(Radiology. 2001;218:389-394.)
© RSNA, 2001
Dynamic Contrast-enhanced Three-dimensional MR Imaging of Liver Parenchyma: Source Images and Angiographic Reconstructions to Define Hepatic Arterial Anatomy1
Michael T. Lavelle, MD,
Vivian S. Lee, MD, PhD,
Neil M. Rofsky, MD,
Glenn A. Krinsky, MD and
Jeffrey C. Weinreb, MD
1 From the Department of Radiology, Division of Body MRI, New York University Medical Center, 530 First Ave, New York, NY 10016. Received April 25, 2000; revision requested June 9; revision received July 19; accepted July 25. Address correspondence to M.T.L. (e-mail: michael.lavelle@med.nyu.edu).
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ABSTRACT
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PURPOSE: To assess the accuracy of an interpolated breath-hold T1-weighted three-dimensional (3D) gradient-echo (GRE) magnetic resonance (MR) imaging sequence with near-isotropic pixel size (
2.3 mm) for evaluation of hepatic arterial anatomy variants during dynamic liver parenchymal imaging and to report patterns of hepatic arterial anatomy.
MATERIALS AND METHODS: Liver MR imaging, including an interpolated breath-hold 3D GRE sequence with fat suppression (4.2/1.8 [repetition time msec/echo time msec], 12° flip angle), was performed in 207 consecutive patients before and after gadopentetate dimeglumine administration. Of the 207 patients, 202 (98%) had technically satisfactory studies clearly defining the hepatic arterial system. The first contrast material–enhanced GRE acquisition was timed for optimal arterial enhancement with a timing examination. In a retrospective review, hepatic arteries were evaluated on the basis of arterial phase images interpreted by two independent readers using transverse source images complemented by multiplanar reconstructions. Twenty-three patients also underwent digital subtraction angiography, which was a reference standard for comparison.
RESULTS: Conventional hepatic arterial anatomy was demonstrated in 135 (67%) of 202 patients. In the 23 patients with angiographic correlation, no discrepancy was noted between MR imaging and digital subtraction angiographic findings.
CONCLUSION: Hepatic arterial anatomy can be reliably demonstrated during liver parenchymal imaging with an optimally timed contrast-enhanced isotropic 3D GRE sequence.
Index terms: Arteries, MR, 952.129412, 952.129415 • Hepatic arteries, 952.132, 952.92 • Liver, anatomy, 761.92 • Liver, angiography, 761.12413, 761.12453 • Liver, blood supply, 952.132, 952.92 • Liver, MR, 761.121412, 761.121415 • Magnetic resonance (MR), three-dimensional, 761.121419
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INTRODUCTION
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The accurate definition of vascular anatomy complements the evaluation of hepatic parenchyma. Procedures such as chemoembolization and transplantation can be optimized with accurate angiographic data (1–6). The potential to provide both dynamic imaging of liver parenchyma and hepatic angiography in a single study now exists in computed tomography (CT) and magnetic resonance (MR) imaging (7–14). The success of CT angiography in accurately demonstrating visceral vascular anatomy has been documented (10–12). MR imaging offers the possibility of improved parenchymal evaluation in patients with cirrhosis (15–17), eliminates exposure to ionizing radiation, and uses contrast materials with favorable safety profiles compared with iodinated contrast materials.
Recently reported (18) was a three-dimensional (3D) gradient-echo (GRE) imaging sequence that provides high-detail breath-hold images of the entire liver and can be used during the arterial and portal venous enhancement phases. Compared with a two-dimensional GRE imaging approach, currently the most commonly used technique for dynamic contrast material–enhanced MR imaging of the liver, the 3D method provides several advantages. For example, the near-isotropic pixel size (2.3 mm) that can be achieved lends itself to angiographic reconstruction. We hypothesized that this 3D approach, if timed correctly, could be used to provide reliable information about hepatic arterial anatomy. The purpose of this study was to determine the accuracy of the interpolated 3D MR sequence in the evaluation of hepatic arterial anatomy variants during arterial phase imaging as a possible noninvasive alternative to digital subtraction angiography (DSA) and to report the various patterns of hepatic arterial anatomy.
