, nonenhanced and dual phase contrast-enhanced examinations were performed with an unchanged fast imaging with steady-state precession sequence in a sequential k-space order. The sequence parameters were kept constant for all patients (5/2 [repetition time msec/echo time msec]; flip angle, 30°). The slab volume of 75 mm was acquired in a coronal oblique orientation perpendicular to the course of the hepatic vascular structures. The volume was divided into 36 partitions to obtain an effective section thickness of 2 mm. The imaging matrix was set to 160 x 256 pixels with a rectangular 6:8 field of view. The acquisition time was 36 seconds, and the acquisition could be performed during a single breath hold.
Gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) was used for all examinations, with a concentration of 0.15 mmol of gadopentetate dimeglumine per kilogram of body weight followed by a saline solution flush of 20 mL through an 18-gauge venous catheter positioned in an antecubital vein. The contrast material was injected by using an MR-compatible power injector (Spectris; Medrad, Pittsburgh, Pa), with an injection flow rate of 2 mL/sec.
For the hepatic arterial perfusion phase, the tailoring of the contrast material bolus to the contrast-sensitive low-frequency lines of k space was achieved individually by means of a transit-time evaluation. For this purpose, a test bolus of 2 mL of gadopentetate dimeglumine followed by a saline solution flush of 20 mL was used, again with a flow rate of 2 mL/sec. The transit time of the contrast material to the celiac artery was measured repetitively by using a fast low-angle shot (TurboFLASH; Siemens Medical Systems) sequence (8.5/1.4/100 [repetition time msec/echo time msec/inversion time msec]; difference between spin echo and gradient echo, 84 msec; flip angle, 10°), with an image-acquisition time of 1 second over a period of 45 seconds at the same location of the abdominal aorta in a transverse plane. The delay of the diagnostic image at the level of the hepatic arteries was calculated with the following equation: ID = CMTT - ACT/2 + CMIT/2, where ID is the imaging delay, CMTT is the measured contrast material transit time, ACT is the acquisition time with respect to the central low-frequency lines of the k space, and CMIT is the total contrast material injection time until shortly before the peak of vascular enhancement.
The portal venous phase was acquired with the same imaging parameters after a fixed delay of 8 seconds after the completion of the arterial phase. During that interval, the patient received breathing instructions so that a second breath-hold acquisition could be achieved for the portal venous phase.
Angiographic Technique
All arterial angiographic examinations were performed with a DSA technique (Integris; Philips Medical Systems, Eindhoven, the Netherlands). In all patients, anteroposterior and lateral aortography was followed by selective demonstration of the splenic, hepatic, and superior mesenteric arteries. For the evaluation of the portal venous system, indirect spleno- and mesentericoportograms were obtained in all cases. The total volume of contrast material (iopromide, Ultravist-300; Schering) was 180250 mL. All arteriograms were obtained after the injection of a 1-mL solution containing an anticholinergic agent (50 mg of scopolamine butylbromide [Buscopan; Boehringer, Ingelheim, Germany]).
Study Part 1
Study groups.The 80 patients in part 1 of the study were randomly assigned to eight study groups (Table). In 20 patients, MR angiography was performed without fat saturation and digital image subtraction (group 1). The images in the same 20 patients were retrospectively subtracted digitally (group 2). Another 20 patients were examined with fat saturation either without (group 3) or with (group 4) retrospective digital image subtraction. A different group of 20 patients underwent intravenous administration of 1 mL of the anticholinergic agent. In these patients, images either were not digitally subtracted (group 5) or were digitally subtracted (group 6). Another 20 patients underwent oral administration of a high-caloric liquid meal (Fresubin; Fresenius, Bad Homburg, Germany). In these patients, digital image subtraction either was not (group 7) or was (group 8) performed.
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Fat saturation was obtained without any time penalty by applying a single, narrow-bandwidth, frequency-selective radio-frequency pulse before the entire centrically reordered partition loop. For the retrospective digital image subtraction, the 36 partitions obtained before the contrast material injection were subtracted from the identically located 36 partitions obtained after the injection. This technique ideally results in subtraction of all unfavorable background noise from the resulting reconstructed image, given that identical pre- and postcontrast positioning was achieved.
