DOI:10.2214/AJR.07.2040
AJR 2007; 189:792-798
© American Roentgen Ray Society
Role of MDCT in the Diagnosis of Hepatocellular Carcinoma in Patients with Cirrhosis Undergoing Orthotopic Liver Transplantation
Annalisa Ronzoni1,2,
Diana Artioli2,
Rosa Scardina3,
Luca Battistig4,
Ernesto Minola5,
Sandro Sironi1,6 and
Angelo Vanzulli2
1 School of Medicine, University of Milano-Bicocca, Milan, Italy.
2 Department of Diagnostic Radiology, A. O. Niguarda Ca Granda, Piazza Ospedale
Maggiore, Milan 20162, Italy.
3 Department of Diagnostic Radiology, A. O. Vimercate, Milan, Italy.
4 Department of Diagnostic Radiology, Policlinico di Monza, Milan, Italy.
5 Department of Pathology, A. O. Niguarda Ca Granda, Milan, Italy.
6 Department of Diagnostic Radiology, A. O. S. Gerardo Monza, Milan,
Italy.
Received February 12, 2007;
accepted after revision May 20, 2007.
Address correspondence to A. Ronzoni.
Abstract
OBJECTIVE. The purpose of this study was to assess the diagnostic
performance of MDCT in the detection of hepatocellular carcinoma in patients
with cirrhosis undergoing orthotopic liver transplantation.
MATERIALS AND METHODS. Eighty-eight consecutively registered
patients who underwent MDCT 6 months before liver transplantation were
evaluated. The original reports were analyzed, and the CT images were
retrospectively reevaluated independently by two radiologists who made the
final interpretation in consensus. The imaging findings were correlated with
histopathologic findings in the explanted livers on a patient-by-patient and a
lesion-by-lesion basis.
RESULTS. Histopathologic examination revealed 139 hepatocellular
carcinomas in 48 of the 88 patients. MDCT correctly depicted 89 of 139
hepatocellular carcinomas (sensitivity, 64%) at the original examination and
102 at reevaluation (sensitivity, 73.3%). Patient-by-patient analysis showed a
specificity of 75% in the original reports and of 77.5% at reevaluation. A
large number of false-positive nodules were found, most (59.2%) of them being
smaller than 1 cm in diameter.
CONCLUSION. MDCT has reasonable sensitivity in the detection of
hepatocellular carcinoma in patients with cirrhosis who undergo liver
transplantation. Attention should be paid, however, to avoiding overestimation
of the extent of disease.
Keywords: explanted liver • hepatocellular carcinoma • MDCT
Introduction
Hepatocellular carcinoma (HCC) is the most frequent malignant neoplasm of
the liver in adults and is the leading cause of death among persons with
cirrhosis [1,
2]. The increasing incidence of
HCC is related to the longer survival of patients with cirrhosis as the result
of improved therapies [3]. HCC
in the early stages is clinically silent, but long-term survival can be
achieved only through early surgical or ablative treatment. Imaging is
important for early detection of malignant lesions
[4]. Orthotopic liver
transplantation in the care of patients with end-stage cirrhosis and HCC
improves long-term survival. Liver transplantation can be performed on
patients with one HCC 5 cm or less in diameter or up to three nodules 3 cm or
smaller
[5–8].
Imaging is thus involved in patient inclusion or exclusion from
transplantation lists. The imaging techniques used are sonography, CT, and
MRI. Sonography has wide ranges of sensitivity and specificity in the
detection of HCC in cirrhotic livers, which probably reflects operator skill
and experience, the technical performance of sonographic equipment, and
disease stage [9]. Abdominal
MRI has good sensitivity but lower specificity than CT in the detection of de
novo HCC nodules [9]. To our
knowledge, no study has been conducted with a liver-targeted MDCT protocol to
compare CT results with the findings in whole explanted livers. The purpose of
this retrospective study was to determine the diagnostic performance of MDCT
in the detection of HCC by comparing imaging findings with histologic findings
in explanted cirrhotic livers.
Materials and Methods
Patients
We retrospectively evaluated the cases of 88 consecutively registered
patients (70 men, 18 women; mean age, 51.3 years; range, 31–65 years)
who underwent liver transplantation between January 2003 and April 2006 and
were examined with MDCT within 6 months before transplantation (mean time
interval, 79.5 days; range, 1–179 days). The underlying indication for
hepatic transplantation was cirrhosis due to hepatitis C (n = 31) or
hepatitis B or D (n = 17), alcohol abuse (n = 6), combined
alcoholic and viral cirrhosis (n = 4), and other, less common
diseases such as cryptogenic cirrhosis (n =4), primary biliary
cholangitis (n = 2), secondary biliary cholangitis (n = 1),
primary sclerosing cholangitis (n = 1), Wilson's disease (n
= 1), and autoimmune hepatitis (n = 1). The cause of cirrhosis was
not obtained in 20 cases. Fifty of 88 patients had undergone therapy for HCC
(surgical resection, radiofrequency, or chemoembolization). Because the study
was retrospective, neither informed consent nor institutional review board
approval was required.