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MATERIALS AND METHODS
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Patients
A total of 207 consecutive patients underwent breath-hold MR examinations of the liver. Studies were deemed satisfactory if the liver was visualized in its entirety during the arterial phase of enhancement with no image degradation by motion or technical artifacts. All MR imaging and DSA studies were performed as part of each patient’s routine clinical work-up, and the sequences used in the MR examinations were part of our standard imaging protocol for the liver. Five studies were technically unsatisfactory due to the inability of the patient to perform a sufficient breath hold (n = 3), positioning error with partial exclusion of arterial anatomy prior to image acquisition (n = 1), and inadequate vascular enhancement due to poor intravenous access (n = 1). Clinical indications for the 202 studies used in the final analysis were as follows: known or suspected hepatocellular carcinoma (n = 83, 41%), metastatic disease (n = 49, 24%), liver lesions seen with other imaging modalities (n = 28, 14%), abnormal liver function test results (n = 21, 10%), evaluation of biliary abnormality (n = 14, 7%), and hemochromatosis (n = 7, 3%). The patient population consisted of 98 male patients and 104 female patients with a mean age of 54 years (range, 7–90 years). MR imaging evidence for cirrhosis was noted according to established criteria (15–17,19–21).
MR Imaging Technique
MR imaging examinations were performed with a 1.5-T system (Symphony and Vision; Siemens, Iselin, NJ) by using a torso phased-array coil. Written informed consent for intravenous administration of contrast material was obtained from all patients. An intravenous catheter was placed in an antecubital or forearm vein prior to the start of the study and attached to an MR-compatible power injector (Spectris; Medrad, Pittsburgh, Pa). The interpolated 3D images were obtained before administration of contrast material and during the arterial, portal venous, and equilibrium phases of contrast enhancement.
The details of our sequence, which is not currently commercially available, are nearly identical to those previously reported (18). In brief, a transverse fat-suppressed 3D spoiled GRE sequence (4.2/1.8 [repetition time msec/echo time msec], 12° flip angle) was modified to provide isotropic or near-isotropic pixel size within a breath hold by using sinc interpolation in the section select (transverse) direction, resulting in 80–100 partitions with a partition thickness of 2.3 mm or less. The imaging matrix was 80–125 x 256 with a field of view of 163–350 x 300–450 mm, resulting in an in-plane pixel size of 2.3 mm or less. Sequential filling of k space was performed. In contrast to the original description of volumetric interpolated breath-hold imaging (18), our sequence was modified to incorporate 256 readout points in the plane of acquisition.
For all sequences, patients were instructed to suspend respiration at end-expiration. Oxygen (2 L/min) via a nasal cannula was routinely offered to patients who might have difficulty with the breath-hold requirements. A timing examination was performed by using a test dose of 1 mL of gadopentetate dimeglumine (Magnevist; Berlex Laboratories, Wayne, NJ) followed by 20 mL of saline, both injected at a rate of 2 mL/sec. This allowed estimation of patient circulation time to ensure optimal timing of arterial phase imaging. In each case, the delay time between initiation of injection and initiation of acquisition was calculated according to a standard formula (22). This yielded imaging delays ranging from 4 to 38 seconds, with a mean of 18 seconds ± 5.6. Following the injection of 19 mL of contrast material and 20 mL of saline at a rate of 2 mL/sec, dynamic 3D MR images were acquired, the first timed for arterial enhancement with 45- and 120-second delays before subsequent portal venous and equilibrium phase acquisitions, respectively. This 19 mL corresponded to a mean dose of 0.14 mmol per kilogram of body weight (range, 0.09–0.21 mmol/kg). Image acquisition times ranged from 11 to 28 seconds, with a mean of 22.5 seconds ± 2.8.
