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Gastrointestinal Imaging |
1 From the Departments of Radiology (M.S.P., R.L.B., J.H.O., S.R.C., L.E.H.) and Surgery (J.W.M.), University of Pittsburgh School of Medicine, 200 Lothrop St, Pittsburgh, PA 15213-2582. From the 1996 RSNA scientific assembly. Received January 28, 2000; revision requested March 15; revision received May 5; accepted May 22. Address correspondence to M.S.P. (e-mail: petersonms@radserv.arad.upmc.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Prospective direct correlation of CT findings with explanted liver specimen findings was performed in 430 transplant recipients with cirrhosis. The prevalence of clinically unsuspected HCC according to liver disease cause was evaluated. Serum 
-fetoprotein (AFP) values in patients with and those without tumor were recorded. Prospective and retrospective CT tumor detection was evaluated with respect to CT technique and time from CT to transplantation.
RESULTS: HCC was found in 59 (14%) of 430 transplant recipients without suspicion of tumor before referral for transplantation. HCC was most prevalent with hepatitis B (27%) and hepatitis C (22%). Serum AFP values were not sensitive for detection of most small tumors. With triphasic helical CT, the prospective and retrospective rates of identifying patients with tumor were 59% and 68%, respectively; the prospective and retrospective tumor nodule detection rates were 37% and 44%, respectively. Tumor detection rates were highest with CT performed within 67 days before transplantation.
CONCLUSION: Clinically unsuspected HCC is most prevalent with cirrhosis secondary to hepatitis B or C, and, when evaluated at CT, is best detected with triphasic contrast material–enhanced helical imaging performed within 67 days before transplantation.
Index terms: Liver, cirrhosis, 761.288, 761.794 • Liver, CT, 761.12111, 761.12112, 761.12114, 761.12115 • Liver, transplantation, 761.459 • Liver neoplasms, 761.323 • Liver neoplasms, CT, 761.12111, 761.12112, 761.12114, 761.12115
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Although the examination of patients with cirrhosis for possible HCC includes thorough clinical, laboratory, and imaging examinations, some patients who undergo transplantation are nonetheless found at pathologic evaluation of explanted native livers to have harbored unsuspected or undiagnosed tumors (11). Accurate preoperative surveillance of transplantation candidates with cirrhosis for unsuspected HCC is important not only to diagnose and correctly stage the tumor so that the appropriate treatment can be offered (12) but also to prevent ineffective transplantation in patients with advanced disease (13). This is particularly important in light of the limited supply of donor livers relative to the large number of patients awaiting transplantation.
Given the length of many transplantation waiting lists, it is important to identify small tumors so that appropriate treatment can be offered or consideration can be given to moving a patient to a higher position on the waiting list. These measures are important to help prevent progression of a small treatable tumor to advanced-stage disease. Furthermore, it is not uncommon to find that unsuspected HCC diagnosed after transplantation is multifocal or bilobar advanced-stage intrahepatic disease that necessitates adjuvant chemotherapy after transplantation. The immunosuppressed state of transplant recipients may adversely affect patient tolerance to chemotherapy and chemotherapy efficacy (14).
Although computed tomographic (CT) scanning is a commonly used conventional technique for pretransplantation imaging evaluation of patients with cirrhosis, the actual sensitivity of CT surveillance for detection of clinically unsuspected HCC tumor may vary according to several factors, including scanning technique, tumor size, and interval from scanning to transplantation. We undertook this study of the prospective direct correlation of pretransplantation CT findings with surgical pathologic findings of explanted livers to assess the sensitivity of helical CT for tumor detection and determine the relative prevalence of unsuspected HCC according to various causes of cirrhosis.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Patients who received transplants for acute fulminant hepatitis or other causes of liver disease without cirrhosis were not included in the study population. Prospective correlation of the surgical pathologic findings with the preoperative CT findings was performed in all 430 transplant recipients. The 430 patients who comprised the study population included 248 male and 182 female patients (mean age, 54 years; age range, 17–73 years). HCC was diagnosed at surgical pathologic evaluation of explanted livers in 59 patients (41 men, 18 women; mean age, 57 years; age range, 28–69 years). Clinical records were reviewed to document the cause of liver disease in each patient and to ensure that no tumor had been clinically suspected or diagnosed before referral for transplantation. Serum -fetoprotein (AFP) values were available in 406 of the 430 transplant recipients, including 58 of the 59 patients with HCC. Mean AFP levels were determined in the subsets of transplant recipients with and without HCC. The time from last CT examination to transplantation in each patient also was determined.