Imaging Technique
All CT studies were performed with an MDCT scanner (Brilliance, Philips
Medical Systems) according to a dedicated multiphase protocol (collimation,
1.5 mm; image reconstruction interval, 3 mm). Patients received 2 mL/kg of
iodinated contrast material (iomeprol, Iomeron 350, Bracco) injected IV at a
rate of 3.5–4 mL/s. Dynamic studies included acquisition of unenhanced
images followed by acquisition of enhanced images in the hepatic arterial,
portal venous, and delayed phases. Computer-assisted bolus-tracking software
was used to determine the optimal scan delay for each patient. Acquisition of
arterial phase images started 12 seconds after the automatic detection of
aortic peak enhancement (120 H). The portal and late venous phases started 55
and 120 seconds after aortic peak enhancement.
Image Analysis
Image analysis was divided into two parts. First, to assess the accuracy of
the imaging technique in routine practice, preoperative CT reports were
compared with histologic findings. Second, to assess the diagnostic potential
of the imaging technique, a retrospective unblinded review was undertaken by
two radiologists (each with 5 years of CT experience), who reached the
diagnosis by consensus. All scans were interpreted for the presence of HCC,
which was defined as an intensely enhancing nodule in the arterial phase
followed by a well-defined area of hypoattenuation relative to surrounding
liver parenchyma in the delayed phase (Fig.
1A,
1B,
1C). Even in absence of
arterial enhancement, well-defined washout in the delayed phase and a
hyperdense rim were considered diagnostic of HCC because a small percentage of
HCCs are hypovascular [10].
Each reviewer specified the total number of nodules detected per patient, the
size of the lesions, and the location of the lesions in liver segments.
Standard of Reference
In all cases, gross and histologic analyses of the explanted liver were
performed by an experienced liver pathologist. All explanted livers were fixed
in formalin and sectioned at 7- to 10-mm intervals in the transverse plane.
Each nodular lesion, that is, tissue different from the background cirrhotic
liver in morphologic features, color, or size, was fixed in formalin, embedded
in paraffin, and further sectioned for additional evaluation. Treated lesions
with complete necrosis at histologic examination were not counted as
nodules.
Statistical Analysis
CT sensitivity, specificity, positive predictive value (PPV), negative
predictive value (NPV), and accuracy of the preoperative diagnosis were
calculated with the histologic findings as the standard of reference.
Commercially available statistical software was used (SAS version 8.02, SAS
Institute). Concordance between CT and histologic findings was established on
a patient-by-patient and a nodule-by-nodule basis. The analyses were performed
both for the primary data subset and for the retrospective review. In a
further statistical analysis, histologic nodules were grouped into three
categories (small, 
10 mm in diameter; intermediate, 11–20 mm;
large, > 20 mm), and CT sensitivity was calculated for each group. Nodules
detected on CT were grouped into the same three categories (small,
intermediate, and large), and the PPV of MDCT was calculated.
Results
Findings at Histopathologic Analysis
Histologic examination revealed 139 hepatocellular carcinomas in 48 of the
88 patients who had undergone liver transplantation and no HCC in the other 40
patients. In 34 of the patients, HCC had a multifocal pattern. The mean nodule
diameter at histologic study was 17 ± 13 mm (range, 2–75 mm).
Sixty of the 139 nodules were small ( 10 mm; mean diameter, 8 mm), 42 were
of intermediate size (11–20 mm; mean diameter, 16 mm), and 37 were large
(> 20 mm; mean diameter, 34 mm).
Original Reports Versus Histopathologic Findings
MDCT depicted 133 HCC nodules in 37 patients. The results of
patient-by-patient and lesion-by-lesion analysis are reported in
Table 1, which shows the
sensitivity, specificity, PPV, NPV, and accuracy of MDCT. Most of the
false-negative lesions (32/50 [64%] in preoperative CT reports and 26/37 [70%]
at retrospective evaluation) were small. Among the false-negative lesions were
16 cases of undetected local recurrence previously treated with transcatheter
arterial chemoembolization (TACE) (n =10), radiofrequency ablation
(n = 2), or combined TACE and radiofrequency ablation (n
=4). Among the 44 false-positive lesions, 36 (82%) exhibited substantial
enhancement during arterial phase enhanced imaging. The other eight (18%) of
the false-positive lesions appeared hypoattenuating in relation to the liver.
