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1 All authors: Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50, Ilwon-Dong, Kangnam-Ku, Seoul 135-710, Korea.
Received November 27, 2001;
accepted after revision February 20, 2002.
Address correspondence to S. H. Kim.
Abstract
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SUBJECTS AND METHODS. Twenty-one patients with 39 hepatocellular carcinomas underwent ferumoxides-enhanced and mangafodipir trisodium—enhanced MR imaging. The diagnosis was established by pathologic examination after surgical resection in all patients. Five MR sequences were obtained 30 min after ferumoxides administration, and two MR sequences were obtained before and 15 min after mangafodipir trisodium administration. Three observers independently interpreted both MR images of all sequences on a segment-by-segment basis. The diagnostic accuracy of MR imaging was assessed using receiver operating characterizing analysis. Lesion (hepatocellular carcinoma > 10 mm in diameter)-to-liver contrast-to-noise ratio was calculated on MR images.
RESULTS. Ferumoxides-enhanced MR imaging (Az = 0.971) was significantly more accurate (p < 0.05) than mangafodipir trisodium—enhanced MR imaging (Az = 0.950). The mean sensitivity of ferumoxides-enhanced MR imaging (86%) was significantly greater (p < 0.05) than that of mangafodipir trisodium—enhanced MR imaging (44%) in lesions smaller than 10 mm. The mean lesion-to-liver contrast-to-noise ratio of hepatocellular carcinoma on ferumoxides-enhanced MR imaging (13.7 ± 8.8) was significantly greater than on mangafodipir trisodium—enhanced MR imaging (5.4 ± 5.1) (p < 0.01).
CONCLUSION. Ferumoxides-enhanced MR imaging has superior diagnostic accuracy in lesions smaller than 10 mm and superior lesion conspicuity compared with mangafodipir trisodium—enhanced MR imaging for the preoperative detection of hepatocellular carcinoma.
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Hepatobiliary contrast agents are taken up by hepatocytes and are eliminated through the biliary system. The only hepatobiliary contrast agent licensed for use is mangafodipir trisodium [12,13,14]. Normal liver and focal hepatic lesions that contain hepatocytes take up these agents. However, lesions that do not contain hepatocytes do not absorb these agents [15, 16]. Recently, the usefulness of mangafodipir trisodium—enhanced MR imaging has been reported for the detection of focal hepatic lesions, including hepatocellular carcinoma [15,16,17,18,19,20,21].
To our knowledge, no study has compared ferumoxides-enhanced MR imaging and mangafodipir trisodium—enhanced MR imaging for the detection of hepatocellular carcinoma. The purpose of our study was to compare the diagnostic accuracy and lesion-to-liver contrast-to-noise ratio of these two types of MR imaging for the preoperative detection of hepatocellular carcinoma.
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Twenty patients were positive for hepatitis B surface antigen, and liver cirrhosis was confirmed by histopathologic examination of resected hepatic parenchyma in 11 patients. The interval between the last MR imaging and the hepatic surgery was 1-26 days (mean, 6.1 days). The surgically resected specimens were fixed in 10% formalin, embedded in paraffin, and sectioned into 5-mm thickness. All nodules, including the surrounding cirrhotic liver, were cut into 4-mm sections and stained with H and E. Imaging studies were correlated with the histopathologic results of the resected hepatic specimens.
Thirty-nine hepatocellular carcinomas ranging from 3 to 125 mm in diameter (mean, 30 ± 29 mm) were detected in surgically resected specimens. Twelve of these hepatocellular carcinomas were smaller than 10 mm in diameter. If the largest lesions in each segment are considered (which is relevant in a segment-by-segment analysis of hepatocellular carcinoma involvement), 29 hepatocellular carcinomas ranging from 3 to 125 mm in diameter (mean, 38 ± 30 mm) were detected in surgically resected specimens. Four of these hepatocellular carcinomas were smaller than 10 mm in diameter. In each patient, the absence of hepatocellular carcinoma in the remaining hepatic segments was ascertained on follow-up CT for at least 4 months.
