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First published online April 26, 2006
British Journal of Radiology (2006) 79, 659-665
© 2006 British Institute of Radiology
doi: 10.1259/bjr/12699987
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Imaging well-differentiated hepatocellular carcinoma with dynamic triple-phase helical computed tomography

C-S Li1,3, R-C Chen1,3,4, H-Y Tu1, L-S Shih2, T-A Zhang2, J-M Lii1, W-T Chen1, S-J Duh1 and L-C Chiang1

Departments of 1Radiology 2Pathology, Renai Branch, Taipei City Hospital, Taipei 3Department of Radiology, School of Medicine, National Yang-Ming University, Taipei and 4Department of Radiology, School of Medicine, Taipei Medical University, Taipei, Taiwan


   Abstract
Top
 Abstract
Introduction
 Materials and methods
 Results
 Discussion
 Conclusion
 References
 
To investigate the imaging appearance of well-differentiated hepatocellular carcinoma (HCC) on dynamic CT, a total of 38 histopathologically proven well-differentiated HCC were included in a retrospective study. We reviewed the contrast-enhanced dynamic CT of all 38 tumours for attenuation of each tumour in unenhanced scan, arterial-dominant and delayed portal venous phases. Our results showed that dynamic CT identified 26 (68.4%) out of the 38 lesions. The remaining 12 lesions were isodense compared with surrounding liver parenchyma in each dynamic CT phase. There was no statistically significant difference between the mean size of tumours detected by dynamic CT and that of tumours not detected by dynamic CT (p = 0.1). Of a total of 38 tumours, most were isodense (n = 19) or hypodense (n = 16) in unenhanced scan, mostly hyperdense (n = 18) or isodense (n = 15) in arterial-dominant phase and mostly isodense (n = 22) or hypodense (n = 15) in delayed portal venous phase. Enhancement of tumour was observed in 19 (50.0%) of 38 lesions. In conclusion, the ability of dynamic CT to detect well-differentiated HCC is poor, and negative CT findings cannot exclude the presence of well-differentiated HCC, especially if there is well-grounded clinical suspicion for HCC.


   Introduction
Top
 Abstract
 Introduction
Materials and methods
 Results
 Discussion
 Conclusion
 References
 
Hepatocellular carcinoma (HCC) is one of the most common malignancies in the world. Globally, there is an increasing incidence of HCC in both eastern and western countries [1, 2]. HCC usually develops in the setting of chronic liver disease and cirrhosis [3]. Screening with ultrasound and {alpha}-fetoprotein levels to detect HCC in patients with chronic liver disease has become common practice [4, 5]. Consequently, an increasing number of nodular hepatic lesions has been detected on screening ultrasound. It is important to distinguish well-differentiated HCC, an early form of HCC in hepatocarcinogenesis, from dysplastic hepatic nodule [3, 6]. Treatment should be applied at this stage with local ablation therapy, surgical resection or transplantation [7]. The biological behaviour of well-differentiated HCC is uncertain, but it is thought to have relatively low malignant potential and rarely invade vessels or metastasise to other sites [8, 9].

When hepatic nodules are identified on ultrasound, CT or MRI is usually used for further characterization because ultrasound appearance of a hepatic nodule may be non-specific [10]. However, imaging characteristics of well-differentiated HCCs have been described in only a few papers in the English literature [11–15]. In this retrospective study, we would like to investigate the imaging appearance of well-differentiated HCC on dynamic dual-phase helical CT.


   Materials and methods
Top
 Abstract
 Introduction
 Materials and methods
Results
 Discussion
 Conclusion
 References
 
Patients
From January 2000 to July 2004, we retrospectively reviewed the histopathological reports of ultrasound-guided liver tumour biopsy in our hospital. A total of 68 patients with 71 well-differentiated HCCs were identified. All patients received abdominal ultrasound for screening of HCC or follow-up after treatment for HCC. Among this group, 37 patients with 38 well-differentiated HCCs were referred for dynamic CT scan because of hepatic nodules detected on abdominal ultrasound, and they were included in our study. They comprised 25 men and 12 women, with ages ranging from 31 years to 82 years (mean age 59.8 years). All patients suffered from chronic liver disease including hepatitis B in 22 patients, hepatitis C in 12 patients, alcoholic liver disease in 1 patient and cryptogenic liver cirrhosis in 2 patients. The dynamic CT images of each patient were reviewed. Written informed consent was obtained from each patient.