The intravenous administration of 1 mL of an anticholinergic agent (50 mg of scopolamine butylbromide) before the examination should eliminate intestinal peristaltic motion by blocking the cholinergic receptors of the intestine. The image quality was evaluated, especially after digital image subtraction.
The oral administration of 500 mL of a high-caloric liquid meal (2,100 kJ [500 kcal]) 30 minutes before the examination was considered to increase the blood flow in the superior mesenteric artery and the portal vein. The benefit for MR angiographic demonstration of these vessels was evaluated.
Image evaluation.The comparative results obtained with the different study groups were calculated quantitatively in five abdominal vascular regions: the abdominal aorta, the common hepatic artery, the superior mesenteric artery, the renal arteries, and the portal vein. A region-of-interest measurement was performed in all vessels on the original source images or after digital image subtraction in the defined groups. For comparison of the groups, the contrast-to-noise ratio (CNR) was used. The CNRs were calculated after measuring the paravascular tissue signal intensity SIparavasc, the postcontrast vascular signal intensity SIvasc, and the SD of the image noise SDnoise as measured outside of the body by using the following equation: (SIvasc - SIparavasc)/SDnoise.
Study Part 2
Study group.The 60 patients in part 2 of the study were candidates for liver transplantation (n = 52) or were examined before liver resection (n = 8). Optimized MR angiography and intraarterial DSA were performed within 1 week of each other. For evaluation of the MR angiograms, three radiologists (L.K., J.R., R.V.) viewed the original paracoronal source data, as well as an overview maximum intensity projection image, a targeted maximum intensity projection image, and a two-dimensional multiplanar rendering of specific vessels of interest. The radiologists were not aware of the DSA results.
Evaluation of the vascular system.All image evaluations were performed independently by three radiologists (L.K., J.R., R.V.) experienced in MR angiography and intraarterial DSA. In cases of disagreement, a consensus reading was performed. The arterial system was classified in nine segments (celiac artery, splenic artery, left gastric artery, common hepatic artery, gastroduodenal artery, proper hepatic artery, left hepatic artery, right hepatic artery, and proximal part of the superior mesenteric artery).
Image quality, with regard to depiction of the arterial system, was graded with a four-point scale: score of 1, nondiagnostic; score of 2, severe diagnostic problems; score of 3, minor diagnostic problems; score of 4, no diagnostic problems. The clinical value of intraarterial DSA and MR angiographic images for depiction of the arterial blood supply to the liver was evaluated in terms of the ability to visualize possible variations of the arterial system. The classification described by Michels (18) was used to define the different anatomic types of the arterial blood supply to the liver. The ability to detect pathologic conditions on MR angiograms was recorded. Intraarterial DSA was considered to be the standard of reference for both issues.
Depiction of the splenic and superior mesenteric veins and of the portal vein with its first branches in the liver was evaluated with a four-point scale for ranking of image quality: score of 1, nondiagnostic; score of 2, severe diagnostic problems; score of 3, minor diagnostic problems; score of 4, no diagnostic problems. All findings of disease detected with the MR angiograms were correlated with the results of indirect splenoportography.
Statistical Evaluation
The comparisons among groups 18 in study part 1 were evaluated by using the Wilcoxon test for unpaired groups. The statistical comparison in study part 2 was performed with the Student t test for paired groups. In all cases, the results were considered to be significantly different when a P value of less than .05 was calculated.
| RESULTS |
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The Michels classification (18) of the MR angiographic demonstration of the hepatic arterial system was correct in 57 (95%) of 60 patients. The overall distribution of the hepatic arterial anatomy was as follows: type I in 39 patients (65%), type II in five patients (8%), type III in 10 patients (17%) (Fig 8), type V in three patients (5%), type VI in two patients (3%), and type IX in one patient (2%). The three incorrect classifications at MR angiography included two small accessory left hepatic arteries originating from the left gastric artery (Michels type V) and an accessory hepatic artery arising from the superior mesenteric artery (Michels type VI).
