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1 Department of Medical Imaging, University Health Network and Mount Sinai
Hospital, University of Toronto, Toronto, ON, Canada.
2 Department of Medical Imaging, NCSB, 1C558, Toronto General Hospital, 585
University Ave., Toronto M5G 2N2, ON, Canada.
Received July 8, 2003;
accepted after revision September 16, 2003.
Address correspondence to M. E. O'Malley
(martin.o'malley{at}uhn.on.ca).
Abstract
 Top Abstract IntroductionMaterials and MethodsResultsDiscussionReferences |
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MATERIALS AND METHODS. Fifty-one patients with newly diagnosed
hepatocellular carcinoma underwent standardized triple-phase CT using a
multidetector scanner. Pathologic proof was obtained in 35 patients (69%); in
16 patients (31%), hepatocellular carcinoma was diagnosed on clinical and
laboratory findings. Two radiologists independently reviewed the CT studies
for the appearance and attenuation of the lesions. Intralesional washout of
contrast material was evaluated subjectively and objectively. Statistical
analysis was performed using Fisher's exact test to analyze the relationships
between tumor appearance and 
-fetoprotein level, tumor grade, and risk
factor. Correlation between tumor size and appearance was analyzed using the
Student's t test and Wilcoxon's rank sum test.
RESULTS. The most common enhancement pattern for hepatocellular
carcinoma was hypervascularity on hepatic arterial phase images with a mosaic
pattern on both arterial and portal venous images; this finding was seen in
86% and 78% of lesions by the two observers, respectively. A hypervascular
component was seen in 96% of lesions by both observers, and the observers
recorded 86% and 63% of lesions as showing washout, respectively. Objective
washout was present in 76% of lesions. Both subjective and objective washout
correlated with an elevated -fetoprotein level (p = 0.01).
CONCLUSION. The appearances of hepatocellular carcinoma on images obtained using MDCT scanners are similar to those described for images obtained using single-detector helical scanners. However, the prevalence of hypervascular hepatocellular carcinoma on MDCT images is higher than previously described on single-detector helical images and most lesions showed washout on portal venous MDCT images.
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Over the past few years, MDCT technology has been introduced into clinical practice. MDCT uses a bank of contiguous detectors to increase effective pitch by 4- to 16-fold, without consequent loss of spatial resolution along the axis of scanning. Single-detector CT typically requires approximately 20 sec to completely scan the liver. Caudal sections of the liver (assuming craniocaudal scanning direction) often show mixed late arterial and early portal venous inflow phases. Multidetector technology allows faster scanning of the liver so that more consistent, uniform hepatic enhancement is achieved during each phase of image acquisition. Although MDCT has been available in clinical practice for several years, little has been written about the impact of multidetector technology on the appearance and attenuation characteristics of hepatocellular carcinomas [3, 8, 10]. Other researchers have concentrated on the improved detection rates of lesions when using multiple scanning phases [14].
The purpose of this study was to describe the appearance and enhancement patterns of hepatocellular carcinoma when using triple-phase MDCT. The study also focused on intralesional contrast washout as seen on arterial and portal venous phase scans.
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In 35 of the 51 patients, the diagnosis of hepatocellular carcinoma was
established by percutaneous biopsy or surgical pathology. In the other 16
patients, the diagnosis was established by a significantly elevated
-fetoprotein level associated with a liver mass or by clinical
diagnosis (e.g., a new or enlarging liver mass in a patient with previous
resection or transplantation for prior hepatocellular carcinoma).
The study group was composed of 40 men and 11 women who ranged in age from 26 to 79 years (mean, 57.6 years). The underlying cause for liver disease was hepatitis B virus (n = 23), hepatitis C virus (n = 9), combined hepatitis B and C viruses (n = 3), alcohol abuse (n = 6), multiple adenomas (n = 1), hemochromatosis (n = 1), and cryptogenic (n = 8).
The -fetoprotein level was recorded in 40 patients (78%) and was
obtained within zero to 181 days of each CT scan (mean delay = 28.4 days).
Eight (20%) of the 40 patients with an -fetoprotein value reported a
normal -fetoprotein level. Mildly elevated -fetoprotein levels
(5–500 ng/mL) were present in 15 patients (38%), and highly elevated
-fetoprotein levels (> 500 ng/mL) were present in 17 patients
(43%).
Pathologic grading was specified in 20 tumors (39%) as follows: well differentiated (n = 7), moderately differentiated (n = 10), and poorly differentiated (n = 3).
