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Gastrointestinal Imaging |
1 From the Departments of Radiology (H.J.J., J.H.L., S.J.L., H.S.P., Y.S.D.) and Diagnostic Pathology (C.K.P.), Samsung Medical Center, College of Medicine, Sungkyunkwan University, 50 Ilwon-dong, Kangnam-ku, Seoul 135-710, Korea. Received January 5, 1999; revision requested April 2; final revision received September 7; accepted September 15. Address correspondence to J.H.L. (e-mail: jhlim@smc.samsung.co.kr).
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Abstract |
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 TOP Abstract IntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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MATERIALS AND METHODS: Fifty-two consecutive patients with pathologically proved HCC underwent THCT (hepatic arterial, portal venous, and delayed phases) and combined CTAP and CTHA. Two radiologists reviewed the images in three sessions: first the THCT images alone, then with the CTAP images, and finally all three sets of images.
RESULTS: There were 73 pathologically confirmed HCCs. Among 72 lesions considered as HCC at THCT, 69 were proved to be HCCs. Of the additional 37 nodules interpreted as HCC at CTAP, only one was confirmed as such. Among the additional 20 lesions presumed to be HCC at combined CTAP and CTHA, only two were proved to be HCCs. The sensitivity was 94% (69 of 73 lesions) at THCT, 96% (70 of 73) with additional CTAP, and 97% (71 of 73) with all three modalities. The positive predictive value was 96% (69 of 72) at THCT, 65% (70 of 107) with additional CTAP, and 80% (71 of 89) with all three modalities.
CONCLUSION: The use of CTAP and CTHA, in addition to being invasive and costly, resulted in an unacceptably high false-positive rate without a substantial increase in sensitivity. Therefore, CTAP and CTHA are not recommended for preoperative evaluation of HCC; THCT alone is preferred.
Index terms: Computed tomography (CT), comparative studies, 761.12112, 761.12114, 761.12115 • Liver, CT, 761.12112, 761.12114, 761.12115 • Liver neoplasms, 761.31, 761.323 • Liver neoplasms, CT, 761.12112, 761.12114, 761.12115
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Introduction |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Hepatocellular carcinoma (HCC) usually occurs in underlying cirrhosis (10). Although metastatic tumors invariably lack portal venous supply, various nodules that manifest in cirrhotic liver have a complicated blood supply from the portal vein and hepatic artery. Hence, characterization of these nodules is often difficult at CTAP. Furthermore, associated portal hypertension and hepatic parenchymal changes that result in hemodynamic alterations such as arterioportal shunt (8,11,12) cause added difficulty. Despite such limitations, the reported sensitivity of CTAP in the detection of HCC exceeds that of any other imaging method except intraoperative ultrasonography (US) (13). Reports (14–17) suggest that in patients with cirrhosis, the combined use of CT hepatic arteriography (CTHA) and CTAP would be helpful in overcoming such limitations of CTAP. However, to our knowledge, the role of CTAP alone or in combination with CTHA for the preoperative evaluation of HCC has not yet been determined.
Technical advances in multiphasic helical CT scanning have improved the detection and characterization of hepatic neoplasms, particularly hypervascular varieties such as HCC (18–22). CTAP is highly sensitive for lesion detection; however, it is invasive, costly, and has a high false-positive rate. There have been several studies to evaluate whether CTAP could be replaced by other less invasive imaging techniques such as helical CT (5,23,24) and magnetic resonance (MR) imaging (25). Some investigators have concluded that helical CT should replace CTAP for the detection of metastasis (23,24), whereas in studies in which two-phase helical CT or MR imaging was compared with CTAP for the detection of HCC, they concluded the opposite (5,25). However, to our knowledge, there is no reported comparison between triple-phase helical CT (THCT) and a combination of helical CTAP and CTHA for the preoperative evaluation of HCC.
The purpose of our study was to determine whether the combination of CTAP and CTHA provides an added benefit to THCT in the preoperative evaluation of HCC.