Ferumoxides-Enhanced MR Imaging
All MR images were obtained using a 1.5-T imager (Horizon; General Electric
Medical Systems, Milwaukee, WI) with a phased array multicoil system. A
ferumoxides solution (Feridex IV; Advanced Magnetics, Cambridge, MA) at a dose
of 15 µmol/kg diluted in 100 mL of a 5% glucose solution was infused
through a 5-µm filter for approximately 30 min. MR imaging was initiated 30
min after the end of the infusion.
The axial images of five sequences were obtained with a section thickness of 6-7 mm and an interslice gap of 2 mm. The MR imaging protocol included fat-suppressed respiratory-triggered fast spin-echo images with two TEs (TR range/first-echo TE range, second-echo TE range: 5000-8571/17-18, 102-117; echo-train length, 10-18; excitations, 2; matrix size, 256 x 256; field of view, 30-36 cm), T2*-weighted fast multiplanar gradient-recalled acquisition in a steady state images (TR/TE range, 130/8.2-8.4; flip angle, 30°; matrix size, 256 x 128), proton density—weighted fast multiplanar spoiled gradient-recalled echo images (130/8.2-8.4; flip angle, 30°; matrix size; 256 x 128), and breath-hold in-phase T1-weighted fast multiplanar spoiled gradient-recalled echo images (TR/TE, 200/4.2; flip angle, 90°; matrix size, 256 x 128-160).
Mangafodipir Trisodium—Enhanced MR Imaging
Mangafodipir trisodium (Teslascan; Nycomed Amersham, Oslo, Norway) at a
dose of 5 µmol/kg (0.5 mL/kg) was infused at a rate of 2-3 mL/min for
approximately 10 min. Breath-hold in-phase (200/4.2; flip angle, 90°) and
out-of-phase (200/2.1-2.2; flip angle, 90°) T1-weighted fast multiplanar
spoiled gradient-recalled echo images were obtained before and 15 min after
the end of the mangafodipir trisodium infusion. The axial images of four
sequences were obtained with a section thickness of 6-7 mm, an interslice gap
of 2 mm, a matrix size of 256 x 128-160, and a field of view of 30-36
cm.
Mangafodipir trisodium—enhanced MR imaging was performed 2-7 days (mean, 2.5 days) after ferumoxides-enhanced MR imaging. Residual ferumoxides may affect the enhancement of liver parenchyma and hepatocellular carcinoma on mangafodipir trisodium—enhanced MR imaging. The half-time of the T2 effect of superparamagnetic iron oxide on liver and spleen in rats has been reported to be 24-48 hr [22]. However, the T1 effect of superparamagnetic iron oxide on liver has not been reported to our knowledge. To evaluate the T1 effect of residual ferumoxides, we compared the signal-to-noise ratio of liver parenchyma on unenhanced breath-hold in-phase T1-weighted fast multiplanar spoiled gradient-recalled echo images in a control group and in a study group. The control group was composed of 10 consecutive patients with chronic liver disease who underwent gadolinium-enhanced liver MR imaging for the evaluation of hepatocellular carcinoma. On enlarged images (full screen) on 2K x 2K monitors of a PACS (picture archiving and communication system, PathSpeed Workstation; General Electric Medical Systems), one radiologist performed operator-defined region-of-interest measurements of the mean signal intensity of the liver parenchyma and the background noise. The signal-to-noise ratio of the liver parenchyma was calculated by dividing the liver signal intensities by the standard deviation of the background noise. To measure the signal intensity of the liver parenchyma, we set regions of interest in areas devoid of focal changes in signal intensity and devoid of large vessels and prominent artifacts. Background noise was measured on each image using regions of interest positioned just ventral to the right anterior abdominal wall (phase-encoding direction) using an identical size and location for all sequences. The signal-to-noise ratio was measured on unenhanced breath-hold in-phase T1-weighted fast multiplanar spoiled gradient-recalled echo images in both the control group and the study group. The mean signal-to-noise ratios of the liver parenchyma were compared using the Student's t test. The mean signal-to-noise ratio of the control group was 11.1 ± 3.3, and the mean signal-to-noise ratio of the study group was 9.9 ± 3.9. The difference was not statistically significant (p > 0.05).