CT Technique
All patients underwent an initial CT examination, and most were followed up with additional examinations until transplantation. Because not every patient who underwent clinical evaluation underwent transplantation, the prospective data entry was performed at the time of gross pathologic evaluation of the explanted livers after transplantation. The availability of donor livers could not be predicted; thus, the time of CT relative to the time of transplantation was not controlled. Early in the study period, some patients underwent CT performed with nonhelical scanners. These patients were included in the database to allow assessment of the prevalence of HCC at transplantation in the entire surveillance population. Because multiple CT scanners were used, no one date when all the patients in the surveillance population would have undergone helical CT could be selected. The majority of patients underwent CT performed by using a helical technique with a current-model scanner (HiSpeed Advantage; GE Medical Systems, Milwaukee, Wis).
CT scans were obtained, when possible, with a triphasic technique (15), which included the acquisition of nonenhanced images of the liver followed by the acquisition of images with intravenous contrast material–enhanced biphasic helical CT during the hepatic arterial and portal venous phases of enhancement. Section collimation was 7 mm with a pitch of 1.5:1.0. Scanning delays were 20–28 seconds for hepatic arterial phase imaging and 60–70 seconds for portal venous phase imaging. The contrast-enhanced images were obtained with 150 mL of iodinated contrast material (iothalamate meglumine injection 60% [Conray] or ioversol injection 68% [Optiray 320]; Mallinckrodt, St Louis, Mo), which was administered intravenously with a mechanical power injector (Medrad, Pittsburgh, Pa) at a rate of 2.5–5.0 mL/sec.
Although most of the patients underwent biphasic CT scanning with contrast material injection rates of 4–5 mL/sec, early in our experience with biphasic CT, before we were aware of the effectiveness of higher contrast material injection rates in increasing the conspicuity of vascular tumors, some patients received contrast material injected at a rate of 2.5 mL/sec. The rates of contrast material injection were not recorded in our medical records, so we cannot determine how many patients were administered contrast material at the lower rate of 2.5 mL/sec.
Of the 430 patients, 320 underwent CT with the triphasic technique, 92 underwent nonenhanced and portal venous phase CT, and 18 underwent only nonenhanced CT. Those patients who underwent nonenhanced and portal venous phase CT rather than triphasic CT usually had poor venous access that precluded the intravenous injection of contrast material at the higher rate necessary for triphasic imaging or underwent imaging with a nonhelical scanner. Those patients who underwent only nonenhanced CT had renal insufficiency or other contraindications to contrast material administration.
CT Scan Interpretation
The CT diagnoses of liver lesions were evaluated in two ways. The prospective original clinical reports on the CT scans rendered by experienced radiologists with subspecialty expertise in abdominal imaging at the time of the examinations were used for primary data analysis of CT tumor detection. The CT scans that showed lesions that were considered to be diagnostic of or highly suspicious for HCC according to the original clinical report were considered to be positive. The lesions considered to be positive for tumor also included those that were described by the readers of the CT scans as enhancing lesions with characteristics not typical of hemangiomas and as hypovascular masses not characteristic of cysts or hemangiomas. Conversely, the CT scans that were reported to be equivocal or negative for tumor were considered to be negative. In the patients who underwent multiple CT examinations, the CT results were considered to be positive when any scan was positive.
Given the large number of patients and CT scans and the clinical interpretation of the CT scans by a number of abdominal imaging subspecialist radiologists, data based on prospective specific diagnostic criteria for HCC diagnosis were not collected.