CT Technique
All scans were obtained on a 4-MDCT scanner (LightSpeed QX/i, General
Electric Medical Systems, Milwaukee, WI). The amount of IV contrast material
(Omnipaque 300 [iohexol], Amersham Health, Princeton, NJ) given was 2 mL/kg to
a maximum of 200 mL. The injection rate was 5 mL/sec into an antecubital vein.
The scanning parameters were as follows: collimation, 5 mm; reconstruction
interval, 2.5 mm; table speed, 11.25 mm per rotation; pitch, 3; 120 kV; and
190–370 mA. Unenhanced, arterial (30 sec after injection), and portal
venous (60 sec after injection) scans were obtained with a standard
reconstruction algorithm.
Image Analysis
Images were independently reviewed by two abdominal imaging staff
radiologists at a PACS (picture archiving and communication system)
workstation (eFilm version 1.8, Merge eFilm, Toronto, Canada) on which the
observer could manually change the image window and center levels as desired.
Only the largest lesion in each patient was analyzed. The size (largest axial
dimension) and location of the lesion were recorded.
On each phase, each lesion was judged to be of homogeneous or heterogeneous attenuation. Homogeneous lesions were scored as being hypo-, iso-, or hyperattenuating relative to the surrounding liver parenchyma. On arterial and portal venous phase images, heterogeneous lesions were judged as having a predominantly ring, peripheral nodular, or mosaic pattern of enhancement. Ring enhancement was defined as irregular or wavy peripheral enhancement that was continuous or interrupted. Peripheral nodular enhancement was said to be present when the attenuation of the peripheral nodules was similar to the aorta in each phase. A mosaic pattern was present when the enhancement pattern was heterogeneous and did not meet the other definitions.
On hepatic arterial phase images, the presence or absence of hypervascular components within the lesion was recorded. A hypervascular component was defined as an area of enhancement greater than the surrounding liver parenchyma. The location of the hypervascular component within the lesion was recorded on the scoring sheet.
Each lesion was subjectively evaluated for the presence or absence of contrast material washout. Washout was said to be present if any part of the lesion that was hypervascular on the hepatic arterial phase images had a corresponding hypoattenuating area relative to the adjacent liver parenchyma on the portal venous phase images. The presence or absence of abnormal internal vessels, a central scar, fat, and calcification within each lesion was recorded. The presence or absence of a capsule around the lesion was also recorded. A capsule was defined as a smooth, continuous area along the periphery of the lesion that had different attenuation than the surrounding liver (as opposed to ring enhancement).
Quantitative analysis of all lesions was performed. To maintain consistency, one radiologist who was not involved in the image analysis performed all the measurements. The area identified as showing subjective washout by the two observers was measured on the arterial and portal venous phase images using a region of interest that was the same size. Objective washout was present if the attenuation of the lesion was less than that of the adjacent liver in the portal venous phase. For lesions that did not show any subjective washout, the most hypervascular or hyperattenuating component of the lesion was measured. The adjacent liver and aorta were also measured on the same image in each phase for comparison. For liver attenuation measurements, care was taken to choose a homogeneous region of interest that did not include any vessels.
Statistical Analysis
Tests for independence of variables were performed using the chi-square
test. The Fisher's exact test was used to analyze the relationships between
tumor appearance and -fetoprotein level, tumor grade, and underlying
risk factor. Correlation between tumor size and appearance was analyzed using
the Student's t test and Wilcoxon's rank sum test. A p value
of less than 0.05 was considered statistically significant.
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Patterns of Enhancement
The enhancement characteristics and the most common patterns of enhancement
of the 51 hepatocellular carcinomas are summarized in Tables
1 and
2. The most common enhancement
pattern was heterogeneous mosaic in the hepatic arterial phase and in the
portal venous phase. This finding was seen in 86% and 78% of lesions by each
observer (Fig. 1A,
1B). Other patterns of
enhancement were not common.
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The mean attenuation measurement of the lesions in the hepatic arterial phase was 111 H (range, 32–207 H), and it decreased in the portal venous phase (Fig. 2) to a mean of 106 H (range, 36–162 H). There was a mean difference of 26 H (range, 146 to –44 H) between lesion and liver in the arterial phase. On average, the hepatocellular carcinomas measured 11 H (range, –98 to 61 H) less than the adjacent liver parenchyma in the portal venous phase. Region-of-interest measurements of the liver and aorta during each phase indicated the overall quality of contrast material enhancement. The mean attenuation of the hepatic parenchyma was 85 H (range, 54–161 H) during the arterial phase and 117 H (range, 91–150 H) during the portal venous phase. The mean attenuation of the aorta during the arterial phase was 312 H (range, 117–478 H), and it decreased to 161 H (range, 95–262 H) in the portal venous phase.
