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1
Department of Radiology, D1 Osaka University Medical School, 2-2 Yamadaoka,
Suita City, Osaka 565-0871, Japan.
2
Department of Radiology, Division of Abdominal Imaging, University of
Pittsburgh Medical Center, 200 Lothrop St., Pittsburgh, PA 15213.
Received July 6, 2001;
accepted after revision October 3, 2001.
Address correspondence to T. Kim.
Abstract
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MATERIALS AND METHODS. Double arterial and late phase
contrast-enhanced helical CT scans were obtained on 287 consecutive patients
suspected of having hepatocellular carcinoma. These included 56 patients with
90 small (
3 cm) hepatocellular carcinomas and 50 patients with no
hepatocellular carcinomas. CT scans of these patients were interpreted by
three reviewers. The first arterial phase scan was initiated automatically 10
sec after the bolus-tracking program detected the threshold enhancement of 50
H in the abdominal aorta. Three reviewers interpreted the late phase CT scans
in combination with the first, second, or both hepatic arterial phases.
Measures of the reviewers' detection of hepatocellular carcinoma included
analysis of interobserver variation, sensitivity, specificity, and area under
receiver operating characteristic curve (Az).
RESULTS. The time elapsed from bolus initiation to threshold aortic enhancement ranged from 10 to 24 sec (mean, 13 sec), resulting in initiation of the first arterial phase CT scan from 20 to 34 sec (mean, 23 sec). The combination of late phase CT and both first and second arterial phase images showed significantly better performance than the combination of the late phase and either the first or second arterial phases, although the difference was most evident in comparison with the combination of second arterial and late phases.
CONCLUSION. An automated bolus-tracking program can be used to optimize the timing of hepatic arterial phase CT. Multiphasic CT performed using this technique is useful in detection of small hepatocellular carcinoma.
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A fixed scan delay (20-30 sec) after the initiation of IV contrast injection has been used commonly to start the arterial phase scan [4,5,6,7], without taking into account differences in transit time of contrast material. Several CT manufacturers offer computer-assisted bolus-tracking software to determine the optimal scan delay for each patient [3,11,12]. However, to our knowledge, there have been no reports of the use of this technique for the detection of hepatocellular carcinomas. Recently, a half-second (0.5 sec/tube rotation) helical CT scanner has been developed, which makes it possible to scan the entire liver twice in the arterial phase during a single breath-hold (double arterial phase scan). We performed multiphasic (double arterial phase and late phase) contrast-enhanced CT of the entire liver by using the half-second helical CT scanner combined with automatic bolus tracking for patients suspected of having hepatocellular carcinoma.
The purpose of this study was to evaluate the usefulness of double arterial phase CT for the detection of small hypervascular hepatocellular carcinomas, using automatic bolus tracking to initiate the hepatic arterial phase CT.
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The medical records of 287 patients and all radiologic images, including
images obtained during follow-up examinations, were reviewed by two
experienced radiologists who served as study coordinators. Patients with
hepatocellular carcinoma larger than 3 cm in diameter were excluded, and 56
patients were found to have only small (3 cm in diameter) hypervascular
hepatocellular carcinomas. For confirmatory imaging, all 56 patients underwent
CT hepatic arteriography, CT during arterial portography, and follow-up CT
performed more than 6 months later. Ninety small (3 cm in diameter)
hypervascular hepatocellular carcinomas (0.9-3 cm, mean 1.7 cm) detected in 56
patients were included in this study. Three sets of inclusion criteria for the
tumors were used. First, angiographic findings considered diagnostic of
hypervascular hepatocellular carcinoma were focal lesions that were
hypervascular on CT arteriography and hypoattenuating on CT portography.
Second, proof of hypervascular hepatocellular carcinoma consisted of surgical
resection of 36 lesions in 20 patients and 21-gauge needle biopsies of 10
lesions in five patients, and the other lesions were confirmed by using a
combination of clinical and radiologic criteria, including response to
transcatheter arterial chemoembolization, focal retention of angiographically
administered iodized oil, or progression or regression in size. Third, when
the number of lesions in a patient was less than or equal to three, all
lesions were included; when the number of lesions was more than three, the
largest three lesions less than or equal to 3 cm in diameter were
included.
In 50 of the 287 patients, there was no CT or angiographic evidence of hepatocellular carcinoma on the initial CT or on a follow-up CT performed at least 6 months later. Images of the 56 patients with hepatocellular carcinoma who met our inclusion criteria and those of the 50 patients with no hepatocellular carcinoma were selected for evaluation in this study.
CT was performed with a single-slice helical CT unit (Aquilon; Toshiba Medical, Tokyo, Japan) with a 0.5 sec/tube rotation. Unenhanced scans through the liver were obtained with 7-mm collimation. All contrast-enhanced series were obtained with 5-mm collimation, pitch of 1.5, 5-mm reconstruction interval, and 300-mA tube current.