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MATERIALS AND METHODS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Thus, 52 consecutive patients (35 men, 17 women; mean age, 54.8 years; age range, 28–71 years) were included in this study. The diagnosis of HCC was proved pathologically—that is, at surgery in 41 patients and at biopsy in 11 patients. All of the tentative HCCs that were diagnosed at THCT were finally proved either at surgical pathologic analysis or at subsequent biopsy in the nonsurgical candidates. All 52 patients were followed up with THCT for 12–29 months (mean, 17.4 months). All patients gave written informed consent, and institutional review board approval was obtained.
Imaging Technique
All CT examinations—that is, THCT, CTAP, and CTHA—were performed with a helical CT scanner (HiSpeed Advantage; GE Medical Systems, Milwaukee, Wis). The images were obtained in a craniocaudal direction with 7-mm collimation, 7 mm/sec table speed during a single breath-hold helical acquisition of 25–30 seconds, depending on liver size, and a 7-mm reconstruction interval. For THCT, hepatic arterial phase, portal venous phase, and delayed phase scanning began 30 seconds, 60 seconds, and 180 seconds, respectively, after the injection of 100 mL of nonionic iodinated contrast material (Iopamiro 300; Bracco, Milano, Italy) through the antecubital vein at a rate of 3 mL/sec.
For CTAP and CTHA, arterial vascular access was obtained with bilateral femoral artery punctures by using the Seldinger technique. Two catheters were selectively placed—one (Cobra; Cook, Bloomington, Ind) in the superior mesenteric artery and the other (Yashiro; Terumo, Tokyo, Japan) in the common hepatic artery or replaced right hepatic artery arising from the superior mesenteric artery, depending on arterial variance. Before CTAP and CTHA, celiac and superior mesenteric angiographic examinations were performed, with use of 50–60 mL of nonionic contrast material (Iopamiro 300), to evaluate the vascularity of the HCC and the vascular anatomy. The hepatic arterial anatomic variations identified were in seven patients in whom the right hepatic artery arose from the superior mesenteric artery and in one patient in whom both the right and left hepatic arteries arose from the superior mesenteric artery. After angiography, the patients were transferred to CT units.
CTAP and CTHA were performed 20–30 minutes after angiography. For CTAP, a 5-F catheter was placed in the superior mesenteric artery. A total of 90 mL of nonionic contrast material (Iopamiro 300) was injected, and CT scanning was performed 25 seconds after the start of the injection, with a power injector, at a rate of 2.5 mL/sec. For CTHA, the other 5-F catheter was placed in the common hepatic artery, or replaced right hepatic artery if it arose from the superior mesenteric artery, and 45 mL of contrast material (Iopamiro 300) was injected at a rate of 1.5 mL/sec. CT scanning from the dome of the liver was initiated 5 seconds after the start of the injection. When the liver was supplied by two arteries, both were selected one by one and CT scanning was performed twice to obtain a complete hepatic arteriogram at CT.
Image Analysis
Two experienced radiologists (J.H.L. and S.J.L.) reviewed the CT images together by means of consensus; they had no prior knowledge of the final results. The readers were shown the THCT images first, and then the CTAP images were added for review. At the third session, CTHA images were also added; the interval between each session was 1 week. The number, size, and enhancement characteristics of the presumed HCCs, dysplastic nodules, and pseudolesions were assessed. All images were evaluated on a 2,000 x 2,000 Picture Archiving and Communication Systems (PACS; GE Medical Systems Integrated Imaging Solutions, Mt Prospect, Ill) monitor. At each reading, the window settings of all the THCT images were fixed at a window width of 200 HU and window level of 30 HU. However, because the range of contrast enhancement during CTAP and CTHA varied markedly, the optimal window setting in each case was adjusted as needed.
For objectivity and reproducibility of the image analysis performed in this study, the criteria for HCC, dysplastic nodule, and pseudolesions (11,26,27) were determined; however, it may be somewhat arbitrary to establish the imaging criteria of nodules within the spectrum of hepatocarcinogenesis. At imaging analysis, the dysplastic nodule category consisted of those nodules other than HCC that were presumed to be related to cirrhosis; this included regenerative nodules. Thus, the criteria for dysplastic nodule described here may not be representative of dysplastic nodules at pathologic analysis in general. The distinction between HCCs and dysplastic nodules was based on usual pattern of blood supply (28–30), nodule size (30–32), presence or absence of a capsule (33), nodule location, nodule shape, and similarity to a pathologically proved nodule in the same liver (5). The size criterion was based on the fact that most regenerative nodules are 3–8 mm in diameter and their size rarely exceeds 1 cm (30) and that dysplastic nodules without malignant foci are usually less than 1.2 cm in diameter (31,32). We arbitrarily determined 1 cm as a practical cutoff value to reduce possible overlap with early-stage HCC, the mean diameter of which is less than 1.5 cm (34).