We also measured the signal-to-noise ratio of liver parenchyma on ferumoxides-enhanced in-phase T1-weighted fast multiplanar spoiled gradient-recalled echo images and compared those measurements with the signal-to noise ratio of liver parenchyma on the same sequence of the unenhanced in-phase T1-weighted fast multiplanar spoiled gradient-recalled echo images in the mangafodipir trisodium set of sequences. The mean signal-to-noise ratios of liver parenchyma were compared using the Student's t test. The mean signal-to-noise ratio of the liver parenchyma on ferumoxides-enhanced in-phase T1-weighted fast multiplanar spoiled gradient-recalled echo images was 7.6 ± 2.1, and the mean signal-to-noise ratio of liver parenchyma on the unenhanced in-phase T1-weighted fast multiplanar spoiled gradient-recalled echo images in the mangafodipir trisodium set of sequences was 9.9 ± 3.9. The mean signal-to-noise ratio of liver parenchyma on ferumoxides-enhanced T1-weighted images was 77% of that on the unenhanced images (p < 0.01). These data are similar to those of a previous study [2] in that the mean signal-to-noise ratio of liver parenchyma on ferumoxides-enhanced MR images decreased to 86% of its unenhanced values. Therefore, we thought that the residual T1 effect of superparamagnetic iron oxide on mangafodipir trisodium-enhanced MR imaging was negligible.
Image Analysis
Qualitative analysis.—Five sequences of ferumoxides-enhanced
MR imaging and four sequences of mangafodipir trisodium—enhanced MR
imaging were evaluated independently by three gastrointestinal radiologists.
They knew that the patients had been referred for assessment of suspected
hepatocellular carcinomas, but the radiologists were not provided any other
information about the patients. Ferumoxides-enhanced and mangafodipir
trisodium—enhanced MR images were reviewed in separate sessions at
3-week intervals. The image review was conducted on a segment-by-segment
basis. Hepatic segmentation according to the Couinaud number system
[23,
24] was assigned by the study
coordinator.
Of the 168 segments from the 21 patients, five segments with cysts and two segments with hemangiomas and no hepatocellular carcinoma on three-phase helical CT were excluded. Two segments with hepatocellular carcinoma were also excluded because intraoperative radiofrequency ablation was performed without biopsy. Two segments in one patient were entirely occupied by a single hepatocellular carcinoma and were considered a single segment.
A total of 158 segments (29 segments with at least one hepatocellular carcinoma and 129 segments with no hepatocellular carcinoma) were finally entered into the receiver operating characteristic (ROC) analysis. Each observer recorded the location (Couinaud segment) and size of each focal lesion and reported whether the presence or absence of hepatocellular carcinoma could be ascertained for each segment. One of five confidence levels was assigned to each decision as follows: 1, definitely absent; 2, probably absent; 3, possibly present; 4, probably present; and 5, definitely present. When a lesion was located in two or more segments, the observers were asked to determine only the segment that was mainly involved and to evaluate the probability of another lesion in the other segments.
At the time of interpreting the ferumoxides-enhanced MR images, the observers were instructed to indicate a score of 1 when no focal signal change was noted; 3 when the focal signal intensity area was subtle, poorly defined, and not circular or oval; and 5 when the focal signal intensity area was discrete, well-defined, and circular or oval. Scores of 2 and 4 were assigned according to the subjective judgment of each observer [10]. At the time of interpreting the mangafodipir trisodium—enhanced MR images, the observers were instructed to indicate a score of 1 when no focal signal change was noted; 3 when the signal change was subtle, poorly defined, and not circular or oval on contrast-enhanced images; and 5 when the signal change was discrete, well-defined, and circular or oval on contrast-enhanced images. Scores of 2 and 4 were assigned by the subjective judgment of each observer.
A binomial ROC curve was fitted to the confidence rating of each observer with a maximum-likelihood estimation. The diagnostic accuracy of MR imaging determined by each observer was evaluated by calculating the area under the ROC curve (Az). Composite ROC curves combining the performances shown on all observers' ROC curves were obtained for ferumoxides-enhanced and mangafodipir trisodium—enhanced MR imaging with the maximum-likelihood curve-fitting algorithm to rate the pooled data of the three observers [25, 26]. The sensitivities for the detection of hepatocellular carcinoma by the three individual observers and the composite data were determined using the number of segments that were assigned a score of 3 or greater (possibly to definitely present) of the 29 segments with hepatocellular carcinoma, and the specificities were determined using the number of segments that were assigned a score of 1 or 2 (definitely or probably absent) of the 129 segments without hepatocellular carcinoma.