All patients received 100 mL of low-osmolarity contrast medium (Iopamilon [300 mg of iodine per milliliter]; Nihon Schering, Osaka, Japan) by means of a power injector (Multilevel CT injector; Medrad, Pittsburgh, PA). Contrast medium was injected at 5 mL/sec through a 20-gauge plastic IV catheter placed in an antecubital vein for 254 of the 287 patients. When venous access permitted placement of only a 20-gauge catheter, contrast material was injected at a rate of 3 mL/sec for the remaining 33 patients.
The automatic bolus-tracking program (Surestart, Toshiba Medical) was used to automatically start the first arterial phase scan after the injection of contrast material. This technique is capable of real-time monitoring, automatic calculation of CT values in a region of interest (ROI), and automatic initiation of diagnostic CT after the CT value of the ROI has reached a trigger threshold level after the injection of contrast material (Fig. 1). The anatomic level for monitoring was set just above the diaphragmatic dome, which was the same level as the start position of the diagnostic scan, and the ROI cursor was placed in the aorta. Real-time low-dose (120-kVp, 50-mA) serial monitoring scans were initiated 10 sec after the start of injection of contrast material. During the 10-sec interval between the start of contrast material injection and the start of the monitoring scan, patients were carefully monitored by a radiologist for side effects and extravasation of contrast material. The trigger threshold level was set at an increase of 50 H over baseline for the aortic ROI. Ten seconds after the trigger, the first arterial phase helical CT scan started automatically. With our CT system, 10-sec duration was the shortest allowable interval between the trigger and the initiation of the diagnostic scan. The second arterial phase helical CT scan was initiated 5 sec after the end of the first arterial phase scan, and the duration of 5 sec between the first and second arterial phase scans was also the shortest possible. The first and second arterial phases were performed during a single breath-hold. Two minutes after the end of the second arterial phase scan, the late phase helical CT scan was obtained.
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Image Analysis
Quantitative analysis.—Quantitative analysis was performed
by two radiologists serving as study coordinators. Time elapsed from the start
of injection until the trigger value was reached, time until initiation of the
first and the second arterial phase scans, and scanning time of the helical
scan for all 287 cases were calculated.
The attenuation (in Hounsfield units [H]) of the abdominal aorta, the portal vein, and the liver parenchyma at the level of the right portal vein bifurcation, representing the center level of the liver, was measured before and after administration of contrast material. Circular ROI cursors at least 1 cm in diameter were placed in the aorta and in the portal vein, and one of at least 2 cm in diameter was placed in the anterior segment of the liver while avoiding vascular structures. Relative enhancement was defined with the following formula:
[relative enhancement (H)] = [attenuation on contrast-enhanced CT] - [attenuation on pre-contrast CT].
Relative enhancement of the aorta, the portal vein, and the liver parenchyma in the first and second arterial phases was calculated for each patient. The attenuation of the 90 hypervascular hepatocellular carcinomas and the surrounding liver parenchyma was also measured on the first and second arterial phase CT. ROI cursors as large as possible were placed in the hepatocellular carcinomas and in the liver parenchyma adjacent to the hepatocellular carcinomas. Relative contrast-attenuation difference between the enhancing hepatocellular carcinoma lesion and the surrounding liver on the first arterial and second arterial phase CT was calculated for the 90 hypervascular hepatocellular carcinomas with the following formula:
[relative contrast attenuation difference] = [attenuation of hepatocellular carcinoma] - [attenuation of the surrounding liver parenchyma].
Relative enhancement of the aorta, portal vein, and liver parenchyma and attenuation and relative contrast-attenuation difference of hepatocellular carcinoma for the first arterial phase was compared with that for the second arterial phase. The paired t test was used for statistical analysis, and a two-tailed p value of 0.05 was considered significant.
Qualitative analysis.—Receiver operating characteristic (ROC) analysis was used for qualitative analysis of the CT images. CT images used for ROC analysis were selected by the two radiologists serving as coordinators. One image each of the first and second arterial phases and of the late phase of all the 90 small hypervascular hepatocellular carcinomas was selected. Furthermore, to prevent bias, if a lesion was present on images obtained at several anatomic levels, only one image of the anatomic level containing the largest part of the lesion was used. Therefore, 90 images each of the first and second arterial and late phases of the 56 patients with small hypervascular hepatocellular carcinomas were selected. In addition, we took the CT scans of 50 patients with no hepatocellular carcinoma and selected 84 representative anatomic levels from the first arterial, second arterial, and late phases. These 84 image sets plus the 90 sets of CT images of hepatocellular carcinomas constituted the data used for the ROC analysis.