Image Interpretation
On the basis of a retrospective review of source images and reformations of the 3D images, two independent readers (M.T.L., V.S.L.) characterized the patterns of hepatic arterial anatomy into one of 10 types according to the standard classification system of Michels (23), plus an 11th category to include other variants not described in the original series (Table 1). In each case, the readers used transverse source images complemented by multiplanar reformations and maximum intensity projection images generated by using the standard commercially available software of the system (VB31B; Siemens). All 3D postprocessing was performed by each reader independently at a console. Any discrepancies between the two readers were resolved by consensus. Readers were blinded to the results of correlative imaging studies.
DSA Technique
After written informed consent was obtained, selective DSA of the celiac trunk and superior mesenteric artery was performed in 23 patients in this series. The indications for DSA included evaluation for hepatocellular carcinoma (19 cases [83%], of which 10 [43%] were specifically for chemoembolization), metastatic disease (two cases [9%], renal cell and colon carcinoma), and pancreatic mass (two cases [9%]). All studies were performed with a femoral artery puncture by using a standard Seldinger technique in a retrograde fashion. Angiographers were blinded to the results of the MR imaging studies. DSA was used as the reference standard for assessing the accuracy of 3D MR imaging in evaluating hepatic arterial anatomy. For the 23 patients with angiographic correlation, the original DSA images were reviewed by the two readers, who were blinded to the MR imaging results.
Statistical Analysis
The sensitivity and specificity of MR imaging for the detection of hepatic arterial variants were calculated by using DSA as the reference standard.
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RESULTS
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The distribution of hepatic arterial variants in the 202 patients studied, including the 46 patients (23%) with cirrhosis, is presented in Table 2. The results from the original autopsy series by Michels (23), a more recent 3D CT arteriographic study by Winter et al (12), and a surgical series by Hiatt et al (24) are also shown for comparison purposes (Table 3). In our study, 135 patients (67%) had conventional hepatic arterial anatomy. This appears to be consistent with previous studies in which the percentage of patients with conventional anatomy (type I) ranged from 51% to 76% (24–27). The most common variants in our series were replaced right hepatic arteries (type III), 11%; replaced left hepatic arteries (type II), 7% (Fig 1); and accessory left hepatic arteries (type V), 7%. No patients in our study had accessory right hepatic arteries, and thus there were no type VI or VII variants. Also, no patients had type VIII anatomy. Nine patients (4%) had hepatic arterial variants not included in the original description by Michels, which we categorized as type XI: right hepatic artery arising from the common hepatic artery proximal to the subsequent bifurcation into the left hepatic artery and gastroduodenal artery (n = 4), proper hepatic artery arising directly from the aorta (n = 2) (Fig 2), right hepatic artery arising directly from the celiac trunk (n = 2), and right hepatic artery arising directly from the aorta (n = 1). An additional variant was noted in one patient with normal hepatic arterial anatomy whose splenic artery arose from the superior mesenteric artery (Fig 3).
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Figure 1a. Replaced left hepatic artery arising from the left gastric artery in a 63-year-old woman with cirrhosis who was referred to exclude hepatocellular carcinoma. (a) Transverse 3D contrast-enhanced source MR image (4.2/1.8, 12° flip angle) acquired during the arterial phase shows the replaced left hepatic artery (arrow) arising from the left gastric artery (arrowhead). (b) Oblique coronal volume-rendered MR angiogram constructed from the transverse source images, as shown in a, demonstrates the replaced left hepatic artery (straight arrows). Right hepatic artery (curved arrow) arises from the common hepatic artery.
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Figure 1b. Replaced left hepatic artery arising from the left gastric artery in a 63-year-old woman with cirrhosis who was referred to exclude hepatocellular carcinoma. (a) Transverse 3D contrast-enhanced source MR image (4.2/1.8, 12° flip angle) acquired during the arterial phase shows the replaced left hepatic artery (arrow) arising from the left gastric artery (arrowhead). (b) Oblique coronal volume-rendered MR angiogram constructed from the transverse source images, as shown in a, demonstrates the replaced left hepatic artery (straight arrows). Right hepatic artery (curved arrow) arises from the common hepatic artery.