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Hypervascularity and Washout
Both observers identified hypervascular components on arterial phase images
in 49 (96%) of the 51 hepatocellular carcinomas. Of the 49 hepatocellular
carcinomas with hypervascular components, portal venous phase washout was
subjectively seen in 42 (86%) by one observer and in 31 (63%) by the other
observer. Objective portal venous phase washout, measured by a third
radiologist using region-of-interest measurements, was present in 39 (76%) of
the 51 hepatocellular carcinomas.
Additional Features
The presence of abnormal internal vessels (Fig.
3A,
3B) was the most common feature
reported by both observers, seen in 53% and 45% of lesions. The presence of a
capsule was seen in 20% and 27% of lesions. For each observer, calcification,
fat, and a central scar were seen in 8% and 4%, 4% and 4%, and 0% and 2% of
lesions.
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Correlations
A heterogeneous appearance on unenhanced images correlated with large tumor
sizes (Student's t test, p < 0.01). A heterogeneous
appearance in the portal venous phase was associated with a high level (>
500 ng/mL) of -fetoprotein (Fisher's exact test, p = 0.03).
There was no statistical correlation between the other enhancement patterns
and size or -fetoprotein level. No enhancement pattern was
statistically correlated with tumor grade or underlying risk factor.
On arterial phase images, hypervascular components were seen in 96% of lesions. Only two lesions did not exhibit any hypervascular components, as reported by both observers. One of these lesions was well differentiated in grade (Fig. 4A, 4B), and the other lesion did not have any reported grade on pathology. All other lesions, including the moderately differentiated and poorly differentiated tumors, had a hypervascular component. Otherwise, there was no statistical correlation (Fisher's exact test, p = 0.75) between hypervascularity and underlying tumor grade on arterial phase images.
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Only a small percentage of lesions that appeared hypervascular during the
arterial phase showed neither subjective nor objective washout (Fig.
5A,
5B). Both subjective washout
(Fisher's exact test, p = 0.01) and objective washout (Fisher's exact
test, p = 0.01) were significantly correlated with mildly elevated
and highly elevated levels of -fetoprotein. Another way to define
washout would be a decrease in attenuation within the lesion itself from the
arterial phase to the portal phase, rather than relative to the adjacent liver
parenchyma. Mildly elevated and highly elevated levels of -fetoprotein
were also significantly correlated with this alternative definition of washout
(Fisher's exact test, p = 0.01). There was no correlation between
subjective or objective washout and tumor grade, tumor size, or underlying
risk factor.
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Increasing tumor size correlated with the presence of abnormal internal vessels (Student's t test, p < 0.0001) and a central scar (Wilcoxon's rank sum test, p = 0.01). A correlation between underlying risk factor and the presence of a capsule was noted, with a capsule more likely to be seen in patients with chronic hepatitis C infection, hemochromatosis, and no underlying risk factor (Fisher's exact test, p = 0.001). However, this correlation was noted with only one of the observers. Otherwise, there was no significant correlation with the remaining features.
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Mean attenuation values for hepatocellular carcinomas of 61 H during the arterial phase and 90 H during the portal venous phase were reported by Loyer et al. [10] who used single-detector helical CT. In our study, the hepatocellular carcinomas had a mean attenuation of 111 H on arterial phase images and 106 H on portal venous phase images. The lower mean attenuation value for hepatocellular carcinomas in the hepatic arterial phase in their study can be attributed to the slower injection rate (2.5 mL/sec) and slower image acquisition obtained with a single-detector helical CT scanner. These differences are also reflected by the lower mean attenuation of 62 H for hepatic parenchyma during the arterial phase obtained in their study versus a mean of 85 H in our study.
Ninety-six percent of the hepatocellular carcinomas in our study showed hypervascular components during the arterial phase, as seen by both observers. The percentage of lesions exhibiting hypervascularity using single-detector CT ranged from 33% to 64% in previous studies [3, 6–8, 10]. Again, the much higher percentage of hypervascular lesions in our study is likely due to the more rapid scanning times through the liver afforded by multidetector scanners. The single-detector helical scanners used in previous studies often completed their arterial phase up to 55 sec after injection, at which time contrast material may have already washed out of the lesions. In addition, we used relatively high injection rates of 5 mL/sec for all of our scans, which produced a more consistent arterial phase acquisition. In the other studies, Van Hoe et al. [6], Lee et al. [7], and Loyer et al. [10] used a slower injection rate—2.5–3 mL/sec—than we did. However, in two other studies, Baron et al. [3] and Kanematsu et al. [8] also used a 5 mL/sec injection rate, but they did not consistently use this injection rate for all patients in these studies. In a more recent study, Murakami et al. [14], used the same multidetector scanner, flow rate, and contrast volume of 2 mL/kg that we did, and they found 81–89% of hepatocellular carcinomas to be hypervascular—findings that are similar to ours [14].
