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1
Department of Radiology, Gifu University School of Medicine, 40 Tsukasamachi,
Gifu City, Gifu 500-8705, Japan.
2
Department of Radiology, Kyoto University Faculty of Medicine, Sakyo-ku, Kyoto
606-8501, Japan.
3
Department of Radiology, Yamaguchi University School of Medicine, Ube City,
Yamaguchi 755-8505, Japan.
4
Department of Radiology, Osaka City University Hospital, Abeno-ku, Osaka
545-8586, Japan.
Received August 14, 2000;
accepted after revision March 8, 2001.
Address correspondence to M. Kanematsu.
Abstract
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SUBJECTS AND METHODS. Both gadolinium-enhanced and ferumoxide-enhanced MR imaging were separately performed in 53 patients with a total of 87 malignant hepatic tumors (57 hepatocellular carcinomas, 28 metastases, two cholangiocarcinomas). Thirty-one of the 53 patients had hepatic cirrhosis. Images were reviewed by three independent off-site observers. Observer performance was evaluated by means of sensitivity, specificity, and receiver operating characteristic curve analyses.
RESULTS. Gadolinium-enhanced MR imaging outperformed ferumoxide-enhanced MR imaging in sensitivity (81% versus 62%, p < 0.01) for malignant-tumor detection. Specificity was comparable (94%) between the two types of MR imaging. Area under receiver operating characteristic curve (Az) value was significantly higher with gadolinium-enhanced MR imaging than with ferumoxide-enhanced MR imaging in patients overall (Az = 0.896 versus 0.805, p < 0.001), in patients with cirrhosis (Az = 0.907 versus 0.807, p < 0.001), and in patients without cirrhosis (Az = 0.899 versus 0.834, p < 0.01). The superiority was enhanced in the subset of patients with cirrhosis.
CONCLUSION. Gadolinium-enhanced MR imaging outperforms ferumoxide-enhanced MR imaging in revealing malignant hepatic tumors. Gadolinium-enhanced MR imaging is recommended, particularly for patients with cirrhosis.
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The purpose of our study was to compare the clinical usefulness of gadolinium-enhanced versus ferumoxide-enhanced MR imaging in the detection of malignant hepatic tumors. Subanalyses in patient groups with or without cirrhosis were also conducted to clarify the efficacy in different liver conditions.
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Seven patients with hepatocellular carcinoma who had undergone transcatheter arterial chemoembolization or percutaneous ablation therapy before MR imaging were excluded from the study population because of possible changes in lesion characteristics. The study population comprised the remaining 53 patients, who included 40 men and 13 women, 46-83 years old (mean age, 64 years). This group included 31 patients with cirrhosis that was diagnosed by definitive surgery in 14 patients and by morphologic findings on sonography, CT or MR imaging, and liver function tests in the others.
A summary of the 53 patients evaluated in this study is shown in Table 1. Thirteen patients with hepatocellular carcinoma, eight with colorectal carcinoma metastasis, one with cholangiocarcinoma, one with cholangiocarcinoma and hepatic abscess, one with gallbladder carcinoma without hepatic metastasis, one with healthy liver and primary colon carcinoma who was suspected of having hepatic metastasis, and one with multiple focal nodular hyperplasias subsequently underwent definitive surgery with intraoperative sonography within 2 weeks of MR imaging. Fourteen patients with hepatocellular carcinoma, two with pancreatic carcinoma metastasis, and one with angiomyolipoma underwent sonographically guided needle core aspiration biopsy for histologic proof within 2 weeks of MR imaging. In these patients, other lesions with imaging findings similar to those of the histologically examined lesions that showed growth or shrinkage after chemotherapy on follow-up images in 3-12 months were considered to be the same disease. In three patients with hepatocellular carcinoma and two with liver metastasis in whom histopathologic evidence of disease was not obtained, the visible hepatic tumors were considered malignant on the basis of tumor growth during a 6- to 20-month interval (mean, 10 months) on follow-up sonography, CT, and MR imaging, and on the basis of increased levels of serum tumor markers. One cavernous hemangioma coexisting with hepatocellular carcinoma was diagnosed on the basis of pathognomonic findings on sonography, contrast-enhanced CT, MR imaging, and follow-up imaging 6 months later. Three patients with cirrhosis and two patients with primary colon carcinoma and healthy livers underwent follow-up imaging 7-24 months (mean, 12 months) later and were confirmed to have no hepatic tumor. Coexisting benign hepatic cysts were finally diagnosed with pathognomonic findings on sonography, CT or MR imaging, and follow-up imaging.