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Figure 2a. Aberrant proper hepatic artery arising independently from the aorta in a 62-year-old woman with known cirrhosis due to hepatitis C, who was referred to rule out hepatocellular carcinoma. (a) Transverse 3D contrast-enhanced source MR image (4.2/1.8, 12° flip angle) acquired during the arterial phase shows the proper hepatic artery (arrows) with a separate origin from the aorta, distinct from the celiac trunk (arrowhead). (b) Coronal oblique projection of the volume-rendered MR angiogram generated from the transverse 3D source images, as shown in a, confirms the independent origin of the proper hepatic artery (arrows), next to the celiac trunk (arrowhead).
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Figure 2b. Aberrant proper hepatic artery arising independently from the aorta in a 62-year-old woman with known cirrhosis due to hepatitis C, who was referred to rule out hepatocellular carcinoma. (a) Transverse 3D contrast-enhanced source MR image (4.2/1.8, 12° flip angle) acquired during the arterial phase shows the proper hepatic artery (arrows) with a separate origin from the aorta, distinct from the celiac trunk (arrowhead). (b) Coronal oblique projection of the volume-rendered MR angiogram generated from the transverse 3D source images, as shown in a, confirms the independent origin of the proper hepatic artery (arrows), next to the celiac trunk (arrowhead).
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Figure 3a. Aberrant splenic artery arising from the superior mesenteric artery in a 53-year-old man referred because of abnormal liver function test results. (a) Frontal projection and (b) craniocaudal projection of an MR angiogram generated from transverse 3D source MR images (4.2/1.8, 12° flip angle) show the aberrant splenic artery (arrows) arising from the proximal superior mesenteric artery (arrowhead). A = anterior, L = left.
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Figure 3b. Aberrant splenic artery arising from the superior mesenteric artery in a 53-year-old man referred because of abnormal liver function test results. (a) Frontal projection and (b) craniocaudal projection of an MR angiogram generated from transverse 3D source MR images (4.2/1.8, 12° flip angle) show the aberrant splenic artery (arrows) arising from the proximal superior mesenteric artery (arrowhead). A = anterior, L = left.
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Of the patients who also underwent DSA (n = 23), no discrepancies were detected between DSA findings and 3D MR imaging findings (Table 4). Among these cases, all vascular anomalies reported at DSA were identified by blinded readers of the MR study. This included two replaced left hepatic arteries, eight replaced right hepatic arteries, three accessory left hepatic arteries, one right hepatic artery arising directly from the aorta, and one proper hepatic artery arising directly from the superior mesenteric artery. Thus, interpolated 3D MR imaging showed a sensitivity of 100% and a specificity of 100% in distinguishing between a hepatic arterial variant of any type versus a normal pattern of vascular anatomy and 100% accuracy in defining the variant anatomy. These 23 patients with DSA studies included 13 patients with MR evidence of cirrhosis.
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TABLE 4. Distribution of Hepatic Arterial Variants in Patients with and Those without Cirrhosis Who Underwent DSA
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DISCUSSION
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Dynamic contrast-enhanced imaging of the liver requires fast techniques that allow coverage of the entire liver in a single breath hold. Until recently, MR imaging has been limited to two-dimensional GRE imaging with relatively thick sections (8–10 mm) and intersection gaps. The interpolated 3D MR imaging approach has the advantage of providing volumetric imaging of the entire liver with near-isotropic pixel size of 2.3 mm or less, thus offering the possibility of improved detection and characterization of small lesions. Moreover, with the 3D sequence, the isotropic pixels allow for valuable angiographic reconstruction of the arterial phase data sets.
To ensure arterial phase imaging during 3D acquisitions, we implemented a timing examination by using a test bolus of contrast material. Although other timing approaches are available, such as a fixed imaging delay (28–30), estimated circulation time (8,9), and automated detection of bolus arrival (31), the test bolus approach allows customization of timing for each patient, without special hardware or software requirements (32). Using the test bolus, we were able to obtain arterial phase images that defined the hepatic arterial anatomy and showed no discrepancies with DSA images (Fig 4).