Although there was a smaller percentage of hypervascular tumors in the study of Loyer et al. [10] compared with our study, similar washout rates were described, with 18 (82%) of 22 hypervascular lesions showing portal venous washout. Their mean attenuation value of 105 H in the portal venous phase was also similar to that obtained in our study. Our findings suggest that mean attenuation values during the hepatic arterial phase and the presence of hypervascular components are highly dependent on scanning technique.
Slightly more than half of the lesions in our study showed abnormal internal vessels. In a study performed using a single-detector scanner, the prevalence of abnormal internal vessels within hepatocellular carcinoma was 29% [11]. The increased incidence of this finding in our study is likely related to a combination of rapid injection rate and faster image acquisition during the arterial phase that is afforded by multidetector scanners. In our study, visualization of a surrounding capsule was not common and fat and calcifications were rarely seen, which is similar to what has been described on images obtained with single-detector scanners. The prevalence of tumor capsule, fat, and calcifications on images obtained with single-detector scanners have been reported as 39%, 2%, and 9%, respectively [1]. Only one lesion had a central scar, and this scar was reported by only one of our two observers.
No significant correlation was noted between the various enhancement patterns and the grade of the tumor or underlying risk factor. However, the significance of this finding is difficult to assess because of the small sample size of the differing tumor grades and various risk factors. A number of authors have reported hypoattenuating appearances of early or early advanced hepatocellular carcinoma on hepatic arterial phase CT and on CT hepatic arteriography [15–18]. Early or early advanced hepatocellular carcinoma corresponds to well-differentiated grades of hepatocellular carcinoma. The hypoattenuating appearance of these low-grade tumors on CT could be explained by the slower scanners and slower injection rates used previously. However, the hypoattenuating appearance of the lesions on CT hepatic arteriography suggests that these lesions are truly hypovascular. We found that one of the two lesions in our study that did not show a hypervascular component was well differentiated in grade. Unfortunately, because of the small sample size of low-grade lesions, no statistical conclusion regarding washout or enhancement pattern could be made.
Almost all lesions showed hypervascular components with subsequent
subjective and objective washout in the arterial phase. Significant
correlations were noted between elevated -fetoprotein level and both
subjective and objective washout. No significant difference was noted between
lesions with mildly elevated -fetoprotein level and those with highly
elevated -fetoprotein. Otherwise, there was no significant correlation
between -fetoprotein level and the enhancement pattern or appearance of
these lesions. Our findings are consistent with other reports that also showed
a poor correlation between -fetoprotein level and tumor grade or
behavior [19].
Tumor appearances on CT angiography have been recently correlated with tumor grade by Tajima et al. [20]. These researchers proposed that lesions without hypervascular components corresponded to well-differentiated lesions in which the preexisting hepatic arteries had been obliterated by tumor but neovascularized arteries had not yet begun to form. An extrapolation of this study can be made to MDCT, and because MDCT with rapid injection rates can produce diagnostic images approaching CT angiography, the usefulness of CT angiography in the detection of hepatocellular carcinoma has been questioned [13]. Scanning technique is obviously critical, and faster injection rates are thought to provide more reliable enhancement during the hepatic arterial phase and, thus, to more closely replicate CT hepatic arteriography images [21]. Timing of the arterial phase is also important, although variability has been reported for the optimal arterial phase delay time with regard to tumor conspicuity, ranging from 20 to 36 sec [21–23]. Certainly, our delay times were fixed and did not take into account alterations in hepatic perfusion resulting from cardiac output, cirrhosis, or extensive portal vein thrombus or arterioportal shunting.
In summary, most hepatocellular carcinomas showed arterial phase hypervascularity and heterogeneous enhancement in both arterial and portal venous phases when we used MDCT. These findings are similar to those described previously with single-detector helical scanners. However, in our study, the main difference with MDCT was the higher prevalence of hypervascular lesions and abnormal internal vessels seen during the arterial phase. These findings were likely due to a faster, more consistent hepatic arterial phase acquisition obtained with a rapid injection of an appropriate volume of IV contrast material.
Acknowledgments
We thank George Tomlinson for assistance with the statistical analysis.
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1.5 cm) malignant hepatic neoplasms.
AJR 1995;164:879
–884
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