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Thus, in 44 of the 53 patients, 87 standard-of-reference malignant tumors consisting of 57 hepatocellular carcinomas (diameter, 5-90 mm; mean, 17.9 mm), 28 metastases (diameter, 6-58 mm; mean, 20.1 mm), and two cholangiocarcinomas (diameter, 10-22 mm; mean, 16.0 mm) were determined. Of the 44 patients, 21 had one malignant tumor, 15 had two tumors, two had three tumors, four had four tumors, and two had seven tumors each. Two focal nodular hyperplasias (diameter, 23-28 mm; mean, 14.0 mm), one cavernous hemangioma (diameter, 10 mm), one angiomyolipoma (diameter, 10 mm), and one abscess (diameter, 30 mm) were also confirmed.
Gadolinium-Enhanced MR Imaging
MR imaging was performed with a superconducting magnet operating at 1.5-T
(Signa Horizon; General Electric Medical Systems, Milwaukee, WI). All MR
images were obtained in the axial plane with a phased-array multicoil for the
body. The gadolinium-enhanced MR imaging protocol comprised chemical
shift-selective fat-suppressed respiratory-triggered T2-weighted fast
spin-echo imaging (effective TR range/effective TE range, 3333-8571/77-80;
matrix, 512 x 256; section thickness, 8 mm with a 2-mm intersection gap;
echo-train length, 8-18; field of view, 32 x 24-29 x 22 cm;
signals acquired, 3 or 4; acquisition time, 3.2-6.0 min) and
gadolinium-enhanced triphasic gradient-recalled echo imaging with a fast
multiplanar spoiled gradient-recalled echo acquisition under a steady-state
free precession sequence (TR/TE range, 150/1.6-1.8; matrix, 512 x 224;
section thickness, 8-10 mm with a 2- to 3-mm intersection gap; flip angle,
90-110°; field of view, 32 x 24-29 x 22 cm; signal
acquisition, 1; breath-hold acquisition time, 26 sec). Immediately after
obtaining unenhanced gradient-recalled echo images, gadolinium-enhanced
triphasic gradient-recalled echo images were obtained after an antecubital IV
bolus injection of 0.1 mmol/kg of gadopentetate dimeglumine (Magnevist;
Schering, Berlin, Germany) flushed by 20 mL of sterile saline solution. The
injection of contrast material and the flushing of sterile saline solution
were performed manually. The scan delay for triphasic gradient-recalled echo
imaging was 14 sec, 60 sec, and 3 min after initiating contrast injection,
predominantly representing the hepatic arterial, portal venous, and
equilibrium phases, respectively. The scan delay for the hepatic arterial
phase was set at 14 sec after initiating contrast injection, so the image data
obtained at approximately 27 sec were used to fill in the central k-space
lines to obtain entire image contrast of the hepatic arterial phase. Chemical
shift selective fat-suppression pulse was not used, because the acquisition
time and number of slices were traded.
Ferumoxide-Enhanced MR Imaging
Ferumoxide (Feridex; Tanabe Pharmaceutical, Tokyo, Japan) was administered
at a dose of 10 mmol of iron per kilogram of body weight. The ferumoxide
suspension was diluted in 100 mL of 5% glucose solution and was administered
IV through a filter over 30 min. The patients underwent MR imaging 2-6 hr
after the administration of ferumoxides solution.
MR imaging was performed with the same scanner and phased-array multicoil as those used for gadolinium-enhanced imaging. All MR images were obtained in the axial plane; the section thickness was 8 mm, with a 2-mm intersection gap. The ferumoxide-enhanced MR imaging protocol comprised respiratory-triggered T2-weighted fast spin-echo imaging (effective TR range/effective TE range, 2857-8571/77-80; matrix, 512 x 256; echo-train length, 8-16; field of view, 32 x 24-29 x 22 cm; signals acquired, 3 to 4; acquisition time, 4.5-6.5 min) and breath-hold T2*-weighted gradient-recalled echo imaging (TR/TE, 150/10; matrix, 256 x 160; flip angle, 20°; field of view, 32 x 24-29 x 22 cm; signal acquired, 1; acquisition time, 8 locations per 19 sec, resulting in 2 or 3 data acquisitions to cover the entire liver). Chemical shift selective fat-suppression pulse was not used for ferumoxide-enhanced imaging because we suspected that sufficient tumor-to-liver contrast would be obtained without fat suppression.