Three experienced radiologists other than the study coordinators reviewed hard-copy CT images. The reviewers were blinded to the patients' information and to the presence or location of liver lesions. Three CT image sets were read: first, a set of first arterial and late phase CT images; second, a set of second arterial and late phase CT images; and finally, a set of first and second arterial (double arterial) and late phase CT images. The interval between each of the blinded reviews was at least 2 weeks. The reviewers scored each image set for the presence or absence of a hypervascular hepatocellular carcinoma, and they assigned the following confidence levels to their observations: 1, definitely absent; 2, probably absent; 3, possibly present; 4, probably present; 5, definitely present.
To assess interobserver variability, the kappa statistic for multiple reviewers was calculated, using a non-weighted binary kappa statistic. Of the 90 proven hypervascular hepatocellular carcinoma lesions, lesions that were assigned a confidence level of 3 or greater were considered to be true-positive findings. The findings of a lesion were considered to be false-negative if it was assigned a confidence level of 1 or 2, but a lesion was actually present. The degree of disagreement was not factored into the calculation. This categorization of a confidence level of 3 or greater as representing a positive diagnosis of hepatocellular carcinoma had been conveyed to the three reviewers before the interpretation of the images. A kappa value of 0.01-0.20 was considered to represent slight agreement; 0.21-0.40, fair agreement; 0.41-0.60, moderate agreement; 0.61-0.80, substantial agreement; and 0.81-1.0, almost complete agreement. Sensitivity and specificity were calculated for the first arterial and late phases, for the second arterial and late phases, and for the double arterial and late phases. A binomial ROC curve was fitted to each observer's confidence-rating data by maximum likelihood estimation. The diagnostic accuracy of each imaging technique was determined by calculating the area under each reviewer-specific binomial ROC curve (Az). Differences among the three image sets in terms of the mean Az values were statistically analyzed first with the two-factor analysis of variance. If the differences were significant, differences between two of the three image sets were statistically compared with the Fisher's protected least significant difference test. A p value of greater than 0.05 was considered significant.
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Table 1 shows the relative enhancement of the aorta, portal vein, and liver parenchyma in the first and second arterial phases. The relative enhancement of the aorta was significantly greater in the first than in the second arterial phase (p < 0.01), whereas those of the portal vein (p < 0.01) and liver parenchyma (p < 0.05) were significantly greater in the second than in the first arterial phase. Whereas the attenuation of the hepatocellular carcinomas was significantly greater in the second than in the first arterial phase (p < 0.05), the relative contrast-attenuation difference between hepatocellular carcinoma and surrounding liver parenchyma was significantly (p < 0.01) greater in the first than in the second arterial phase (Table 2).
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The kappa values for the three observers, calculated on the basis of each observer's confidence level for the ROC analysis, were 0.79 for the first arterial and late phases, 0.73 for the second arterial and late phases, and 0.88 for the double arterial and late phases. The kappa values for the three observers showed substantial or almost complete agreement with regard to the presence of lesions. Table 3 shows the Az values for the detection of the hypervascular hepatocellular carcinomas. The mean Az value for the double arterial and late phase images was greatest, followed by, in diminishing order, those for the first arterial and late phase images and for the second arterial and late phase images. The improved performance using the double-arterial and late phases was significantly better (p < 0.05) than that using either the first or second arterial phase with late phase combination.
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The detection sensitivity and specificity of the three reviewers for the small hypervascular hepatocellular carcinomas are shown in Table 4. The mean sensitivity for the double arterial and late phase images was significantly greater (p < 0.05) than that of the combination of first arterial and late phases or the second arterial and late phases (Figs. 3A,3B,3C,3D,3E and 4A,4B,4C,4D,4E). Specificity did not vary significantly between the double arterial plus late phases combination and either the first or second arterial plus late phases combination.
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We used the bolus-tracking technique to determine the elapsed time from IV injection to a threshold trigger of 50 H aortic enhancement and found that it varied from 10 to 24 sec among our patients. Because the optimal time window for CT detection of hypervascular hepatocellular carcinoma may last only a few seconds, it is apparent that some means of individualizing the scan delay is necessary. The mean elapsed time from IV injection to a threshold trigger of 50 H aortic enhancement was 13 sec, although aortic enhancement in many of the patients reached the threshold in the first monitoring scan obtained 10 sec after IV injection. Although it might be advantageous to start the monitoring scans somewhat sooner, we do not advocate this procedure because we prefer to physically monitor and observe the patients for the first 10 sec of the injection for any adverse effects, including extravasation. Moreover, our results indicate that we achieved the goals of hepatic arterial phase imaging, namely bright aortic enhancement, moderate portal venous enhancement, and minimal hepatic parenchymal enhancement.
