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1
Department of Radiology, Samsung Medical Center, Sungkyunkwan University
School of Medicine, 50 Ilwon-dong, Kangnam-ku, 135-710 Seoul, Korea.
2
Department of Diagnostic Pathology, Samsung Medical Center, Sungkyunkwan
University School of Medicine, Kangnam-ku, 135-710 Seoul, Korea.
3
Department of Gastroenterology, Samsung Medical Center, Sungkyunkwan
University School of Medicine, Kangnam-ku, 135-710 Seoul, Korea.
4
Department of General Surgery, Samsung Medical Center, Sungkyunkwan University
School of Medicine, Kangnam-ku, 135-710 Seoul, Korea.
Received November 18, 1999;
accepted after revision January 19, 2000.
Address correspondence to J. H. Lim.
Abstract
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SUBJECTS AND METHODS. Three-phase helical dynamic CT in 41 patients with liver cirrhosis was evaluated prospectively before orthotopic liver transplantation. The numbers of hepatocellular carcinomas and dysplastic nodules were assessed in the explanted livers and compared with pretransplantation CT findings.
RESULTS. Examination of the explanted livers revealed 21 hepatocellular carcinomas in 15 patients and 23 dysplastic nodules in 10 patients. The size of the hepatocellular carcinomas was 0.6-5.0 cm (mean, 1.9 cm), and that of the dysplastic nodules was 0.7-2.0 cm (mean, 1.0 cm). The use of helical dynamic CT enabled detection of 15 of 21 hepatocellular carcinomas (sensitivity, 71%) and nine of 23 dysplastic nodules (sensitivity, 39%). Patient sensitivity and specificity in the detection of hepatocellular carcinomas were 80% (12/15) and 96% (25/26), respectively, and for dysplastic nodules, 50% (5/10) and 97% (30/31), respectively.
CONCLUSION. Three-phase helical dynamic CT is relatively insensitive for detection of hepatocellular carcinomas and dysplastic nodules in cirrhotic livers, especially for dysplastic nodules and hepatocellular carcinomas smaller than 2 cm.
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Multiphasic dynamic CT using a helical scanner has become the standard CT technique for the detection and characterization of nodular lesions in cirrhotic liver parenchyma [1, 5,6,7]. To our knowledge, only one study has investigated the true sensitivity and specificity of helical dynamic CT in cirrhotic patients before transplantation, and this group of patients was small [8]. Furthermore, to our knowledge, no study has been reported regarding the true detectability of dysplastic nodules in cirrhotic patients. Using the three-phase helical dynamic CT and comparing the findings with the explanted liver as the gold standard, we undertook this study to evaluate the true sensitivity and specificity of helical CT for the detection of hepatocellular carcinomas and dysplastic nodules in cirrhotic patients. To our knowledge, this is the first prospective study to assess the efficacy of helical dynamic CT in the detection of hepatocellular carcinomas and dysplastic nodules in a large number of patients.
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Three-phase helical CT was performed in all 41 patients using a helical CT scanner (HiSpeed Advantage; General Electric Medical Systems, Milwaukee, WI). The scans were obtained through the liver in a craniocaudal direction with 7-mm collimation; 7-mm/sec table speed (pitch, 1.0) during a single breath-hold helical acquisition of 25-30 sec, depending on the size of the liver; and a 7-mm reconstruction interval. For the three-phase CT, the hepatic arterial, portal venous, and delayed phases were scanned 30 sec, 60 sec, and 180 sec, respectively, after the start of the injection of 120 mL of nonionic iodinated contrast material, iopamidol (Iopamiro 300; Bracco, Milano, Italy), via the antecubital vein at a rate of 3 mL/sec by power injector.