Image Review
Three off-site observers working mainly as gastrointestinal radiologists
for 8-19 years and who interpreted MR images of the liver as part of their
daily clinical and research practice were invited from two other institutions
to do the image review. The observers were informed that the patients were
referred for assessment of suspected malignant hepatic tumors but not provided
with any other information about the patients' histories.
Each independent observer separately reviewed unenhanced and gadolinium-enhanced gradient-recalled echo and unenhanced T2-weighted fast spin-echo images combined and ferumoxides-enhanced T2-weighted fast spin-echo and T2*-weighted gradient-recalled echo images combined, on a lesion-by-lesion and segment-by-segment basis. Three of 53 patients had undergone a liver resection (one segment in two patients and two segments in another), and a total of 420 liver segments, including 81 segments with 87 malignant hepatic tumors (57 hepatocellular carcinomas, 28 metastases, two cholangiocarcinomas), were reviewed. To prevent mislocation of the lesions by the observers, the hepatic segment numbering system of Couinaud [11] was drawn on the images by the study coordinator. The images were reviewed in random order, and the order in which the images obtained with gadolinium or ferumoxides enhancement were reviewed was randomized. To minimize learning bias, the name, age, and identification number for each patient were masked.
Each observer independently recorded the size, site (Couinaud segment), and confidence level for the probability of malignant tumor (2, probably not malignant; 3, undetermined; 4, probably malignant; 5, definitely malignant) for each visible lesion and allocated the same confidence level for the presence of malignant tumor (1, definitely absent; 2, probably absent; 3, undetermined; 4, probably present; 5, definitely present) in each segment. When two or more lesions existed in a given segment, a larger confidence level was allocated to the segment. The three observers were asked to disregard benign hepatic cysts when the observers were sure of the diagnosis. When a lesion was located in multiple segments, observers were asked to consider only the segment that was mainly involved and to assess the probability of another lesion in the other segments. When a gallbladder tumor was seen, observers were asked to disregard the lesion and to assess the probability of the presence of other separate hepatic lesions. Each observer was instructed to indicate a score of 1 when no focal signal intensity change was seen; a score of 3 when the signal intensity change was subtle, ill defined, and not circular or oval; and a score of 5 when the signal intensity change was discrete, well circumscribed, and circular or oval. Scores of 2 and 4 were assigned on the basis of the observer's subjective judgment. Each observer finally recorded the most probable name of disease for each visible lesion.
Statistical Analysis
The sensitivity of each imaging technique for detection of liver segments
with malignant tumors was determined by using the number of segments assigned
a confidence level of 3-5 of the total number of 81 segments that harbored
malignant tumors. Likewise, specificity was determined by using the number of
segments assigned a confidence level of 1 or 2 of the total number of 339
segments that harbored no malignant tumors.
We determined the sensitivity for detection of malignant tumors by lesion-size criteria, using the number of tumors assigned a confidence level of 3-5 of a total of the 87 standard-of-reference malignant tumors. We also determined rates of correct characterization, using the number of tumors that were correctly characterized with a confidence level of 4 or 5. We compared sensitivities, specificities, and correct characterization rates using an extension of the McNemar test for clustered data (CLUSTPRO; Lieber ML and Ashley C, Cleveland Clinic Foundation, Cleveland, OH) [12].
Observer performance was examined by receiver operating characteristic (ROC) analysis for clustered data in the 53 patients overall, 31 with cirrhosis and 22 without cirrhosis. The ROC analysis was conducted on Couinaud's segment-by-segment basis because one of the chief determinants of hepatic resectability is an accurate definition of the number of segments to be resected and because our objective was to compare observer performances with different imaging techniques. For each imaging technique, a nonparametric ROC curve for clustered data was constructed for each observer and by pooling rating data from the three observers (CLUSTER.FOR; Lieber ML and Obuchowski NA, Cleveland Clinic Foundation, Cleveland, OH). Differences between two ROC curves for clustered data were tested by comparing ROC areas with a z test that takes into account correlation between imaging techniques on each segment and clustering of segments in patients (CLUSTERBI.FOR).
To assess interobserver variability in assigning a confidence level to each segment, we used multiple-observer kappa statistics to measure the degree of agreement. We used the nonweighted kappa statistics with binary data defined in terms of the presence (i.e., definitely present, probably present, or undetermined) or absence (i.e., probably absent or definitely absent) of a lesion in a liver segment. A kappa value of up to 0.20 stood for slight agreement; a value of 0.21-0.40, for fair agreement; a value of 0.41-0.60, for moderate agreement; a value of 0.61-0.80, for substantial agreement; and a value of 0.81 or greater, for almost perfect agreement.