According to the Milan criteria, the number of HCC nodules was overestimated
in 17 (19%) and underestimated in 22 (25%) of the 88 patients on prospective
preoperative MDCT. On the basis of CT results, transplantation would have been
precluded in the care of six (7%) of the 88 patients because of false-positive
results, and six of 88 patients incorrectly underwent liver transplantation on
the basis of false-negative results.
In analysis based on lesion diameter, the sensitivity of MDCT was
calculated for the three size groups of nodules detected at histologic
examination. The results are reported in
Table 2. For calculation of the
PPV of MDCT according to lesion diameter, the nodules detected on MDCT were
divided into three size categories: small, intermediate, and large. Of the 133
nodules detected on preoperative CT, 53 were small, 46 were of intermediate
size, and 34 were large (Table
2).
Retrospective Interpretation Versus Histopathologic Findings
MDCT depicted 129 HCC nodules in 40 patients. The results of
patient-by-patient and lesion-by-lesion analysis are reported in
Table 1, which shows the
sensitivity, specificity, PPV, NPV, and accuracy. Nine (8.9%) of the 102
true-positive nodules detected at retrospective review had an atypical
hypovascular pattern (Fig. 2A,
2B,
2C). At unblinded review, the
number of undetected local recurrences was similar to that (15 cases) in the
CT preoperative reports. An additional case of HCC recurrence was detected
after TACE, showing an intrinsic limitation of CT (Fig.
3A,
3B,
3C,
3D). Unblinded review of the
CT scans allowed better characterization of the lesions. A smaller number of
false-positive lesions were found among the total number of nodules detected:
44/133 versus 27/129. Twenty-six (96%) of the 27 false-positive lesions
detected at unblinded review were hypervascular, and one (4%) was
hypovascular. Thirteen of these 27 nodules were identified at gross and
histologic examination as regenerative (n = 12) or dysplastic nodules
(n = 1). False-positive nodules were further grouped according to
size. As shown in Table 3, most
of these nodules were small (Fig.
4A,
4B,
4C). At review of CT images,
the use of MDCT led to overestimation, according to the Milan criteria, of the
number of lesions in 15 (17%) and underestimation in 22 (25%) of the 88
patients. Transplantation would have been precluded in the care of two (2%) of
the 88 patients on the basis of false-positive results. According to the
false-negative results even at reevaluation, four (5%) of 88 patients would
have undergone liver transplantation outside the Milan criteria.
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Fig. 2B —53-year-old man with true-positive finding of histologically
proven hepatocellular carcinoma with hypovascular pattern. Portal phase of
MDCT scan shows mildly hypodense area without hyperdense rim.
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Fig. 2C —53-year-old man with true-positive finding of histologically
proven hepatocellular carcinoma with hypovascular pattern. Delayed phase of
MDCT scan shows mildly hypodense area without hyperdense rim.
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Fig. 3A —43-year-old man with false-negative findings. Large nodule of
hepatocellular carcinoma was managed with transcatheter arterial
chemoembolization in first liver segment. Unenhanced MDCT scan shows
hyperdense particles of iodized oil making density inhomogeneous.
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Fig. 3B —43-year-old man with false-negative findings. Large nodule of
hepatocellular carcinoma was managed with transcatheter arterial
chemoembolization in first liver segment. Arterial phase of MDCT scan shows
lesion enhancement cannot be assessed.
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Fig. 3C —43-year-old man with false-negative findings. Large nodule of
hepatocellular carcinoma was managed with transcatheter arterial
chemoembolization in first liver segment. Portal phase of MDCT scan shows
lesion washout cannot be assessed.
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Fig. 3D —43-year-old man with false-negative findings. Large nodule of
hepatocellular carcinoma was managed with transcatheter arterial
chemoembolization in first liver segment. Delayed phase of MDCT scan shows
lesion washout cannot be assessed.
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The sensitivity and PPV of MDCT resulting from analysis based on lesion
diameter are reported in Table
2. For calculation of PPV, nodules were divided into the three
size-based groups as follows: Of the 129 total nodules identified, 50 were
small, 42 were of intermediate size, and 37 were large.