Pretransplantation three-phase CT scans were prospectively and independently interpreted. All scans were read by at least two investigators (combination of fellows and staff radiologists for a total of eight), and a consensus was reached in all cases. All nodular lesions, either with high or low attenuation not explainable by normal structures and different from attenuation of the normal liver parenchyma, were interpreted as potentially hepatocellular carcinoma or dysplastic nodule. Small wedge-shaped hyperenhancing lesions at the periphery of the liver at the arterial phase were regarded as pseudolesions [9] and excluded from the category of hepatic nodules. The number, size, and location of nodular lesions were recorded. The CT criteria for the diagnosis of hepatocellular carcinoma at initial interpretation before transplantation were a nodule showing the enhancement pattern of the hepatic arterial supply and lack of the portal venous supply [10] (e.g., hyperattenuation or isoattenuation at hepatic arterial phase and lower attenuation or isoattenuation at portal venous phase and delayed phase compared with the adjacent parenchyma). Typical patterns included nodules of high attenuation at hepatic arterial phase and low attenuation at portal venous and delayed phases; nodules of high attenuation at hepatic arterial phase, isoattenuation at portal venous phase, and low attenuation at delayed phase; and nodules of high attenuation at hepatic arterial phase and isoattenuation at portal venous and delayed phases. In addition, the following helical CT findings were regarded as being hepatocellular carcinoma: a nodule of mixed attenuation with areas of low attenuation at hepatic arterial, portal venous, and delayed phases; a nodule with discrete capsular enhancement at delayed phase; and a nodule larger than 1 cm that showed predominantly low attenuation at all three phases. The helical CT criteria for the diagnosis of dysplastic nodule were either a nodule smaller than 1 cm in diameter showing low attenuation during all three phases of helical CT or a nodule only seen at delayed phase as low attenuation [10]. The results of other imaging studies such as sonography, angiography, or MR imaging were not taken into consideration in the CT interpretation.
Explanted livers were serially sectioned in the transverse or coronal plane at 5- to 10-mm intervals (mean, 7 mm). Section of the explanted liver was independently performed without information of CT findings. The explanted liver specimens were examined in the fresh state immediately after surgery as well as in the preserved state in formalin. All visible nodules on the gross specimens were recorded and examined microscopically. The size, numbers, and location of all hepatocellular carcinomas and dysplastic nodules in the liver specimens were recorded. All nodular lesions seen at three-phase CT were compared on a one-by-one basis with corresponding hepatocellular carcinomas and dysplastic nodules in the explanted liver specimens in terms of location, size, and numbers. For statistical analysis, CT diagnosis was considered correct if the mass identified on dynamic CT corresponded anatomically to the pathologic specimens. In patients with multiple nodules, including hepatocellular carcinomas and dysplastic nodules, all the lesions were recorded for calculation of sensitivity and specificity.
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Pretransplantation dynamic helical three-phase CT revealed 15 of 21 hepatocellular carcinomas (sensitivity, 71%). Six (60%) of 10 hepatocellular carcinomas smaller than 2 cm and nine (82%) of 11 hepatocellular carcinomas ranging from 2.0 to 5.0 cm were detected (Fig. 1A,1B,1C,1D). In one patient, a nodule on CT was diagnosed as a hepatocellular carcinoma but was later confirmed to be a dysplastic nodule at pathologic examination. In another patient, CT depicted two hepatocellular carcinomas but the explanted liver disclosed four hepatocellular carcinomas. One nodule on the CT scan was hepatocellular carcinoma but the other nodule on CT was not present in the explanted liver (Fig. 2A,2B,2C,2D,2E). Therefore, in this patient, only one of four hepatocellular carcinomas was detected on CT, and the other one nodule revealed on CT was considered to be a small arterioportal shunt. In three other patients, whose CT scans did not detect hepatocellular carcinoma, the explanted livers were found to contain one hepatocellular carcinoma each. Patient sensitivity and specificity for hepatocellular carcinoma were 80% (12/15) and 96% (25/26), respectively.
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Dysplastic Nodules
At pathologic analysis, 23 dysplastic nodules were identified in 10
patients. Of these 10 patients, four had one dysplastic nodule each and six
had one to five dysplastic nodules. The diameter of the nodules ranged from
0.7 to 2.0 cm (mean, 1.0 cm). Pretransplantation helical dynamic three-phase
CT detected nine of 23 dysplastic nodules, with a sensitivity of 39%. In one
patient, three nodules diagnosed as dysplastic nodules on CT were not present
at pathologic examination. In five patients, CT did not depict any dysplastic
nodules but 11 dysplastic nodules were found in the explanted livers (Fig.
2A,2B,2C,2D,2E).
Patient sensitivity and specificity for dysplastic nodules were 50% (5/10) and
97% (30/31), respectively.