All 37 patients underwent ultrasound-guided biopsy of hepatic nodules before or soon after (within 1 month) CT scan. All biopsies were performed with a 3.5 MHz guiding probe with a Logiq 400 unit (GE pro series). The biopsy needle was either a 1.2 mm Surecut needle (Top Surgical Manufacturing, Tokyo, Japan) or a 0.8 mm Majima needle (Top Surgical Manufacturing, Tokyo, Japan).

The needle biopsy specimens were fixed in formalin immediately and processed according to standard procedures in the department of pathology. Both haematoxylin and eosin (H&E) and reticulin stains were routinely performed on each case. The specimens were interpreted by one of the two authors (LSS and TAZ); both of them were experienced pathologists in the diagnosis of differentiation of HCC. The histopathological criteria of well-differentiated HCC included: (1) increased cell density (more than 1.8 times non-neoplastic hepatic tissue of the same patient); (2) increased nuclear/cytoplasmic ratio of individual tumour cells; and (3) disorganized reticulin framework with irregular thin-trabecular pattern [16]. In most cases, the cancer cells of well-differentiated hepatocellular carcinoma were smaller in size with increased cytoplasmic eosinophilia. In addition, fatty changes of tumour tissue were occasionally observed [17]. Correlation between imaging characteristics and histopathological evidence of fatty change and vascular density was not a focus of our study, because the histopathological diagnosis in our study was based on liver biopsy.

Image acquisition
Hepatic CT scan was performed with a helical CT scanner (HiSpeed Advantage; General Electric Medical Systems, Milwaukee, WI). All patients received oral contrast material before the CT examination. The unenhanced scans of entire liver were performed with slice thickness of 7 mm and space of 10 mm. The enhanced CT scans were then performed by intravenous injection of 100–120 ml iopromide (Ultravist 370; Schering, Berlin, Germany), depending on patients' body weight. A mechanical power injector was used. The rate of injection was 2.5–3.5 ml s–1 depending on accessibility to patients' peripheral veins. The length of delay between intravenous contrast material administration and scanning was 30–35 s for the arterial-dominant phase, according to cardiac function estimated by patient's age and general medical condition. The delayed portal venous phase was obtained at 110 s after contrast material administration. The delayed portal venous phase, in-between the usual portal venous phase and delayed phase, was the standard dynamic CT protocol for evaluation of nodular liver lesions in our institution. The dual-phase enhanced CT scan was performed with a slice thickness of 7 mm and a pitch of 1.2:1. Images acquired during each phase of contrast were obtained using a breath-hold technique and required two split acquisitions to cover the entire liver. For most cases, a total of 15 slices were obtained in each acquisition and there was a 6 s interval between the two acquisitions.

Image interpretation
The ultrasound features of each patient in this study were carefully correlated with the CT scan findings in respect of tumour location. The tumour sizes were determined by the maximal diameter of each tumour on the basis of ultrasound. The attenuations of these lesions in unenhanced scan, arterial-dominant phase and delayed portal venous phase of dynamic CT scan were independently analysed by two experienced radiologists specialized in liver imaging. The attenuations of these lesions were compared with surrounding liver and were categorized as hyperdense (or high-density), isodense (or iso-density) and hypodense (or low-density) by visual inspection. Identification of extremely low attenuation representing the fat component within these lesions was also noted. Positive enhancement of tumour was defined as when a hypodense tumour in unenhanced scan becomes isodense or hyperdense in arterial-dominant phase, or when an isodense tumour in unenhanced scan turns hyperdense in arterial-dominant phase. The window levels of images were kept constant during interpretation. Disagreements of images interpretation were resolved by consensus.