The criterion for HCC at THCT was basically a nodule showing the enhancement pattern of hepatic arterial blood supply and no portal venous supply—for example, a hyperattenuating or isoattenuating lesion during the hepatic arterial phase and lesion with lower attenuation during the portal venous and delayed phases compared with that during the hepatic arterial phase (28). In addition, the following lesions were regarded as HCCs at THCT: a nodule of mixed attenuation with areas of washout during the portal venous and delayed phases; a nodule with discrete capsular enhancement during the delayed phase; a nodule with an enhancement pattern similar to that of the main mass (ie, the preoperatively proved HCC); and a nodule larger than 1 cm that was predominantly hypoattenuating during the hepatic arterial phase (35,36). The criterion for a dysplastic nodule at THCT was a nodule smaller than 1 cm that was hypoattenuating during all three phases or a hypoattenuating nodule that was seen only during the delayed phase (37).
The criterion for HCC at CTAP was (a) an area of perfusion defect that coincided with tentative HCC at THCT, (b) a round perfusion defect showing soft-tissue attenuation (ie, attenuation of skeletal muscle) (11), or (c) a round perfusion defect larger than 1 cm in diameter showing intermediate attenuation (ie, degree of attenuation between that of skeletal muscle and that of normal enhancing hepatic parenchyma) (11). The criterion for a dysplastic nodule at CTAP was (a) a round perfusion defect smaller than 1 cm showing intermediate attenuation or (b) a round perfusion defect of any size with intermediate attenuation that coincided with a tentative dysplastic nodule at THCT. The criterion for a pseudolesion at CTAP was a wedge-shaped, flat, or irregularly shaped perfusion defect (11,26,27) or a perfusion defect around the gallbladder fossa, medial segment of the left hepatic lobe anterior to the porta hepatis, or intersegmental fissure, without a corresponding lesion at THCT (11,26,27).
The criterion for HCC at CTHA was (a) an enhancing lesion that coincided with tentative HCC at THCT, (b) a round enhancing lesion that coincided with a round perfusion defect at CTAP, or (c) a round enhancing lesion larger than 1 cm without a corresponding lesion at THCT and CTAP. The criterion for a dysplastic nodule at CTHA was a discrete, round, hypoattenuating lesion. The criterion for a pseudolesion at CTHA was an enhancing area that did not meet the criteria for HCC.
Typical cysts and hemangiomas were marked at THCT so that they would not be counted at CTAP and CTHA. The presence or absence of HCC and lesion category—that is, HCC, dysplastic nodules, or pseudolesion—were determined by means of consensus between the two radiologists.
In the cases of resected lobes or segments, the standard of reference was the result of pathologic analysis of the surgical specimen. All resected specimens were cut into 5-mm sections and retrospectively reviewed by one experienced pathologist (C.K.P.). In the nonsurgical cases and for the remaining livers after hepatic resection, the standards of reference were the results of biopsy and follow-up THCT for a minimum of 12 months. The final number of HCCs in the unresected part of the liver was determined as follows: Biopsy was performed on all tentative HCCs detected at initial THCT. All additional nodules or pseudolesions identified at CTAP or CTHA were correlated with the findings at follow-up THCT by means of lesion-to-lesion analysis. We assumed there was no HCC when there was no discernible lesion or there was no interval change in the size or shape of the nodule at THCT for a minimum of 12 months. If there was a growing nodule at THCT during the follow-up period, biopsy was performed subsequently. The following were not included in the final number of HCCs: recurrent masses at the resection margin where no lesion was seen at preoperative imaging in two patients and new lesions after 17–23 months in an area where no lesion had been previously (regarded as metachronous HCCs) in eight patients.