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The elapsed time between CT examination and transplantation was 50-100 days (mean, 75 days), and a few hepatocellular carcinomas or dysplastic nodules might have developed during this period. Although the rate of development of hepatocellular carcinoma per year in cirrhotic patients was reported as 5.3-8.8% [12], to our knowledge, no data have been reported regarding the cumulative incidence in a relatively short period.
Detection of hepatocellular carcinoma and hepatocytic nodules such as dysplastic nodules is difficult because the cirrhotic liver parenchyma contains fibrosis, regenerative nodules, fatty infiltration, and parenchymal necrosis [2]. Thus, the appearance of the liver is dramatically altered on imaging studies such as sonography, CT, and MR imaging. Furthermore, nontumoral small arterioportal shunts presenting as pseudonodules complicate the interpretation of CT [9], MR imaging, hepatic angiography, CT during arterial portography [13], and CT during hepatic arteriography. There have been several reports on the ability of CT in screening for hepatocellular carcinoma in patients with cirrhosis [1, 5,6,7, 12, 14,15,16]. Takayasu et al. [17] reported a detection rate of 84% in 100 patients (including 76 patients with chronic liver disease) using CT, showing relatively high sensitivity and specificity. However, all of these studies were limited by retrospective reviews, and the diagnosis was made by imaging studies, clinical findings, or both. Even with the histologically confirmed cases of hepatocellular carcinoma, pathologic correlation was incomplete because the pathology was based on the partial resection of the liver or imaging-guided biopsy.
On the basis of explanted livers, Miller et al. [2] reported that the true sensitivities of unenhanced and enhanced CT in the detection of malignancy were 63% and 68%, respectively, and specificities were 63% and 81%, respectively. They emphasized the value of unenhanced CT because some of the tumors were visible only on unenhanced CT, although the enhanced CT generally had a higher sensitivity and specificity. In other studies, the accuracy of conventional CT in the detection of hepatocellular carcinoma in patients with orthotopic liver transplantation has been reported to be 45-58% [3, 4]. Iodized oil CT has been known to be the most sensitive CT technique in the detection of small hepatocellular carcinomas. However, the reported accuracy in transplantation patients after a one-to-one radiologic-pathologic analysis was relatively low, ranging from 50% to 58% [18,19,20]. The high sensitivity of iodized oil CT in some other reports is probably because of a lack of pathologic correlation [21,22,23,24].
Because the detectability of hepatic nodular lesions on CT depends on the attenuation difference between the normal parenchyma and nodular lesions, the presence of cellularity, fibrosis, fatty change, necrosis, peliosis, and vascularity of nodules affect the sensitivity of detection. Multiphasic CT makes use of the dynamic change including different contrast material enhancement patterns of the nodular lesions and surrounding parenchyma [25]. This may in part be a result of the difference in uptake and secretion of iodinated contrast material by hepatocytes of the normal liver parenchyma and tumor cells of hepatocellular carcinoma [14]. In addition, the number of vascular channels and their hemodynamics might well affect the attenuation of normal parenchyma and tumor. These differences in enhancement patterns can be visualized on CT by acquiring multiple scans during a relatively short time after contrast material injection. Helical CT is able to acquire data in 20 sec, finish a dynamic CT of the whole liver in a single breath-hold, and permit examination during the hepatic arterial, portal venous, and delayed phases. Arterial phase CT proved to be the most useful in the detection of hypervascular tumors such as hepatocellular carcinoma, whereas CT during the portal venous and delayed phases proved to be useful in the detection of less vascularized tumors such as well-differentiated or early hepatocellular carcinoma.
One paper has assessed the accuracy of helical dynamic CT (two phases) in patients with orthotopic liver transplants [8]. According to this study, the sensitivity for detection of hepatocellular carcinoma was 76%; for hepatocellular carcinomas with a diameter of 0.5-1.0 cm, 20%; 1.1-2.0 cm, 82%; 2.1-3.0 cm, 86%; and larger than 3.0 cm, 100%. Our investigation yielded similar results for the detection of hepatocellular carcinomas. Patient sensitivity was 80% (12/15) and individual lesion sensitivity was 71% (15/21). For dysplastic nodules, patient sensitivity was 50% (5/10) and individual lesion sensitivity was 39% (9/23). As might be expected, the hepatocellular carcinomas and dysplastic nodules that were not detected tended to be smaller. The detection rate for hepatocellular carcinomas smaller than 2 cm was 60% and those larger than 2 cm was 82%. The detection rate for dysplastic nodules smaller than 2 cm was 39%. Our detection rates for hepatocellular carcinoma are slightly better than those of Miller et al. [2], who yielded a patient sensitivity of 68% and lesion sensitivity of 54% using the conventional CT scanner. Comparison of the two studies appears to indicate that helical dynamic CT is slightly more sensitive than conventional CT in the detection of hepatocellular carcinomas in patients with liver cirrhosis.