To prospectively correlate the imaging findings with the surgical pathologic findings (described in next section), all of the CT scans were also retrospectively reviewed at the time of specimen sectioning. Any tumor detected at pathologic analysis that was not reported in the clinical CT reports was recorded. The tumors not initially reported that were retrospectively detectable at CT after surgical pathologic correlation were subsequently confirmed by means of agreement between two investigators.
Imaging-Pathologic Correlation
Within 24 hours after transplantation, at surgical pathologic gross-specimen evaluation, the explanted livers were cut into 8–10-mm-thick sections that matched as closely as possible the transverse orientation of the CT images. The preoperative CT findings were prospectively and directly correlated with the surgical pathologic findings by an investigator experienced in abdominal imaging who was present during specimen sectioning. The number, size, and location of all lesions suspicious for HCC at specimen sectioning were recorded prospectively. The specimens were also carefully examined to identify any lesions seen on the preoperative CT scan that were suspicious for tumor. If a lesion seen at preoperative CT was not found in the initial specimen sections, additional thinner sections in additional planes were made to improve correlation between the imaging and pathologic findings. Specimen section maps were recorded to correlate the imaging and pathologic findings. Lesion specimen pathologic section numbers also were recorded for subsequent direct histologic correlation with specific CT findings.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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AFP Levels
The reference range for normal serum AFP values at our clinical laboratory is 0–20 µg/L. The mean serum AFP level in 348 patients without HCC was 8 µg/L (range, 1–166 µg/L; median, 4 µg/L). The mean serum AFP level in 58 patients with HCC was 48 µg/L (range, 0–1,378 µg/L; median, 5 µg/L). When two patients with HCC and outlier AFP values of 776 and 1,378 µg/L were excluded from consideration, the mean serum AFP level in the remaining 56 patients with tumor was 11 µg/L (range, 0–87 µg/L; median, 5 µg/L). The elevated AFP values in these two patients were first detected after the patients had been referred to our institution, without clinical suspicion of tumor, for liver transplantation evaluation, which included CT scanning. Triphasic helical CT in these two patients depicted small (<3-cm) solitary tumors, which were confirmed at subsequent pathologic analysis.
HCC Detection at CT
Of 59 patients with HCC, 44 (75%) underwent triphasic helical CT; 11 (19%), nonenhanced and portal venous phase CT; and four (7%), only nonenhanced CT prior to transplantation. Prospectively, CT with all techniques depicted tumor in 26 (44%) patients with HCC (Fig 1). At retrospective review, tumor was detectable by using CT in 31 (52%) patients with HCC (Fig 2). When only triphasic helical CT was considered, however, prospective tumor detection was increased to 59% (26 of 44 patients) and retrospective tumor detection was increased to 68% (30 of 44 patients). Prospective and retrospective HCC tumor detection rates at CT are presented in Table 2.
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Of 105 tumor nodules detected at pathologic analysis, 30 (29%) were detected prospectively at CT and 37 (35%) were detectable retrospectively at CT. When only triphasic helical CT was considered, however, prospective tumor nodule detection increased to 37% (30 of 82 tumor nodules found at pathologic analysis) and retrospective tumor nodule detection increased to 44% (36 of 82 tumor nodules). The 37 tumor nodules that were detectable retrospectively at CT ranged in size at surgical pathologic analysis from 9 to 60 mm (mean, 24 mm), whereas the 68 tumor nodules that were not detected at CT and found only at surgical pathologic analysis ranged in size from 2 to 40 mm (mean, 13 mm).
The mean time from the last CT examination to transplantation in the 59 patients with HCC was 107 days (median, 49 days; range, 1–671 days). The HCC detection rates according to time from last CT examination to transplantation are presented in Table 3. Note that no tumor was prospectively detected by using CT in any patient whose scan was obtained more than 180 days before transplantation. CT tumor detection was highest in patients who underwent scanning within 67 days before transplantation.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Imaging in the transplantation candidate with cirrhosis, which is often performed with CT, helps to confirm suspected manifestations of portal hypertension and enables noninvasive imaging of the liver parenchyma and major hepatic vessels. Recent technologic advances in CT scanner design have led to the implementation of helical scanning techniques that enable imaging of the entire liver in both the early phase of hepatic arterial parenchymal contrast enhancement and the slightly later phase of portal venous parenchymal contrast enhancement (15,17–19). Because virtually all primary liver tumors are perfused predominantly by the hepatic arterial circulation, the ability to rapidly scan the entire liver during the arterial phase of enhancement allows increased detection of hypervascular arterial phase enhancing tumors (18,19). Furthermore, the ability to rapidly scan the liver again during the portal venous phase of enhancement facilitates the detection of less vascular tumors that are not hypervascular on initial arterial phase images (19).