Other investigators have advocated a test bolus injection technique to optimize timing for multiphasic liver CT [13,14,15]. Foley et al. [14] used a multislice helical CT scanner and the test bolus technique to evaluate optimal CT detection of hypervascular liver tumors. They determined that the attenuation difference between the hypervascular tumors and liver was significantly greater on what they called the second hepatic arterial phase, whereas our results showed that these tumors were more apparent on what we called the first arterial phase. These discrepant results may be explained by differences in the monitoring technique and in the delay time used for the first and second arterial phases in these two studies. Foley et al. measured the elapsed time to peak aortic enhancement and used this as the time to initiate the first arterial phase. We also monitored aortic enhancement but triggered the scan when aortic enhancement reached 50 H. The minimum delay in our scanner between the trigger point and acquisition of the first diagnostic scan is 10 sec. Because the trigger threshold in our subjects was reached from 10 to 24 sec, we initiated the first arterial phase scanning at 20-34 sec (mean, 23 sec). Using the test-bolus technique, Foley et al. initiated their first arterial phase scanning at 14 to 21 sec (mean, 18 sec). In both investigations, the second arterial phase commenced almost immediately after completion of the first, still in a single breath-hold. Of interest, the average hypervascular tumor-to-liver attenuation difference in Foley's second arterial phase was identical to that determined for our first arterial phase images, probably because they were obtained within about the same time after injection. We can conclude that arterial phase images obtained from 14 to 21 sec (Foley's first phase) are too early in most patients and that those obtained at 34-52 sec (our second arterial phase) are too delayed in many patients.
The automated bolus-tracking technique that we used offers certain advantages, including the fairly rapid and automatic initiation of the diagnostic scan once the threshold trigger is reached for aortic enhancement. Other computer-based bolus-tracking techniques have required a considerable delay between the test monitoring CT sections, display of the enhancement curve, and initiation of the diagnostic scan. The technique we used monitors enhancement in almost realtime and can trigger the diagnostic scan 10 sec later Prior bolus-tracking techniques have been effective for monitoring and initiating portal venous phase CT imaging, which is well suited for evaluation of hypovascular liver tumors and many other pathologic processes [11]. In these applications, the monitoring ROI cursor is usually placed over the liver, and the diagnostic scan is initiated when liver enhancement has reached a threshold, such as 50 H above baseline. This technique is not applicable for detection of hypervascular tumors in which the goal is to detect the tumors as hyperattenuating foci on a background of minimally enhanced liver.
Both the test-bolus technique used by Foley et al. [14] and other investigators and the automated bolus-tracking technique that we used monitored aortic enhancement. Our choice of a threshold of 50 H aortic enhancement versus the Foley threshold of peak aortic enhancement may have resulted in our first arterial phase images being obtained somewhat later than those in their investigation. Use of the test-bolus technique requires the administration of an additional 12-20 mL of contrast material [13,14,15] and is more time-consuming and less convenient than the use of the automated bolus-tracking technique.
Even with the use of the bolus-tracking technique for optimal timing of the CT scans, we found that the use of both the first and second arterial phases resulted in significantly improved detection of hepatocellular carcinoma. However, the combination of the first arterial phase and late phase CT, as we defined them, achieved a sensitivity of 90% and a specificity of 92%, which compare favorably with those achieved by the combination of the double arterial and late phase CT (sensitivity, 97%; specificity, 93%).
The CT protocol ultimately chosen requires balancing marginal improvement
in disease diagnosis with potentially deleterious effects including increased
time, expense, and radiation exposure. We did not obtain CT images during the
portal venous phase but substituted later phase (160-190 sec) images. Whereas
the portal venous phase (
60-90 sec) is often optimal for CT detection of
most hypovascular liver tumors, it is less useful for detection of
hepatocellular carcinoma, which is often nearly isoattenuating to liver on
portal venous phase images but is typically hypoattenuating to liver on later
phase CT [4]. Because detection
of hepatocellular carcinoma was our goal, we chose to eliminate the portal
venous phase.
One limitation of our study could be the lack of histologic proof for each hepatocellular carcinoma lesion, although all lesions were subjected to several confirmatory studies, including CT arteriography, CT arterial portography, and follow-up CT. Moreover, we could use criteria such as focal retention of iodized oil and progression or regression of lesions after transarterial chemoembolization. Whereas none of these are a gold standard, we think they constitute compelling confirmation of the hepatocellular carcinoma diagnosis.
The volume of contrast material that we used was 100 mL, which is less than that used in other investigations from North America and Europe. The mean weight of our patients was 60 kg. The injection ratio of 1.7 mL/kg seems to be in line with that used for investigations with a larger mean weight per patient.
In summary, our results show that an automated bolus-tracking program can be used to time, optimally and individually, the acquisition of hepatic arterial phase CT images. Acquiring both a first and second arterial phase set of images allows detection of small hepatocellular carcinomas with greater sensitivity than acquiring images with either single arterial phase scan.
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