Dysplastic nodules refer to nodules 1 mm or larger that have dysplasia but lack definite histology of malignancy. Histologically, the cell density is moderately increased in comparison with the surrounding liver; however, no evident structural abnormality is present [26]. Dysplastic nodules can be further characterized as low-grade or high grade to denote the degree of atypia [27, 28]. Sakamoto et al. [29] proposed the development of hepatocellular carcinoma from a regenerative nodule to a low-grade dysplastic nodule, then to a high-grade dysplastic nodule, and subsequently into well-differentiated hepatocellular carcinoma and overt hepatocellular carcinoma in a multistep fashion or in a continuous transition. Therefore, dysplastic nodules have been considered premalignant lesions. Most dysplastic nodules without malignant foci are 1.0-1.2 cm in diameter [30, 31].
Several reports have described the detectability of dysplastic nodules on dynamic CT scans. Dysplastic nodules may present as hyperattenuating, hypoattenuating, or isoattenuating lesions, depending on the vascular phases of dynamic CT scans. According to Cho et al. [32], the detectability of dysplastic nodules on dynamic helical CT was 38%; most of the lesions were not visualized because they were isoattenuating. Some low-attenuation dysplastic nodules were present on portal venous phase and delayed phase scans, and a few dysplastic nodules showed high attenuation on hepatic arterial phase scans. Hemodynamic characteristics of dysplastic nodules on CT during arterial portography and on CT during hepatic arteriography have been reported. Lim et al. [33] suggested that 66% of dysplastic nodules were isoattenuating; therefore, these were not detected on CT during arterial portography and on CT during hepatic arteriography. Hayashi et al. [34] reported that 77% of low-grade dysplastic nodules were isoattenuating on CT during arterial portography and 69% of low-grade dysplastic nodules were isoattenuating on CT during hepatic arteriography, whereas 32% of high-grade dysplastic nodules were isoattenuating both on CT during arterial portography and CT during hepatic arteriography. These reports suggest that the reason why many dysplastic nodules are isoattenuating to the adjacent liver parenchyma on CT is that the blood supply to these nodules is similar to that of the surrounding liver parenchyma.
The policy for liver transplantation has been changed over the past few years. Initially, detection of hepatocellular carcinoma in a candidate was a contraindication. As transplantation techniques have been improved, exclusion criteria have become narrower and patients with hepatocellular carcinoma now undergo transplantation. In our institution, patients with a single hepatocellular carcinoma no larger than 5 cm or with as many as three hepatocellular carcinomas smaller than 3 cm each may undergo transplantation. Even with this policy, detection of hepatocellular carcinoma is important in the management and timing of transplantation; in those candidates with hepatocellular carcinoma, tumor growth may be inhibited with delaying procedures such as ethanol injection, thermal ablation, microwave ablation, or transarterial chemoembolization.
Although multiphasic helical dynamic CT is slightly superior to conventional CT for the detection of hepatocellular carcinomas and dysplastic nodules in patients with cirrhosis, our results showed that it is still not satisfactory in detecting small hepatocellular carcinoma. CT during arterial portography and CT during hepatic arteriography have been known to be the most sensitive methods in the detection of hepatic tumors, but these studies proved to have many false-positive results [35, 36]. In a comparison study of helical dynamic CT versus combined CT arterial portography and CT during hepatic arteriography by Jang et al. [33], a considerable number of nodular pseudolesions were found to mimic hepatocellular carcinoma on CT during arterial portography and on CT during hepatic arteriography; thus, three-phase helical dynamic CT showed comparable sensitivity and superior positive predictive value. Comparative studies between helical dynamic CT and dynamic MR imaging in patients undergoing liver transplantation are underway.
Acknowledgments
We thank Young Joo Moon for her assistance in manuscript preparation and
Sam Chun for his editorial assistance.
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1.5 cm) malignant hepatic neoplasm.
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