Although inclusion of nonenhanced CT occasionally facilitates the detection of less common HCC tumors that are enhancing to a similar degree as normal liver and consequently are not visible on contrast-enhanced images (19), the use of nonenhanced or portal venous phase CT alone is inadequate to effectively examine patients with cirrhosis for possible HCC. In patients who cannot undergo contrast-enhanced CT because of renal insufficiency or sensitivity to iodinated contrast material, dynamic gadolinium-enhanced magnetic resonance (MR) imaging is an effective alternative (20).
The reported sensitivities of CT for HCC detection vary, although in an earlier, often-referenced well-written and well-performed study of the efficacy of imaging for detecting HCC, CT reportedly depicted tumor in 84 (84%) of 100 patients with small (<3-cm) tumors (21). This reported detection rate, however, was from a retrospective unblinded study of CT scans obtained in only patients referred with known tumors. Patients at high risk for tumor but with no detected tumor were not included. Consequently, that study did not include patients with tumors and false-negative entry CT studies, because these were not corroborated with follow-up imaging or pathologic correlation. This bias due to the exclusion of false-negative CT studies can lead to higher reported CT tumor detection rates.
A valuable feature of our study was the prospective direct correlation of surgical pathologic findings with preoperative CT scan findings in a large surveillance population of patients with cirrhosis but without known or suspected HCC who were referred for transplantation evaluation. Unlike earlier studies (21,22) of tumor detection rates at imaging that involved the retrospective assessment of imaging modality efficacy in cases of known tumors, in our study we correlated the surgical pathologic findings in all 430 transplant recipients—both with and without HCC—with the preoperative CT findings.
Studies in which an imaging modality is evaluated for detection of a disease diagnosed by using a surgical procedure performed only in cases of a positive imaging result cannot avoid major biases. In such studies, designed so that only those patients with positive imaging results undergo surgery, retrospective review of imaging efficacy in surgically proved cases circuitously leads to spuriously high imaging examination sensitivity. A study of this design also has an inherent bias due to the exclusion of patients who did not have a positive imaging result and consequently did not undergo the surgical procedure. In other words, such a study does not include the further examination of those patients with negative (both true and false) imaging results. This leads to a higher reported sensitivity of disease detection, because the patients with false-negative imaging results do not undergo the diagnostic procedure performed because of positive imaging results and are consequently excluded from further analysis.
The examination of all patients with cirrhosis who are referred for transplantation without suspicion of tumor, even those who are found not to have tumor, enables a more accurate assessment of the sensitivity of surveillance CT imaging. This is the most likely reason that the tumor detection rate in our study, which was not limited to patients with positive imaging findings and included those with both true- and false-negative CT results, was lower than that in previous reports (21,22).
Furthermore, prospective direct imaging-pathologic correlation of the entire liver at the time of gross surgical pathologic evaluation allows a more comprehensive pathologic reference standard for the assessment of tumor detection. Because of the intensive examination of surgical specimens in our study, a larger number of HCC tumors may have been identified compared with that detected with other tumor detection imaging studies that had less intensive or less directed examination of surgical specimens. The additional tumors identified with a more extensive examination of the pathologic specimen often are small tumors, as reflected in the mean size of the tumor nodules seen only at pathologic analysis in our study—1.3 cm. The detection of these additional small tumors at pathologic analysis, which probably would not have occurred with less intensive specimen examination, probably also contributed to the higher false-negative CT detection rate in our study compared with that in prior studies.
