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Original Report |
1 All authors: Department of Radiology, Johns Hopkins University School of Medicine, Johns Hopkins Hospital, 600 N. Wolfe St., Baltimore, MD 21287.
Received September 8, 2000;
accepted after revision January 11, 2001.
Address correspondence to D. A. Bluemke.
Abstract
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CONCLUSION. The contrast-to-noise ratio of cholangiocarcinoma compared with that of the adjacent liver significantly (p < 0.03) improves after ferumoxides administration. Ferumoxides-enhanced MR imaging is a useful technique for the visualization and localization of intrahepatic cholangiocarcinoma.
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Most published data on the usefulness of ferumoxides have been collected on patients with metastatic colorectal carcinoma; therefore, we also evaluated 10 consecutive patients (six men and four women) who were 30-75 years old (mean age, 64 years) with pathologically proven metastatic colon carcinoma to determine if the contrast-to-noise ratio changes with ferumoxides were similar for cholangiocarcinoma and for colon metastases. Ferumoxides administration was approved by our institutional review board, and all patients gave informed consent.
All patients (four patients with cholangiocarcinoma and five with colon metastases) had histopathologic specimens obtained from needle biopsy or surgery (three patients with cholangiocarcinoma and five patients with colon metastases). Four cholangiocarcinomas were central and three were peripheral. Three patients with cholangiocarcinoma (one patient with peripheral cholangiocarcinoma and two patients with Klatskin's tumor) had nonresectable tumor because of liver, vascular, or bile duct extension of the tumor, and one patient with peritoneal involvement (Klatskin's tumor) also had nonresectable disease. Five patients with colon metastases had nonresectable tumors (three with extensive bilobar liver involvement, one with peritoneal and liver involvement, and one with peritoneal and lymph node metastases). Five patients with colon metastases were suitable for surgical resection.
MR Imaging
All MR imaging examinations were performed on 1.5-T MR scanners (Signa;
General Electric Medical Systems, Milwaukee, WI). Phased array surface coils
were used in all patients for reception of the signal. Before the injection of
the contrast agent, fast spin-echo T2-weighted MR images (TR range/TE range,
3000-5000/95-105, with an echo train length of 10-16, 4 signal averages, a
matrix of 256 x 256, chemical shift selective fat suppression with
manual optimization of the suppression pulse, and 7-mm slice thickness with no
intersection spacing [interleaved acquisition]) were obtained. In addition,
T1-weighted fast multiplanar spoiled gradient-echo images (110-190/1.6-4.2;
flip angle, 70-80°), with 1 signal average, a matrix size of 128-256
x 256, and 7-mm slice thickness with zero gap, were obtained. The field
of view varied between 30 and 40 cm and was adjusted to patient size. A
three-quarter field of view was used in the phase-encoding direction.
After the unenhanced (baseline) images were obtained, patients were removed from the MR scanner. For each patient, 0.56 mg (0.10 mmol) of iron (0.05 mL Feridex IV; Berlex Laboratories, Wayne, NJ) per kilogram of body weight, diluted in 100 mL of a 5% dextrose solution, was infused IV over 30 min. The drug was administered through a 5-µ filter at a rate of 2-4 mL/min.
After ferumoxides administration, patients returned to the same MR scanner for contrast-enhanced imaging. Identical pulse sequences were used both before and after contrast administration. MR scanning was between 60 and 180 min after the beginning of the Feridex IV infusion.
Image Analysis
Qualitative analysis.—Lesion conspicuity on T2-weighted fast
spin-echo images was evaluated in consensus by two radiologists. Tumor margins
were visually assessed on a relative scale of 1-4, on the basis of the extent
of the tumor circumference that was considered to be distinct from adjacent
structures, as follows: 1 = 0-90° of tumor circumference was distinct, 2 =
91-180°, 3 = 181-270°, and 4 
271° of circumference was
distinct.
Quantitative analysis.—MR signal-intensity changes on T2-weighted images before and after ferumoxides administration were measured. Because contrast-enhanced T1-weighted images were visually inferior to unenhanced images, we did not use these sequences for the quantitative analysis. For each patient, the largest extent of tumor in the liver was identified by a single observer who carefully defined regions of interest (ROIs) in the tumor using a work-station (Advantage Windows; General Electric Medical Systems, Waukesha, WI). For lesions with high-signal-intensity areas similar to that of fluid on T2-weighted images, care was taken to measure signal intensity only in the solid portions of the tumor. ROIs were chosen to be centered in the lesion and away from major vessels or bile ducts. The ROI size (both focal liver lesion and uninvolved organ parenchyma) was greater than or equal to 100 mm2. For normal liver parenchyma, ROIs were measured in adjacent liver at approximately the same anteroposterior position of the liver as the tumor, also away from major vessels and dilated bile ducts.