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The sensitivities for detection of malignant tumors by lesion-size criteria are listed in Table 3. The sensitivity was significantly higher (p < 0.05) with gadolinium-enhanced MR images than with ferumoxide-enhanced MR images for two observers in the group of lesions smaller than 10 mm, for all three observers in the group of lesions 10-20 mm, and for one observer in the group of lesions larger than 20 mm.
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The correct characterization rates for hepatocellular carcinoma and metastasis are summarized in Table 4. The correct characterization rates for hepatocullular carcinoma were significantly higher (p < 0.05) with gadolinium-enhanced images than with ferumoxide-enhanced images for all three observers and pooled data. The correct characterization rates for metastasis were significantly higher (p < 0.05) with gadolinium-enhanced images than with ferumoxide-enhanced images for one observer and pooled data. No observer could correctly characterize two cholangiocarcinomas with any type of imaging. All observers could correctly characterize one cavernous hemangioma with gadolinium-enhanced images, and one observer could characterize it with ferumoxide-enhanced images. Only one observer correctly characterized two focal nodular hyperplasias with gadolinium-enhanced images. No observer could correctly characterize one angiomyolipoma with any type of imaging. Two of three observers correctly characterized one hepatic abscess only with gadolinium-enhanced images.
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The values for the area under the ROC curve (Az values) for detection of malignant liver tumors are shown in Figures 3,4,5. In patients overall (Fig. 3), the Az value was significantly greater (p < 0.05) with gadolinium-enhanced images (Az = 0.886-0.903, 0.896 for pooled data) than with ferumoxide-enhanced images (Az = 0.787-0.832, 0.805 for pooled data) for all three observers and in pooled data. In patients with cirrhosis (Fig. 4), the Az value was significantly greater (p < 0.05) with gadolinium-enhanced images (Az = 0.877-0.937, 0.907 for pooled data) than with ferumoxide-enhanced images (Az = 0.805-0.811, 0.807 for pooled data) for all three observers and in pooled data (Fig. 1A,1B,1C,1D). In patients without cirrhosis (Fig. 5), the Az value was significantly greater (p < 0.05) with gadolinium-enhanced images (Az = 0.889-0.911, 0.899 for pooled data) than with ferumoxide-enhanced images (Az = 0.789-0.863, 0.834 for pooled data) for two observers and in pooled data (Fig. 2A,2B,2C,2D).
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The multiple-observer kappa values for the three observers were 0.73 and 0.65 with gadolinium-enhanced and ferumoxide-enhanced images, respectively. Substantial agreement was obtained among the observers with both types of imaging.
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Our observer performance study showed an evident superiority of gadolinium-enhanced imaging in the detection of malignant liver tumors. The reasons are threefold: first, gadolinium-enhanced imaging revealed increased tumor vascularity in the hepatic arterial phase. Increased conspicuity of hypervascular tumors with gadolinium-enhanced images was achieved because of the strong T1-shortening effect of gadolinium chelates injected as a bolus, good T1-weighted contrast resolution of the spoiled gradient-recalled echo sequence, and the use of phased-array multicoil. Second, the combination of unenhanced T2-weighted and gadolinium-enhanced images allowed the observers to better discriminate benign nonsolid lesions such as hepatic cysts or cavernous hemangiomas. Third, the presence of cirrhosis (31/53 patients) degraded the image quality more with ferumoxide-enhanced images because of decreased uneven uptake of ferumoxide particles due to impaired liver function or multiple nodular changes in the liver [15], resulting in the inferior tumor detectability (Fig. 1A,1B,1C,1D).
Our subset analyses suggested a superiority of gadolinium-enhanced imaging in patients with cirrhosis (Figs. 4 and 5). Explanations for the result are the following: first, gadolinium-enhanced imaging may well exceed ferumoxide-enhanced imaging in revealing hypervascular hepatocellular carcinomas that are prone to develop in cirrhotic livers; second, some well-differentiated hepatocellular carcinomas with residual Kupffer cells may uptake ferumoxides, resulting in decreased tumor-to-liver contrast after administration of ferumoxides; and third, tumor-to-liver contrast can be decreased with ferumoxide-enhanced images in cirrhotic livers with impaired liver function in which ferumoxides uptake is disturbed [15].