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Figure 4a. Replaced right hepatic artery arising from the superior mesenteric artery in a 58-year-old man with cirrhosis. (a, b) Transverse 3D contrast-enhanced source MR images (4.2/1.8, 12° flip angle) acquired during the (a) arterial and (b) portal venous phases of enhancement show a 1.5-cm enhancing mass (arrowheads) in the right hepatic lobe. The liver has a nodular contour (small arrows in b), and there are esophageal varices (large arrows in b). (c) Coronal volume-rendered MR angiogram constructed from the transverse 3D source images, as shown in a, shows the replaced right hepatic artery (arrows) feeding the mass (arrowhead). (d) DSA image after selective superior mesenteric artery injection confirms a replaced right hepatic artery (arrow) feeding the faintly opacified tumor (arrowhead).
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Figure 4b. Replaced right hepatic artery arising from the superior mesenteric artery in a 58-year-old man with cirrhosis. (a, b) Transverse 3D contrast-enhanced source MR images (4.2/1.8, 12° flip angle) acquired during the (a) arterial and (b) portal venous phases of enhancement show a 1.5-cm enhancing mass (arrowheads) in the right hepatic lobe. The liver has a nodular contour (small arrows in b), and there are esophageal varices (large arrows in b). (c) Coronal volume-rendered MR angiogram constructed from the transverse 3D source images, as shown in a, shows the replaced right hepatic artery (arrows) feeding the mass (arrowhead). (d) DSA image after selective superior mesenteric artery injection confirms a replaced right hepatic artery (arrow) feeding the faintly opacified tumor (arrowhead).
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Figure 4c. Replaced right hepatic artery arising from the superior mesenteric artery in a 58-year-old man with cirrhosis. (a, b) Transverse 3D contrast-enhanced source MR images (4.2/1.8, 12° flip angle) acquired during the (a) arterial and (b) portal venous phases of enhancement show a 1.5-cm enhancing mass (arrowheads) in the right hepatic lobe. The liver has a nodular contour (small arrows in b), and there are esophageal varices (large arrows in b). (c) Coronal volume-rendered MR angiogram constructed from the transverse 3D source images, as shown in a, shows the replaced right hepatic artery (arrows) feeding the mass (arrowhead). (d) DSA image after selective superior mesenteric artery injection confirms a replaced right hepatic artery (arrow) feeding the faintly opacified tumor (arrowhead).
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Figure 4d. Replaced right hepatic artery arising from the superior mesenteric artery in a 58-year-old man with cirrhosis. (a, b) Transverse 3D contrast-enhanced source MR images (4.2/1.8, 12° flip angle) acquired during the (a) arterial and (b) portal venous phases of enhancement show a 1.5-cm enhancing mass (arrowheads) in the right hepatic lobe. The liver has a nodular contour (small arrows in b), and there are esophageal varices (large arrows in b). (c) Coronal volume-rendered MR angiogram constructed from the transverse 3D source images, as shown in a, shows the replaced right hepatic artery (arrows) feeding the mass (arrowhead). (d) DSA image after selective superior mesenteric artery injection confirms a replaced right hepatic artery (arrow) feeding the faintly opacified tumor (arrowhead).
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In our study population, we were unable to identify any patients with Michels variants VI, VII, or VIII (Table 1). We did, however, note several variants that were not described previously by Michels (23). The possibility that some vessels could not be resolved with MR imaging must be considered. The resolution of MR imaging, based on pixel size, is still considerably less than that of DSA. Furthermore, the use of selective, direct intraarterial injections with DSA may distend vessels and make them more conspicuous.