The standard deviation of the background noise (SDnoise) was measured anterior to the ventral abdominal wall in the phase-encoding direction of the image acquisition. ROIs of the background signal were at least 500 mm2. Because the unenhanced and ferumoxides-enhanced MR images were from different acquisitions, the signal intensities of the tumor and liver were normalized to paraspinal muscle signal. Muscle signal is not known to be affected by ferumoxides administration because of the lack of reticuloendothelial cells. Normalization to muscle signal would thus account for potential signal differences caused by MR scanner tuning and coil positioning. The normalized contrast-to-noise ratio (CNR) was calculated as follows: CNR = [(SI lesion / SI muscle) — (SI liver / SI muscle)] / SDnoise, where SI is the signal intensity of the corresponding ROI. Contrast-to-noise ratio values were negative for hypointense lesions and positive for hyperintense lesions. The maximum liver lesion diameter at the same anatomic location was measured before and after ferumoxides administration.
Statistical Analyses
The nonparametric paired sign test was used to assess the difference in
contrast-to-noise ratios before and after the use of ferumoxides. The
Mann-Whitney test was used to compare the difference in increase in
contrast-to-noise ratio between cholangiocarcinoma and colon metastases after
the use of ferumoxides (
% = [contrast-to-noise ratio on enhanced images
— contrast-to-noise ratio on unenhanced images] / contrast-to-noise
ratio on unenhanced images). All calculations were performed using Statview
4.5 (Abracus Concepts, Berkeley, CA).
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Quantitative Analyses
The mean contrast-to-noise ratio on unenhanced imaging for patients with
cholangiocarcinoma was 36.1 ± 36.8; on ferumoxides-enhanced imaging,
the mean contrast-to-noise ratio increased to 75.8 ± 37.5 (p =
0.03). The contrast-to-noise ratio increased in seven of seven patients, with
a median increase of 89% (range, 24-5734%; Fig.
3A,3B).
The mean contrast-to-noise ratio on unenhanced images for patients with colon
metastases was 74.7 ± 52.3; on the ferumoxides-enhanced images, the
mean contrast-to-noise ratio increased to 111.1 ± 60.0 (p =
0.04). The contrast-to-noise ratio increased in nine of 10 patients with colon
cancer, with a median of 52% (Fig.
4A,4B).
In one patient with colon metastases, the contrast-to-noise ratio decreased
(-19%) on ferumoxides-enhanced images. Although the lesion was qualitatively
similar before and after ferumoxides administration, patient motion resulted
in an increased standard deviation of the background noise, thus decreasing
normalized contrast-to-noise ratio.
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Overall, the mean normalized contrast-to-noise ratio increase for cholangiocarcinoma was not different from that of colon carcinoma (p = 0.24).
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Previously, MR imaging with ferumoxides has been shown to be safe and significantly more sensitive than dual-phase CT in the depiction of colorectal metastases [7, 8]. Blakeborough et al. [9] reported that ferumoxides-enhanced MR imaging improved the detection and diagnostic accuracy of focal liver lesions compared with gadolinium-enhanced MR imaging. To our knowledge, the use of ferumoxides for the evaluation of liver extension of intrahepatic cholangiocarcinoma has not previously been studied.
Advances in surgical techniques have improved the long-term survival of patients with intrahepatic cholangiocarcinoma when the tumor is completely resected [1, 10]. However, because hepatic resection is suitable in only a minority of patients with intrahepatic cholangiocarcinoma, imaging has an important role in the preoperative selection of patients who are most likely to benefit from surgery or drainage procedures. The diagnosis and staging of patients with cholangiocarcinoma is usually difficult and is made with the use of many different imaging procedures (sonography, CT, MR imaging, cholangiography). In hilar cholangiocarcinoma, the intrahepatic tumor spread is usually underestimated with sonography [5] and CT [3, 4, 11]. MR imaging may be useful when CT is contraindicated, or in patients with proximal biliary obstruction when CT either does not show an obstructing mass or shows a potentially resectable tumor [11]. Gadolinium-enhanced MR imaging has also been reported to be useful in characterizing hilar cholangiocarcinoma and may provide a critical contribution to the assessment of parenchymal, vascular, and bile duct invasion for determining resectability [11]. The distribution of gadopentetate dimeglumine is similar to that of iodinated contrast agents for CT, so the use of ferumoxides provides an alternative mechanism to gadopentetate dimeglumine for visualizing hepatic tumors. Thus, in our institution we perform ferumoxides-enhanced MR imaging in patients who are potential candidates for surgery on the basis of a staging CT examination.
Our study has several limitations. First, we had a limited number of patients. Because only three patients with cholangiocarcinoma had resectable disease, we did not have precise measurements of tumor size in these patients. Instead, we evaluated the apparent size before and after ferumoxides-enhanced imaging. Second, we could not look for iron particles in the tumors because the time between surgery and biopsy was 7-21 days. Third, some features of the analysis were subjective. Further studies are needed to determine the reliability and cost—benefit ratio of ferumoxides used as a contrast agent in MR imaging of intrahepatic cholangiocarcinoma.
In conclusion, this study suggests that ferumoxides are useful for defining the extent and location of intrahepatic cholangiocarcinoma and should be used before contemplated surgical exploration when CT shows a potentially resectable tumor.
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