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In eight patients, severe portal hypertension with extensive collateral vessel pathways was present. In a total of 12 patients, collateral circulation was seen. The hepatic veins could be evaluated with MR angiography in 42 of 60 patients, but these vessels were not detectable with indirect spleno- or mesentericoportography. In eight patients, a thrombus in the portal vein was detected on the MR angiographic and DSA images (Fig 10). A cavernous transformation was diagnosed in four cases on the basis of the MR angiographic and DSA findings. The reason for the lesion could be evaluated better with the MR angiogram because of the visualization of the surrounding hepatic parenchyma and possible liver tumors. In four patients, the region of the confluence of the splenic and superior mesenteric arteries was difficult to evaluate with DSA, so a thrombus could not be excluded. This finding was not supported at MR angiography or other imaging modalities such as computed tomography (CT) and duplex ultrasonography (US), where a normal region of the confluence was seen.
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| DISCUSSION |
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The increasing numbers of patients being treated for cirrhotic or malignant liver diseases led to a growing demand for methods for preoperative visualization of the vascular blood supply to the liver (1,2). Other noninvasive or minimally invasive diagnostic methods such as duplex US or CT angiography were already starting to replace intraarterial DSA for some purposes (1,4,5,2022). However, the quality of duplex US is dependent on the skills of the investigator and has limitations in terms of preoperative road mapping of the hepatic arterial system (1,23). Duplex US is well suited for blood flow measurements of the arterial and portal venous system in acute bedside situations (5,23). CT angiography is a useful technique for the demonstration of the hepatic blood supply (4,20,22), but it is limited in its ability to demonstrate small vascular structures, due to partial volume averaging with the typical section thicknesses of 35 mm. CT angiography also necessitates a large volume (150 mL) of iodinated contrast material and the use of ionizing radiation. Time-of-flight or phase-contrast MR angiographic techniques were often adequate for the depiction of the portal vein but failed to yield reproducibly good-quality morphologic images of the hepatic arterial blood supply and of the entire portal venous system. The phase-contrast technique still allows functional studies, such as those of the measurement of portal venous blood flow (3,7,8,10).
Current MR sequences will be improved in terms of higher spatial and temporal resolution and faster acquisition times. There is agreement (15,16,24) that for contrast-enhanced 3D MR angiography, the tailoring of the timing and volume characteristics of the bolus of contrast material to the contrast-sensitive low-frequency lines of k space is essential. The use of an automatic MR-compatible power injector also seems to improve intravascular contrast enhancement (24,25).
We evaluated some general examination parameters that can be applied to most MR sequences in terms of possible improvement of dual phase 3D MR angiography of the hepatic vessels. Fatty tissue has a short T1 of about 260 msec and, therefore, adds unfavorably high signal intensity to the images and can obscure contrast-enhanced vascular structures. This can be eliminated by using a frequency-selective fat-saturation pulse. The performance of a fat-saturation sequence without prolonged acquisition times proved to be very important in our study and should be used in all patients. Other even more effective fat-saturation techniques require longer repetition times and, therefore, longer acquisition times.
Retrospective digital image subtraction ideally eliminates all unfavorable background noise in the calculated image. This can be assumed when identical pre- and postcontrast positioning are used and the absence of any movement of the anatomic structures between the successive image acquisitions is achieved. The motion problems can be even more severe at MR angiography than at DSA because of the longer interval between the acquisition of pre- and postcontrast images without the opportunity for retrospective pixel shifting. Obviously, the large-diameter blood vessels or vessel segments located in the retroperitoneal space are better suited for this method. Digital subtraction can also reduce image quality by subtracting high signal intensity due to in-flow effects in the vessel on the precontrast images. Image quality can be improved in about 50% of patients by using digital image subtraction. In these patients, it has sufficient value and, therefore, should be performed in all patients. Digital image subtraction leads to a minimally longer postprocessing time but has no influence on examination time. In all patients, the original and the subtracted image data must be reviewed by the radiologist.
The use of an anticholinergic agent does not adequately reduce the motion problems and therefore does not improve digital image subtraction. In general, the use of an anticholinergic agent did not prove to be of value for MR angiography and seems to be superfluous. Small mesenteric vessels in very close relationship to intestinal structures are not important to the hepatic blood supply.