Sensitivity was defined as the number of HCCs correctly detected at each reading session divided by the final number of HCCs proved by using pathologic analysis. The false-positive rate was defined as the number of false-positive lesions detected at each reading session divided by the total number of lesions (true-positive and false-positive) considered to be HCC at each session. The positive predictive value was defined as the number of HCCs correctly detected at each session divided by the total number of lesions considered to be HCC at each session.
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RESULTS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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At review of all three sets of images, 89 nodules—69 lesions at THCT and 20 additional lesions at combined CTAP and CTHA—were interpreted as HCC. Among these, 71 nodules were confirmed to be HCC (Fig 1c). Two HCCs 4 mm in diameter were not detected with any of the three modalities. Reading of the combined THCT, CTAP, and CTHA images yielded 18 false-positive nodules (Fig 2, Table) and two false-negative nodules, resulting in a sensitivity of 97% (71 of 73 lesions), false-positive rate of 20% (18 of 89 lesions), and positive predictive value of 80% (71 of 89 lesions). Four of the 89 tentative HCCs were seen only at CTHA. Twenty-three of the 107 lesions that were presumed to be HCC at interpretation of the combined THCT and CTAP images were recategorized as dysplastic nodules in eight cases and as pseudolesions in 15 cases when the CTHA images were added. Thus, the addition of CTHA prevented false-positive diagnoses of HCC in 23 nodules. These nodules were confirmed to be lesions other than HCC: Seven were dysplastic nodules in the resected specimens, and the others were either normal at pathologic analysis or no longer seen at follow-up THCT. The three false-positive nodules at THCT alone were correctly categorized with CTAP and CTHA. Among the 20 additional nodules that were interpreted as HCC on the combined CTAP and CTHA images, only two were confirmed to be HCC (Fig 3).
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DISCUSSION |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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All of the final 18 false-positive nodules were hypoattenuating at CTAP and hyperattenuating at CTHA and thus indistinguishable from HCC. Although pseudo-HCCs tend to be small and homogeneous, we could not find any reliable criteria to distinguish them from true HCCs, even in retrospect. Such false-positive lesions are not uncommon. Kim et al (38) reported that nodular arterioportal shunt could mimic HCC at two-phase helical CT. The arterioportal shunt appeared at two-phase helical CT as an area of high attenuation during the hepatic arterial phase and as slightly high attenuating or isoattenuating with the liver during the portal venous phase, but it never appeared as a low-attenuating area. With CTAP and CTHA, distinguishing a nodular arterioportal shunt from an HCC is likely to be more problematic because the shunt is seen more frequently and both structures have similar attenuation patterns at CTAP and CTHA. Some of the pseudo-HCCs in this study, particularly those that had no corresponding pathologic finding in the resected specimen, may have represented nodular arterioportal shunts.
Another possible explanation for some pseudo-HCCs could be an unusual type of regenerative or dysplastic nodule, although there is no clear reason. According to Lim et al (30), some regenerative nodules may be hypoattenuating at CTAP and hyperattenuating at CTHA. They speculated that diminished portal venous flow in certain regenerative nodules is an initial process of hepatocellular carcinogenesis and the reciprocal increase in hepatic arterial supply might result in such an appearance. In another more recent study by Lim et al (39), some (five of 32) dysplastic nodules demonstrated such a reciprocal relationship, that is, decreased portal venous supply and increased arterial supply. Other investigators (40) have also reported that dysplastic nodules can enhance during the hepatic arterial phase of both CT and MR.
The rate of HCC detection ranges from 38% to 84% with conventional CT (1,2,6) and is 87% with biphasic helical CT (9). Compared with the results in these reports, the results of THCT in our study indicated a much higher sensitivity (94% [69 of 73 lesions]). This is partly understandable, because the number of the tumors per patient in our study was small and the readers were aware that all the patients had histologically proved HCC. Another explanation is that THCT including the delayed phase has several advantages compared with biphasic CT. The delayed phase of helical CT has been reported to show higher liver-HCC contrast than does the portal venous phase (41) and thus improve the rate of detecting well-differentiated hypovascular HCCs (35). In the Hwang et al (42) study, there was a considerable chance (seven of 81 HCCs) of missing an HCC when only hepatic arterial phase and portal venous phase images are obtained. In the present study, one HCC was seen only during the delayed phase, and many HCCs with subtle enhancement during the hepatic arterial phase were detected with the help of the delayed phase; some of these tumors could have been missed if the images in each of the three phases had been interpreted separately.