Statistical analysis
All 38 tumours in the study were subdivided into two groups, one that could be visualized by CT scan and another group that could not. The size of tumour in each group was expressed as mean ± standard error (SE). Comparison of sizes between different groups was performed using the Student's t-test. A threshold p-value of 0.05 was chosen for statistical significance.


   Results
Top
 Abstract
 Introduction
 Materials and methods
 Results
Discussion
 Conclusion
 References
 
The sizes of these 38 well-differentiated HCCs detected by ultrasound ranged from 0.5 cm to 2.7 cm (mean: 1.7±0.6 cm). 27 (71.1%) out of 38 tumours were small HCCs with the sizes less than 2 cm. Dynamic CT scan depicted 26 (68.4%) out of the 38 nodules. The remaining 12 nodules were isodense in unenhanced, arterial-dominant and delayed portal venous phases of dynamic CT scan (we coded this as "iso-iso-iso" pattern) and, as a result, could not be identified (Figure 1Go).


Figure 1
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  		Figure 1. Images of a 1.1 cm-diameter well-differentiated hepatocellular carcinoma in segment IV of the liver in a 73-year-old man. (a) Abdominal ultrasound disclosed a hepatic tumour with high echogenicity (arrow). (b,c) The tumour was isodense to surrounding liver parenchyma in unenhanced (not shown), arterial-dominant phase (b) and portal venous phase (c) of dynamic CT and, as a result, could not be identified. (d) Photomicrograph of the needle biopsy specimen showed a well-differentiated hepatocellular carcinoma. Haematoxylin and eosin, original magnification x100.

 
The mean size of the 26 nodules detected by dynamic CT scan was 1.8±0.6 cm; and that of the remaining 12 nodules not identified by dynamic CT scan was 1.5 ±0.4 cm. There was no statistically significant difference in size between the two groups of nodules (p = 0.1). Besides that, there was no statistically significant difference in size between all 38 nodules and the group of 26 nodules that could be visualized by CT scan (p = 0.4), as well as the group of 12 nodules that could not be visualized by CT scan (p = 0.3).

In unenhanced CT scans, these 38 well-differentiated HCCs were mostly isodense (n = 19, 50.0%) or hypodense (n = 16, 42.1%); in arterial-dominant phase, they were mostly hyperdense (n = 18, 47.4%) or isodense (n = 15, 39.5%); in delayed portal venous phase, they were mostly isodense (n = 22, 57.9%) or hypodense (n = 15, 39.5%) (Table 1). Positive enhancement in arterial-dominant phase was observed in 19 (50.0%) of 38 tumours (Figure 2Go). One of the lesions was hypodense and enhanced to be isodense on the arterial-dominant phase images. All of the 19 tumours demonstrated washout of enhancement in delayed portal venous phase.


Figure 2
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  		Figure 2. Dynamic CT images of a 1.5 cm-diameter well-differentiated HCC in segment II of the liver in a 43-year-old man. (a) The tumour was hypodense in unenhanced scan (arrow), (b) hyperdense in arterial-dominant phase (arrow) and (c) isodense in portal venous phase. (d) Photomicrograph of the needle biopsy specimen with reticulin stain showed a disorganized reticulin framework with irregular thin-trabecular pattern. Original magnification x100.

 
In our study, the most common appearance of well-differentiated HCC in each phase of dynamic CT was the "iso-iso-iso" pattern (n = 12, 31.6%). These tumours could not be identified on dynamic CT. The other well-differentiated HCC in our study presented varying imaging appearances, and common patterns included: a "low-high-low" pattern (n = 7, 18.4%) (Figure 3Go), an "iso-high-iso" pattern (n = 5, 13.2%), a "low-high-iso" pattern (n = 4, 10.5%), and a "low-low-low" pattern (n = 4, 10.5%).