As shown in Table 1, our results indicated that different prevalences of HCC were associated with different causes of end-stage liver disease. The highest prevalence of unsuspected HCC (27%) was found in patients with cirrhosis secondary to hepatitis B infection. A prevalence of 22% was observed in patients with hepatitis C, the most common cause of cirrhosis in our transplant recipient population. These findings indicate that patients with cirrhosis secondary to viral hepatitis should undergo particularly careful tumor surveillance. Any lesions suspicious for tumor that are detected at CT or any other imaging examination in patients with cirrhosis—especially those with cirrhosis secondary to viral hepatitis or alcohol-related disease, which have higher prevalences of HCC—should be carefully evaluated further, usually with biopsy.
The time from surveillance CT to transplantation has been shown to inversely correlate with tumor detection at CT. A small number of false-negative CT studies reflect observer errors or "misses" at scan interpretation—that is, tumors visible retrospectively at direct correlation with the explanted liver specimen findings that were not diagnosed prospectively (Fig 2). However, many false-negative CT studies, particularly those performed with the optimal triphasic technique, more likely reflect interval tumor development or growth between the time of CT and the time of transplantation. In a few cases, a false-negative CT study represents true failure of the technique to depict tumor (Fig 3).
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A 6-month interval for surveillance of patients with cirrhosis for possible HCC also has been proposed by other authors (4) as a reasonable approach, given that the median tumor doubling time for HCC tumors smaller than 5 cm has been reported to be 117 days. Although undiagnosed tumors are usually stage I tumors, HCC has variable biologic behavior and small tumors can grow to advanced-stage disease in a short time.
Our study was not without limitations. As a large epidemiologic study with hundreds of patients, some variables (eg, time of CT relative to time of transplantation) could not be rigorously controlled. Unlike in smaller controlled studies, in our study we did not attempt to evaluate interobserver variability in scan interpretation or specific diagnostic signs for HCC diagnosis. Our data reflect our experience in an academic tertiary-care medical center with an active transplantation program, with determination of HCC prevalence in patients with end-stage cirrhosis and assessment of the sensitivity of practical surveillance CT—particularly helical triphasic scanning—for HCC tumor detection.
Of additional interest is the spectrum of other lesions that may mimic HCC, particularly at arterial phase CT. Although this topic was beyond the scope of our current study, it merits further investigation. Finally, it has been observed that the rate of contrast material administration can affect the capability of CT to depict hypervascular lesions at arterial phase contrast-enhanced CT (23). A minority of the patients underwent biphasic scanning with a slower contrast material injection rate (2.5 mL/sec) early in our study; this may have affected the effectiveness of CT for tumor detection in this small group of patients.
Our study results represent data on the epidemiology of HCC in a large surveillance population of patients with cirrhosis who were referred for transplantation evaluation without known or clinically suspected tumor. Because these patients were not suspected of having tumor, they represented a true surveillance population, not a series of consecutive transplant recipients. Although HCC detection is also possible with ultrasonography (US) or MR imaging, US does not readily lend itself to as strict an imaging-pathologic correlation as does CT, because US documentation of the entire volume of liver tissue is not routinely performed. Although MR imaging is a powerful technique for liver imaging, to our knowledge, a large study of MR imaging surveillance of patients with cirrhosis but without known or clinically suspected HCC who have undergone transplantation has not been published.
CT scanning is a common powerful noninvasive diagnostic examination with a greater sensitivity for detection of small HCC tumors than serum AFP screening, but it must be performed with the optimal triphasic helical technique. In summary, clinically unsuspected HCC is most prevalent with cirrhosis secondary to hepatitis B or C, and, when evaluated at CT, is best detected with triphasic contrast-enhanced helical scanning performed within 67 days before transplantation.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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-fetoprotein,
HCC = hepatocellular carcinoma Author contributions: Guarantor of integrity of entire study, R.L.B.; study concepts and design, R.L.B.; definition of intellectual content, M.S.P., R.L.B.; literature research, M.S.P.; clinical studies, all authors; data acquisition, R.L.B., S.R.C., L.E.H., M.S.P., J.H.O.; data analysis, M.S.P., R.L.B.; manuscript preparation, M.S.P.; manuscript editing, M.S.P., R.L.B.; manuscript review, M.S.P., R.L.B., J.W.M.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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