In recent studies, Kopka et al (13) and Hawighorst et al (14) used 3D GRE T1-weighted sequences to define hepatic arterial anatomy. However, there are several key differences between these sequences and our 3D technique. First, in the previous studies, a larger flip angle was used for greater background suppression. Second, coverage was limited to a 75-mm slab, resulting in an incomplete evaluation of the liver parenchyma. Third, in those studies, echo asymmetry was used in the frequency- and phase-encoding directions, which in our experience degrades the image quality in the extravascular anatomy. The 3D sequence we used was developed in an attempt to improve on the conventional two-dimensional fat-suppressed GRE sequence for parenchymal imaging (18). Compared with 3D MR angiographic sequences, advantages include a lower flip angle for better soft-tissue contrast, extended anatomic coverage with a slab thickness of 160–200 mm, and echo symmetry in the read direction for improved image quality in the soft-tissue structures. While providing information about soft-tissue details, this sequence presents reliable angiographic renderings as demonstrated by the agreement with DSA imaging in our study. It is worth noting that our results were achieved by using a contrast material concentration of 0.14 mmol/kg, as compared with previous 3D MR angiographic studies in which concentrations of up to 0.2 mmol/kg were routinely used (13,14). We recognize that a limited subset of our patients (n = 23) had DSA comparison. However, those data showing agreement with 3D MR imaging are further strengthened by the comparisons with the results of previous studies mapping arterial variants (12,22,24).
The combination of dynamic 3D volumetric parenchymal imaging and angiographic reconstruction has many valuable clinical applications. Arterial phase imaging has been shown to increase hepatocellular carcinoma detection by up to 11% compared with portal venous phase imaging alone and aids in the characterization of other malignant and benign hepatic lesions (19,20,29,30,33–35). The combination of parenchymal imaging with vascular evaluation may be particularly helpful in candidates for transplantation, not only in identifying parenchymal disease and arterial variants, but also in detecting hepatic and portal venous variants for surgical planning. This is especially true in living, related hepatic transplantation, where accurate imaging of both the donor and recipient is necessary to ensure the best possible outcome for each. Presently, DSA plays a role that is complementary to cross-sectional imaging in assessing the patency, location, and caliber of hepatic vessels, identifying the sequelae of portal hypertension, and assessing the patency of prior surgical portacaval shunts. With the use of cross-sectional imaging modalities that accurately and reliably portray angiographic information, it becomes possible to streamline routine preoperative radiographic evaluation of these patients, with the potential to achieve cost savings.
Like MR imaging, spiral CT may also provide both dynamic contrast-enhanced parenchymal imaging and angiographic reconstruction. However, the radiation exposure inherent in CT poses certain safety concerns, especially as multiphasic thin-section techniques proliferate. CT also requires the use of iodinated contrast material, which has a higher incidence of adverse and nephrotoxic reactions (36) compared with that of the gadolinium chelates used for contrast-enhanced MR imaging. Furthermore, with CT, higher injection rates and contrast material volumes are needed for optimized angiographic evaluations compared with those of gadolinium-enhanced MR imaging.
The simpler and safer administration of MR contrast materials is associated with preserved diagnostic accuracy. Dual-phase MR imaging has been shown to be equivalent to or better than dual-phase CT for the detection of small hepatocellular carcinomas (34). This, in conjunction with the high degree of accuracy of our 3D MR technique in correctly characterizing hepatic arterial anatomy, suggests that it may represent a reliable alternative to spiral CT and conventional angiography. In the future, comparative studies of 3D MR imaging and multidetector CT imaging may be of value.
We conclude that with the use of a near-isotropic volumetric interpolated 3D MR imaging sequence that allows complete coverage of the entire liver in approximately 20 seconds, accurate angiographic reconstructions can be obtained that may be useful for preoperative and preinterventional planning. The value of MR imaging as a means to a comprehensive evaluation of parenchymal disease and vascular anatomy in a single setting deserves further investigation.
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FOOTNOTES
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Abbreviations: DSA = digital subtraction angiography,
GRE = gradient echo,
3D = three-dimensional
Author contributions: Guarantors of integrity of entire study, M.T.L., N.M.R., V.S.L.; study concepts and design, M.T.L., N.M.R., V.S.L.; definition of intellectual content, M.T.L., V.S.L.; literature research, M.T.L.; clinical studies, M.T.L., N.M.R., V.S.L., G.A.K.; data acquisition, M.T.L.; data analysis, M.T.L., V.S.L.; statistical analysis, M.T.L.; manuscript preparation and editing, M.T.L.; manuscript review and final version approval, all authors.
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ABSTRACT
INTRODUCTION