We determined the sensitivity for the lesion size criterion for the detection of hepatocellular carcinoma by using the number of tumors assigned a score of 3 or greater (possibly to definitely present) of the 39 hepatocellular carcinomas. We compared the sensitivities and specificities of ferumoxides-enhanced and mangafodipir trisodium—enhanced MR imaging using the McNemar test.
Interobserver agreement for the evaluation of ferumoxides-enhanced and mangafodipir trisodium—enhanced MR images was assessed using the kappa value. A kappa value of greater than 0.60 indicated substantial to excellent agreement [27].
Quantitative analysis.—On enlarged images (full screen) on 2K x 2K PACS monitors, one radiologist performed operator-defined region-of-interest measurements of the mean signal intensity of each lesion, the liver parenchyma, and the background noise. Measurements were made with the five sequences of the ferumoxides-enhanced MR images (T2- and proton density—weighted fat-suppressed respiratory-triggered fast spin-echo images, T2*-weighted fast multiplanar gradient-recalled acquisition in a steady state images, proton density—weighted fast multiplanar spoiled gradient-recalled echo images) and the two sequences of the mangafodipir trisodium—enhanced MR images (contrast-enhanced in-phase and out-of-phase T1-weighted fast multiplanar spoiled gradient-recalled echo images).
To measure the liver signal, we set regions of interest in areas devoid of focal changes in signal intensity and devoid of large vessels and prominent artifacts. For liver lesions, circular or ovoid regions of interest were drawn to encompass as much of the lesion as possible. For lesions with cystic or necrotic components, care was taken to measure the signal intensity in only the solid portion of the lesion. To avoid partial volume artifacts, we studied lesions larger than 1 cm. Background noise was measured on each image using regions of interest positioned just ventral to the right anterior abdominal wall (phase-encoding direction) with identical size and location among the sequences. The areas with the most prominent ghosts were not included. Regions of interest were electronically drawn larger than 256 mm2 in the liver, 50 mm2 in the lesions, and 256 mm2 in the noise area. Regions of interest were drawn three times in each place, and the mean values were obtained.
The lesion-to-liver contrast-to-noise ratio was calculated by dividing the difference between lesion and liver signal intensities by the standard deviation of the background noise. We used absolute lesion-to-liver contrast-to-noise ratio because of the opposite enhancement effects seen in the different lesions. Although some lesions showed hyperintense enhancement relative to the enhanced liver parenchyma, others showed hypointense enhancement. When the lesion was not visualized on any sequence of MR imaging, we regarded the lesion as having the same contrast-to-noise ratio as the surrounding liver parenchyma and recorded the lesion-to-liver contrast-to-noise ratio as 0.
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The mean sensitivities and specificities for the detection of segments with hepatocellular carcinoma for each observer and each contrast agent are shown in Table 2. The mean sensitivities of ferumoxides- and mangafodipir trisodium—enhanced MR imaging were 93% and 90%, respectively; the differences are not statistically significant (p > 0.05). The mean specificities of ferumoxides- and mangafodipir trisodium—enhanced MR imaging were 99% and 98%, respectively; the differences are not statistically significant (p > 0.05).
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The sensitivities for the detection of hepatocellular carcinoma by lesion size are shown in Table 3. The mean sensitivity of ferumoxides-enhanced MR imaging (86%) was significantly (p < 0.05) greater than that of mangafodipir trisodium—enhanced MR imaging (44%) in lesions smaller than 10 mm (Fig. 2A,2B,2C,2D). Differences of sensitivities between ferumoxides- and mangafodipir trisodium—enhanced MR imaging were not significant (p > 0.05) for all observers in lesions of 10-20 mm and in lesions larger than 20 mm (Fig. 3A,3B,3C,3D). The mean sensitivities of ferumoxides- and mangafodipir trisodium—enhanced MR imaging were 92% and 81%, respectively; the differences are statistically significant (p < 0.05).