Figure 3
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  		Figure 3. Dynamic CT images of a 2.1 cm-diameter well-differentiated HCC in segment III of the liver in a 54-year-old man. (a) The tumour was hypodense in unenhanced scan (arrow). (b) Positive enhancement of the tumour was demonstrated in arterial-dominant phase (arrow). (c) In portal venous phase, the tumour was again hypodense (arrow), representing the "low-high-low" pattern on dynamic CT scan.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
Conclusion
 References
 
Early detection of HCC is becoming feasible owing to the wide use of ultrasound for screening [18]. High rates of ultrasound detection for small HCCs, ranging from 89% to 98.6%, have been reported [19, 20]. However, the differentiation of a hepatic nodule between early malignant tumour and pre-malignant nodule is often difficult. The distinction between well-differentiated HCC and dysplastic nodule is clinically important because of the difference in their management [10]. Therefore, advanced imaging modalities such as CT and MRI play an important role in characterizing these hepatic nodules in a non-invasive fashion.

The appearance of well-differentiated HCC on CT scan has been studied before, but these prior studies either had too small a case number of well-differentiated HCCs or were lacking in dynamic CT protocols [5, 13, 14, 21]. Takayasu et al reported a poor detection rate of 56% for well-differentiated HCC, which was based on mixed table incremental CT and helical CT protocols [5]. Our study presented a 68.4% detection rate on the basis of dynamic helical CT protocol. The detection rate in our study was still low. Our study revealed that the mean size of well-differentiated HCC undetected by dynamic CT was not statistically different from tumours detected by dynamic CT. The reason behind the low detection rate was that well-differentiated HCC was commonly isodense in unenhanced, arterial-dominant and delayed portal venous phases of dynamic CT scan.

Only half of our cases showed tumour enhancement in arterial-dominant phase of dynamic CT scan, which means the other half were hypovascular hepatocellular carcinoma. Well-differentiated HCC had less neoplastic angiogenesis and incomplete vascularization of the sinusoid-like blood spaces of the tumour, and therefore frequently presented as a hypovascular tumour [22–25]. In contrast, most moderately- and poorly-differentiated HCCs present as hypervascular lesions, and are easier to detect on dynamic CT [21].

Choi et al considered that combination of arterial and portal venous phases on dynamic CT was enough for detecting HCC, and delayed phase images could be omitted to decrease scanning time and radiation hazard [26]. However, other authors suggested that delayed phase CT images were important in detecting early or hypovascular hepatocellular carcinoma [5, 27, 28]. The CT protocols used in these studies were composed of arterial-dominant phase of 30–35 s, portal venous phase of 60 s and delayed phase of 180 s after commencing intravenous contrast medium administration [27, 28]. In our institution, we used arterial-dominant phase to detect hypervascular lesions, followed by delayed portal venous phase at 110 s after contrast medium administration. The purpose of our dual-phase CT protocol was to avoid excessive radiation exposure of triple-phase CT; and our study showed that the CT protocol could offer a comparable (68.4%) detection rate for well-differentiated HCC. According to the results of our study, roughly half of well-differentiated HCCs are hypovascular; we hypothesized that dynamic CT scan with additional delayed-phase images might increase the detection rate of well-differentiated HCC. However, the hazard of increased radiation exposure should also be a concern. Further study with the triple-phase dynamic CT protocol to detect well-differentiated HCCs may be needed.

It is clinically important to distinguish pre-malignant hepatic dysplastic nodules from well-differentiated HCCs. However, our study showed some overlapping dynamic CT appearances between the well-differentiated HCCs and hepatic dysplastic nodules. Choi et al had reported that hepatic dysplastic nodules were mostly isodense or hypodense in arterial-phase and portal-phase CT images; most of them were relatively avascular [7]. Compared with radiographic features demonstrated in our study, high density or positive enhancement of a small hepatic nodule in arterial-dominant phase of dynamic CT could be an important feature pointing to the diagnosis of a HCC rather than a pre-malignant dysplastic nodule. However, in the appropriate clinical settings (chronic B or C viral hepatitis, elevation of serum {alpha}-fetoprotein level, positive ultrasound findings), negative CT finding may not be sufficient to exclude a well-differentiated HCC. Further imaging study or biopsy should be considered in such situations.