Oral administration of a high-caloric liquid meal before the examination improved image quality of the superior mesenteric artery and the portal vein, as was theoretically expected. Results of previous US and MR imaging studies (26,27) demonstrated the increase in blood flow in the superior mesenteric artery and the portal vein. The rationale for adapting these results to MR angiography of the liver was that increased blood flow implies higher concentration of contrast material in these vessels. Blood flow in the hepatic arteries could be reduced by means of the same mechanism. This did not decrease the image quality in our study, perhaps because many of our patients had cirrhotic livers and increased arterial blood supply.
MR angiographic image quality was comparable to that of DSA in terms of the Michels classification (18) for preoperative arterial landmarking. The entire arterial system of importance to the liver blood supply could be evaluated with high diagnostic confidence in all patients. The only diagnostic problems were identified in three patients in whom there were accessory arteries with a diameter of 1 mm that originated from the left gastric artery or the superior mesenteric artery. All 13 arterial stenoses observed in our study (nine celiac artery, four superior mesenteric artery) were seen at MR angiography, with no false-positive findings. Hemodynamic grading of celiac artery stenoses could not be achieved with MR angiographic results because of the limited temporal resolution (relative to that of DSA). Further technical developments that would allow faster acquisition times (<10 seconds) could overcome these problems in the future.
The image quality and diagnostic confidence associated with MR angiography were significantly better than those associated with DSA in the evaluation of the splenic, superior mesenteric, and portal veins. In particular, patients with portal hypertension benefited from the use of MR angiography, probably because of the increased contrast material sensitivity of the technique. In particular, the region of the confluence of the portal vein could be evaluated with higher diagnostic confidence on MR angiograms than on DSA images due to the inflow of unenhanced blood from the splenic vein (at splenoportography) or the superior mesenteric vein (at mesentericoportography). Three possible thromboses suggested at DSA in this region could be excluded by using MR angiographic results.
Collateral vessel pathways in patients with portal hypertension were detected in all cases. MR angiography had some limitations with regard to ventral extension of some collateral vessel pathways (eg, umbilical veins), because these vessel regions were beyond the acquired slab thickness. However, the missing ventral part of these vessels did not cause any diagnostic misinterpretations in our study. In cases where such vessels have clinical relevance, a further MR angiographic examination can be performed.
The hepatic veins can be demonstrated with MR angiography, whereas this is almost impossible with indirect spleno- or mesentericoportography. The image quality of MR angiograms seemed to be good enough to detect severe flow obstructions in the hepatic veins, although no pathologic conditions in these vessels were proved in the present study.
The MR angiographic sequences we used are still in development and will allow faster acquisition times of less than 10 seconds, which will enable the analysis of the dynamics of intravascular contrast material in multiple acquisition phases. Better spatial resolution can be achieved with use of a larger acquisition matrix of 512 pixels in the frequency-encoding direction and a decreased effective section thickness of less than 1 mm. Further technical improvements will allow better tailoring of the characteristics of the contrast material bolus to the k space by using automatic bolus-tracking systems. The importance of newer contrast materials (eg, blood-pool agents) must be evaluated in the future and may be especially useful for the venous system.
In conclusion, dual phase contrast-enhanced 3D MR angiography of the hepatic blood supply can be optimized by using fat saturation, the administration of a high-caloric liquid meal, and, in many patients, the performance of digital image subtraction. The intravenous injection of an anticholinergic agent seems to be superfluous. This technique compares favorably with intraarterial DSA, especially for the venous system, and may, in the future, replace the latter invasive method for preoperative evaluation of the hepatic vasculature.
| Acknowledgments |
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| Footnotes |
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Author contributions: Guarantor of integrity of entire study, L.K.; study concepts and design, L.K.; definition of intellectual content, L.K., J.R., R.V.; literature research, B. Renner, J.G.; clinical studies, L.K., J.R., R.V., T.L.; data acquisition, L.K., J.R., B. Renner, U.F.; data analysis, L.K., B. Renner; statistical analysis, L.K., B. Renner; manuscript preparation, L.K.; manuscript editing, L.K., B. Renner; manuscript review, U.F., J.G., B. Ringe, E.G.
J.G. is an employee of Siemens Medical Systems (Hamburg, Germany), which manufactured imaging equipment used in this study.
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