Discussion
MDCT is currently considered one of the most reliable techniques for
evaluating hepatic cancer in the presence of cirrhotic liver disease
[11,
12], and it is primarily
involved in patient treatment strategies. Our retrospective study, through
comparison of imaging and histologic findings, showed that MDCT has acceptable
diagnostic performance in the detection of HCC in patients with cirrhotic
liver disease. In many previous studies
[9,
11,
13–26]
in which investigators assessed the accuracy of CT in the diagnosis of HCC in
cirrhotic livers with the explanted liver as the reference standard,
lesion-by-lesion sensitivity ranged from 37% to 82%
(Table 4). Our results are
consistent with those of the previous studies, in which the patient-by-patient
sensitivity of CT ranged from 50% to 96% and the specificity from 75% to 96%.
The low sensitivity reported in some studies can be due to fairly high slice
thickness (5–10 mm) and to imaging in the early arterial phase. It is
well known that to obtain the best conspicuity of lesions, arterial phase
images should be acquired 30–35 seconds after injection of contrast
medium [27]. However, even if
sensitivity and specificity are within the reported range, our study showed
specificity lower than sensitivity, likely because of the high false-positive
rate.
As expected, in our study the performance of MDCT was related to lesion
size, even when we used thin slices and established the arterial phase with
bolus-tracking technique. The sensitivity of MDCT for nodules decreased with
lesion size. We found very good sensitivity for HCCs larger than 20 mm,
acceptable sensitivity for nodules measuring 11–20 mm, and low
sensitivity for nodules 10 mm or smaller. This finding may have been due to
the altered hepatic structure from cirrhosis, which reduces the conspicuity of
small HCC lesions and makes their characterization difficult. Liver
inhomogeneity can also be increased by previous therapy for HCC (frequently
administered to patients with cirrhosis to reduce the extent of disease),
especially the use of radiopaque material in TACE
[12], and in hypodense areas
exposed to thermoablation. In our series, the numbers of HCC recurrences were
similar in analysis of the preoperative MDCT reports and at retrospective
review. An interesting finding was that two HCCs recurred after radiofrequency
treatment and four after combined TACE and radiofrequency ablation.
We noticed that not only sensitivity but also the PPV of MDCT decreased
with lesion size. These values were quite low for small nodules, increased to
an acceptable level for nodules of intermediate size, and were very good for
nodules larger than 20 mm. Brancatelli et al.
[28] and Valls et al.
[29] reported false-positive
rates of approximately 8% and 12%. We found a higher false-positive rate. A
possible explanation for the difference is that Brancatelli and Valls and
their colleagues used single-detector helical CT, whereas we used 16-MDCT. The
higher spatial and temporal resolution of 16-MDCT may have led to detection of
a higher number of nodules. It is well known, however, that hyperattenuating
nodules frequently correspond to benign lesions, such as regenerative and
dysplastic nodules [28,
29]. On the other hand, the
high false-positive rate might have been related to overlooking nodules at
histologic examination, because the histopathologic slice thickness was
greater than the CT slice thickness. Small hypervascular nodules should be
strictly monitored for size changes at followup or should be studied with MRI
[23,
24,
30].
The interpretation of small hypervascular lesions is clinically crucial to
patients with cirrhosis who are candidates for orthotopic liver
transplantation. According to the Milan criteria, on the basis of the
unblinded review of CT images in our series, transplantation would have been
precluded in the care of two patients. Some studies have shown that the Milan
criteria may be too strict and that approximately 50% of patients receiving
transplants outside the Milan criteria survive 5 years
[31]. Thus it is better that
MDCT findings lead to an underestimation of disease extent rather than an
overestimation, which would exclude from transplantation patients who would
benefit from it. In comparing results of previous studies with ours, it should
be emphasized that unlike the other investigators, we used MDCT to evaluate a
large number of patients and that pathologic diagnosis was obtained on whole
explanted liver in all cases.
The study had limitations. A disadvantage was that the histologic section
thickness was 7–10 mm. Even though it is commonly reported in
literature, this section thickness was higher than our CT slice thickness. Use
of thinner histologic sections would have allowed identification of smaller
nodules, likely reducing the CT false-positive rate. Another limitation was
that retrospective review of CT images does not reflect clinical routine,
increasing the sensitivity of the technique in day-to-day practice.
Retrospective review, however, can help illustrate how to exploit the
diagnostic performance of CT at the highest level.
Our study showed that MDCT has acceptable overall sensitivity in the
detection of HCC lesions, especially in staging for liver transplantation. The
caveat is that the high spatial and temporal resolutions of MDCT can lead to
detection of a large number of false-positive nodules and to inappropriate
exclusion of patients from transplantation lists.
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Abstract
Introduction