Lee et al reported a 96% arterial-phase enhancement rate of HCC, using triple-phase multidetector CT (MDCT) as well as rapid injection of contrast material at 5 ml s–1 [29]. However, only a small number of well-differentiated HCCs were presented in their study. MDCT, with its rapid scanning time, should have better detection ability than single-detector scanner; but the role of MDCT in diagnosis of well-differentiated HCC still needs further investigation.

Dynamic gadolinium-enhanced MRI has been considered the method of choice for HCC diagnosis [30–32]. In cirrhotic patients, dynamic gadolinium-enhanced MRI is also a useful modality for detection and characterization of regenerative or dysplastic nodules [33]. Through its superior tissue contrast, MRI might detect more well-differentiated HCCs based on signal intensity change on pre-contrast T1 weighted or T2 weighted images than CT [11, 13, 34]. Amano et al studied the CT and MRI patterns of HCC and concluded that they were useful in predicting the degree of histological differentiation of cancer cells in HCC [35]. However, no specific CT patterns or MR signals can offer accurate diagnosis of well-differentiated HCC, and absence of arterial phase enhancement cannot exclude the possibility of early or "borderline" malignancy [32]. In recent years, superparamagnetic iron oxide (SPIO)-enhanced MRI has been reported as useful for the detection of hepatic tumours [36, 37]. SPIO-enhanced MRI provided a fundamentally different approach for HCC diagnosis: SPIO would be taken up by Kupffer cells in normal liver parenchyma, but not in hepatic tumours which generally lacked reticulo-endothelial cells. However, the diagnosis of well-differentiated HCC could still be problematic because well-differentiated HCC may contain Kupffer cells as in normal liver parenchyma. Consequently, it may show similar SPIO uptake comparable with surrounding normal liver parenchyma and would be poorly delineated on SPIO-enhanced MRI [30, 38, 39]. Contrast-enhanced MRI could be a better imaging modality for diagnosis of well-differentiated HCC than CT, but further investigation would be needed to achieve better sensitivity and specificity.

We recognized two limitations in our study. First, this is a retrospective study in which there might be case selection bias, with respect to referral and patients undergone CT scanning. Second, there is a limitation in the correlation between CT appearances and histopathological findings in our study. All of our cases only had needle biopsy specimen for histopathological diagnosis, and underwent percutaneous ethanol injection therapy (PEIT) or transcatheter arterial chemoembolisation (TACE) for subsequent treatment. HCC may have different grades of differentiation within the tumour and the biopsy sample may not be representative of the whole tumour. In a study from Japan [24], about 20% of small HCCs (less than 2 cm in diameter) of the distinctly nodular type were composed of varying mixtures of well-differentiated and moderately-differentiated cancerous tissues. Needle biopsy of a tumour cannot fully reflect the differentiation of HCC. Better imaging-pathology correlation could be obtained if we were able to examine the entire tumours.


   Conclusion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Conclusion
References
 
In conclusion, the detecting ability of dynamic dual-phase helical CT for well-differentiated HCC is low. This type of tumour is frequently isodense to surrounding liver parenchyma in unenhanced, arterial-dominant or portal venous phase of CT scan, and positive enhancement is seen only in 50% of them. It is difficult to diagnose well-differentiated HCCs based solely on the density changes on CT scans. Hepatic nodules with high density or positive enhancement in arterial-dominant phase of dynamic CT scans suggest a diagnosis of a HCC rather than a hepatic dysplastic nodule in cirrhotic liver. However, in the appropriate clinical settings, a negative CT scan cannot be relied upon in exclusion of well-differentiated HCCs. Further imaging study, including contrast enhanced-MDCT or MRI, and liver biopsy should be considered in this situation.

Received for publication November 7, 2005. Revision received January 26, 2006. Accepted for publication February 13, 2006.


   References
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Conclusion
 References
 

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