The patients included in this study represented a select group of potential candidates for hepatic resection who had relatively tolerable liver function. They had one or two nodular HCCs, confined to one hepatic lobe, that were demonstrated at THCT. Therefore, our patient population was vastly different from that of patients with end-stage hepatic disease who are being evaluated for liver transplantation. The latter group represents yet another select group of patients who have no or a few small HCCs depicted on imaging studies, but who also have more advanced cirrhosis. Thus, they potentially have many more dysplastic nodules or small HCCs that are not apparent on imaging studies (43). 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 HCCs and varying degrees of cirrhosis (9,15–17) also would have limitations because of difficulties in lesion-to-lesion analysis and in obtaining histopathologic confirmation of the majority of the nodules.
False-positive lesions were seen in 15 patients at combined CTAP and CTHA. This result was important because the false-positive lesions prevented surgery in seven of these patients. In another four patients, additional nodules were detected in the other lobe at CTAP and CTHA, and surgery was performed because these additional nodules turned out to be pseudolesions at intraoperative US. In the remaining four patients, the false-positive results did not substantially alter their treatment because the additional nodules detected were in the same lobe as the main lesion. Hence, combined CTAP and CTHA did not fulfill the anticipated role of either enabling the selection of surgical candidates or reducing the need for intraoperative US. The results of this study indicate that the routine use of combined CTAP and CTHA is not beneficial in the preoperative evaluation of patients with HCC.
To our knowledge, most of the other studies in which CTAP and CTHA were evaluated have not included any objective interpretation criteria for HCC or considered premalignant lesions. To improve objectivity and reproducibility, before analysis we determined the criteria for each nodule entity on the basis of its blood supply, but these criteria are not well validated at this point. However, nodules related to cirrhosis have a wide variety of CT appearances. The results of one study (44) showed that not all foci of HCC were hyperattenuating at CTHA. The results of a radiology-histopathology correlation suggested that the hemodynamic properties of early HCC are different from those of overt HCC, with different enhancement patterns at CTAP and CTHA (36). In addition, the difference in enhancement patterns was not correlated with the degree of dedifferentiation of HCC (36). This difficulty in establishing the distinctive criteria for interpreting various nodules in cirrhosis on the basis of blood supply may add limitations to CTAP and CTHA in clinical practice.
In the patients who did not undergo surgery, follow-up THCT was used as the reference standard method to exclude HCC. This was an inherent limitation of our study. In these cases, we could have missed small and very slowly growing isoattenuating HCCs that were invisible on any of the three imaging studies and thus excluded these lesions from our final number of HCCs. This limitation may also partly explain the high sensitivity rate in our study compared with that in studies with patients being considered for transplantation (44). However, for the additional false-positive nodules at CTAP and CTHA, the results of lesion-to-lesion analysis, in which there was a minimum follow-up of 12 months and mean period of 17 months, seemed sufficient to exclude malignancy.
In summary, for preoperative evaluation of HCC, THCT had comparable sensitivity and a superior positive predictive value compared with CTAP, and even with CTAP used in conjunction with CTHA. At CTAP and CTHA, there was a considerable number of nodular pseudolesions mimicking HCC that might have seemingly contraindicated surgery in patients with otherwise resectable tumors. Considering the frequent false-positive findings, invasiveness, and high cost of CTAP and CTHA, these examinations should not be included in the routine preoperative work-up for the detection of HCC.
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Acknowledgments |
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Footnotes |
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Author contributions: Guarantor of integrity of entire study, H.J.J.; study concepts, J.H.L.; study design, H.J.J.; definition of intellectual content, J.H.L.; literature research, H.J.J.; clinical studies, C.K.P., H.S.P., Y.S.D.; data acquisition, C.K.P., H.J.J., H.S.P., Y.S.D.; data analysis, S.J.L., J.H.L.; manuscript preparation and editing, H.J.J.; manuscript review, J.H.L.
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References |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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