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All observers interpreted two false-positive findings on ferumoxides-enhanced MR images and seven false-positive findings on mangafodipir trisodium—enhanced MR images. On ferumoxides-enhanced MR images, both of the two false-positive lesions were smaller than 1 cm and were attributed to vessels. On mangafodipir trisodium—enhanced MR images, all seven false-positive lesions were smaller than 1 cm and were hyperintense to the surrounding liver parenchyma. Hepatocellular carcinoma was not found on pathologic examination or on follow-up CT, and these false-positive lesions were attributed to regenerative nodules (Fig. 4A,4B,4C,4D).
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The kappa analyses of the three observers showed excellent agreement (Table 4).
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Quantitative Analysis
The mean lesion-to-liver contrast-to-noise ratios of 27 hepatocellular
carcinomas larger than 1 cm in diameter on each sequence of ferumoxides- and
mangafodipir trisodium—enhanced MR imaging are shown in
Table 5. The mean
lesion-to-liver contrast-to-noise ratio of hepatocellular carcinoma on
ferumoxides-enhanced MR images (13.7 ± 8.8) was significantly greater
than that on mangafodipir trisodium—enhanced MR images (5.4 ±
5.1) (p < 0.01) (Fig.
5A,5B,5C,5D).
Two of five well-differentiated hepatocellular carcinomas larger than 1 cm
showed a greater lesion-to-liver contrast-to-noise ratio on mangafodipir
trisodium—enhanced MR images than on ferumoxides-enhanced MR images
(Fig.
6A,6B,6C,6D).
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Cirrhosis is a common clinical setting for hepatocellular carcinoma, and the similar imaging appearance of benign and malignant hepatocellular nodules is troublesome. Features that may suggest hepatocellular carcinoma, including heterogeneous enhancement or the presence of a peritumoral capsule, will be helpful in differentiation [18].
Our study showed a significantly greater sensitivity of ferumoxides-enhanced MR imaging for the detection of hepatocellular carcinomas smaller than 1 cm than of mangafodipir trisodium—enhanced MR imaging. Most hepatocellular carcinomas smaller than 1 cm are isointense to the liver parenchyma on unenhanced and mangafodipir trisodium—enhanced MR images and cannot be differentiate from regenerative or dysplastic nodules.
Mangafodipir trisodium—enhanced MR imaging permits reliable distinction between hepatocellular and nonhepatocellular tumors, including hemangiomas, metastases, and hepatic cysts [15, 16]. Meanwhile, the differentiation between hepatocellular and nonhepatocellular tumors is difficult on ferumoxides-enhanced MR images. A T1-weighted sequence is needed to differentiate malignancy from cysts on ferumoxides-enhanced MR images. However, in clinical practice, helical multiphasic (two- or three-phase) CT is generally used as the initial screening examination for patients with suspected hepatocellular carcinoma, and nonhepatocellular tumors, including hemangiomas, metastases, and hepatic cysts, can be excluded with helical multiphasic CT.
One study showed that well-differentiated hepatocellular carcinoma showed significantly greater enhancement than poorly differentiated hepatocellular carcinoma on mangafodipir trisodium—enhanced MR images [18]. Meanwhile, well-differentiated small hepatocellular carcinoma may show active uptake of ferumoxide particles, which consequently results in iso- or slight hypointensity on ferumoxides-enhanced MR images. In a recent study [11], hepatocellular nodule conspicuity on ferumoxides-enhanced MR images depended on differences in the number of Kupffer's cells in a nodule and the surrounding cirrhotic liver, and six of the 10 well-differentiated hepatocellular carcinomas had contrast-to-noise ratios of 0 or nearly 0. Therefore, some well-differentiated hepatocellular carcinomas may show greater lesion conspicuity on mangafodipir trisodium—enhanced than on ferumoxides-enhanced MR images. In our study, two of five well-differentiated hepatocellular carcinomas larger than 1 cm showed a greater lesion-to-liver contrast-to-noise ratio on mangafodipir trisodium—enhanced than on ferumoxides-enhanced MR images (Fig. 6A,6B,6C,6D). Further comparison in larger studies is necessary to evaluate the usefulness of mangafodipir trisodium—enhanced MR imaging for the detection of well-differentiated hepatocellular carcinoma.
A previous study reported that 24-hr delayed imaging with mangafodipir trisodium showed additional information in 49 (38%) of the 129 cases, and in five cases this additional information led to a change in patient management [14]. However, 24-hr delayed imaging is not practical in the clinical setting.