The specificity was virtually identical with both techniques. Although hypervascular pseudolesions in the hepatic arterial phase presumably caused by arterioportal shunting or peripheral portal-flow obstruction occasionally hampered the correct diagnosis, the observers could distinguish hypervascular pseudolesions by referring to T2-weighted images or equilibrium phase images. In ferumoxide-enhanced imaging, peripheral hepatic vessels, nonsolid lesions, or image artifacts could present with tumor-mimicking focal abnormalities. However, the observers could differentiate them by referring to fast spin-echo images obtained with respiratory-triggered data acquisition and high (512 x 256) image matrices.
The reported sensitivity for liver metastases smaller than 1 cm with superparamagnetic iron oxide—enhanced MR images has been as high as 56% [16]. Our results indicated no more than 32% sensitivity for detection of malignant tumors smaller than 10 mm. Such an apparent difference in sensitivity from the previous result was partly attributed to the differences in image review, study population, and method of determining sensitivity. In our study, the off-site observers were completely blinded to the results. The population included cirrhosis and hepatocellular carcinomas, and only the tumors assigned a confidence level of 3-5 were counted as findings positive for sensitivity. Also, small tumors might have been obscured on T2*-weighted gradient-recalled echo images due to blooming effect caused by the long echo time (10 msec) used in the study.
There was superiority also in characterizing hepatic lesions of gadolinium-enhanced imaging (Figs. 1A,1B,1C,1D and 2A,2B,2C,2D); this result was reasonable because the gadolinium-enhancement patterns of hepatocellular carcinomas and metastases are known to be characteristic and different from each other. Although we used T2- and T2*-weighted pulse sequences because these sequences were currently in common use in the clinical setting, inclusion of T1-weighted imaging in ferumoxide-enhanced imaging might have offered useful information concerning fat deposition, increased cellularity, or fibrous capsules or intratumoral septa that are seen particularly in hepatocellular carcinomas [17]. No observer could correctly characterize any of the cholangiocarcinomas, but gadolinium-enhanced imaging may have a chance of better characterization because of prolonged enhancement of cholangiocarcinoma in the equilibrium or delayed phase. Also, for benign conditions, some observers successfully characterized hepatic abscess or focal nodular hyperplasia only with gadolinium-enhanced images, and all could characterize cavernous hemangioma with gadolinium-enhanced images.
This study had limitations. Twenty-six patients underwent definitive surgery with intra-operative sonography, but the other patients did not. Although, ideally, histologic proof should be obtained for all lesions by definitive surgery, lesions are otherwise confirmed with intraoperative sonography. Surgical proof is obtained infrequently, especially in patients with hepatocellular carcinoma, because small hepatocellular carcinoma lesions are often treated with transcatheter arterial chemoembolization or percutaneous ablation, especially in cirrhotic patients whose functional reserve is severely impaired. Other potential limitations are reviewing-order bias and recall bias. However, because the order in which two types of images were reviewed was randomized and the tumors evaluated were relatively small (mean, 18.6 mm), we believe that these biases were minimal.
Unenhanced images were not obtained in ferumoxide-enhanced imaging because ferumoxide solution was administered by drip infusion over 30 min, and acquisition of unenhanced images was not practical in the clinical setting. However, bolus-injectable reticuloendothelial agent under research and development, iron oxide/carboxydextran sol (SH U 555A) [18], would permit obtaining unenhanced and contrast-enhanced images in a single examination. Contrast material would also enable inclusion of dynamic T1-weighted MR imaging in the workup of focal hepatic lesions, due to its high longitudinal relaxivity [19, 20], probably improving the diagnosis with superparamagnetic iron oxide—enhanced MR imaging. Furthermore, hepatobiliary agents under research and development such as gadoxetic acid, disodium [21], or gadobenate dimeglumine [22] would enable both dynamic and static contrast-enhanced MR imaging in a single session, decreasing patient burden and medical costs, while preserving diagnostic accuracy.
In conclusion, we found gadolinium-enhanced imaging to be superior to ferumoxide-enhanced imaging for the detection of malignant hepatic tumors. This superiority was enhanced in patients with cirrhosis. Gadolinium-enhanced imaging is particularly recommended for screening of patients with chronic liver damage or for preoperative detection of hepatocellular carcinomas. Gadolinium-enhanced imaging may be recommended for routine MR imaging of the liver, especially when gadolinium or ferumoxide is to be chosen as the contrast agent, although further comparison in a larger population is necessary.
Acknowledgments
We thank Michael L. Lieber of the Department of Biostatistics and
Epidemiology, Cleveland Clinic Foundation, for statistical advice.
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