Although serious adverse events with ferumoxides-enhanced MR imaging are rare, approximately 3% of patients will experience severe back pain while the contrast agent is being administered [2]. Back pain develops in patients in whom the contrast agent is administered too rapidly and is more likely to occur in patients with liver dysfunction (e.g., cirrhosis). Reducing the injection rate or terminating the injection to allow the back pain to resolve and reinitiating the administration at a slower rate are generally sufficient measures. Ferumoxides-enhanced MR imaging may be most useful clinically in the detection of liver metastases and hepatocellular carcinomas [2,3,4,5,6,7,8,9,10,11]. Previous studies showed that ferumoxides-enhanced MR imaging is more accurate than dual-phase helical CT for detecting focal liver lesions [28,29,30], and our unpublished data show that the mean sensitivity of ferumoxides-enhanced MR imaging (94%) for the preoperative detection of hepatocellular carcinoma is significantly greater than that of triple-phase helical CT (84%). Studies have shown that ferumoxides-enhanced MR imaging has a performance comparable to that of CT during arterial portography for the detection of liver metastases [31, 32] and hepatocellular carcinomas [6], which suggests that ferumoxides-enhanced MR imaging may have a role as a replacement for CT during arterial portography for the preoperative examination.
Serious events with mangafodipir trisodium—enhanced MR imaging are rare and are not contrast-related. The most commonly reported adverse events are nausea and headache [12,13,14]. Mangafodipir trisodium—enhanced MR imaging may be most useful clinically in differentiating between hepatocellular and non-hepatocellular tumors, including hemangiomas, metastases, and hepatic cysts [15, 16], and in the detection of liver metastases in patients in whom hepatic resection is contemplated.
This study has several limitations. First, although the standard of reference was the findings from histopathologic analysis in the 47 resected segments, follow-up imaging findings were used as the standard of reference for the 121 nonresected segments, which was an inherent limitation of our study. In these cases, we might have missed small and slowly growing hepatocellular carcinomas that were invisible on any of the imaging studies. This limitation may also partly explain the high sensitivity rate in our study compared with that in studies with patients being considered for transplantation.
Second, our study showed relatively greater sensitivity and specificity than those shown in previous studies [4,5,6,7,8, 18,19,20]. The patients in our study were a selected group of hepatic resection patients who had relatively tolerable liver function and one or two nodular hepatocellular carcinomas confined to one hepatic lobe. The number of hepatocellular carcinomas per patient in our study was small, and the observers were aware that all the patients had histologically proven hepatocellular carcinoma. Therefore, our patients were vastly different from patients with end-stage hepatic disease who are being evaluated for liver transplantation. The latter group represents yet another selected group of patients who have no or a few small hepatocellular carcinomas depicted on imaging, but who also have more advanced cirrhosis. Thus, they potentially have many more dysplastic nodules or small hepatocellular carcinomas that are not apparent on imaging studies. These differences might be responsible for the discrepancy in sensitivity values between the two groups. Studies with a less select group of patients who have a larger number of hepatocellular carcinomas and varying degrees of cirrhosis [4,5,6,7, 18,19,20] also have limitations because of difficulties in lesion-to-lesion analysis and in obtaining histopathologic confirmation of most nodules.
Finally, unenhanced MR images were not obtained because of the long time required for the biphasic mode of MR imaging (unenhanced and ferumoxides-enhanced imaging). Unenhanced MR images are known to be necessary to decrease the number of false-positive findings attributed to small vessels [31]. However, the results of our study show only a few false-positive lesions without using unenhanced MR images.
In summary, the results of this study confirmed that ferumoxides-enhanced MR imaging has superior diagnostic accuracy for lesions smaller than 10 mm and superior lesion conspicuity when compared with mangafodipir trisodium—enhanced MR imaging for the detection of hepatocellular carcinoma. Therefore, we recommend ferumoxides-enhanced MR imaging as more accurate than mangafodipir trisodium—enhanced MR imaging for the preoperative examination of patients with hepatocellular carcinoma.
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) MR images of all five sequences (area under ROC
curve [Az] = 0.971 ± 0.013) and mangafodipir
trisodium—enhanced (
) MR images of all four sequences
(Az = 0.950 ± 0.016). Difference in mean areas
under curves was significant (p < 0.05).
