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1 All authors: Department of Clinical Radiology, St. James's University Hospital, Beckett St., Leeds LS9 7TF, United Kingdom.
Received May 23, 2002;
accepted after revision August 27, 2002.
Address correspondence to P. J. Robinson.
Abstract
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SUBJECTS AND METHODS. Thirty-one patients underwent double-contrast MR imaging and subsequent liver transplantation. Breath-hold T1- and T2-weighted MR images were obtained before and after administration of superparamagnetic iron oxide, and three-dimensional T1-weighted gradient-recalled echo MR images were obtained 10, 40, and 120 sec after a bolus injection of gadolinium. Hypervascular lesions that failed to take up superparamagnetic iron oxide were regarded as showing typical characteristics of hepatocellular carcinoma; lesions that had only one of these two characteristics (either hypervascularity or failure to take up superparamagnetic iron oxide) were regarded as highly suspicious for hepatocellular carcinoma. Radiology reports were correlated with pathology reports for the explanted livers.
RESULTS. Thirty-two hepatocellular carcinomas were found in 14 of the 31 patients. Combining the number of MR imaging reports citing lesions that were "typical of hepatocellular carcinoma" with the number of those citing lesions that were "highly suspicious," we found that for 25 of 32 lesions, an accurate MR imaging diagnosis of hepatocellular carcinoma was made (overall sensitivity, 78%). These lesions included 10 of the 11 lesions that were larger than 20 mm (sensitivity, 91%), 12 of the 13 lesions that were 11-20 mm (sensitivity, 92%), and three of the eight lesions that were 10 mm or less (sensitivity, 38%). Nineteen (76%) of 25 lesions had characteristics considered typical of hepatocellular carcinoma; the remaining six lesions either failed to take up superparamagnetic iron oxide and were hypovascular or were hypervascular but showed some uptake of superparamagnetic iron oxide.
CONCLUSION. In patients with a cirrhotic liver, double-contrast MR imaging is highly sensitive in the diagnosis of hepatocellular carcinomas of 10 mm or larger, but success in the identification of tumors smaller than 10 mm is still limited.
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The prognosis of patients with untreated hepatocellular carcinoma is dismal, with a 5-year survival rate of less than 5%; lack of functional reserve precludes resection of tumors in many of these patients. Orthotopic liver transplantation offers a potential cure for patients with early-stage disease, but the prognosis is related to the size of the tumor. Transplantation in patients with a single hepatocellular carcinoma smaller than 5 cm in diameter or up to three hepatocellular carcinomas smaller than 3 cm in diameter resulted in a 4-year survival rate for 85% of the patients studied by Mazzaferro et al. [2]. Clinically silent hepatocellular carcinoma has a rapid doubling time [3], and unfortunately most patients present with advanced disease. Accurate early diagnosis and staging of hepatocellular carcinoma are critical in the selection of patients for and timing of transplantation.
Krinsky et al. [4] investigated the efficacy of gadolinium-enhanced MR imaging for revealing hepatocellular carcinoma in patients with a cirrhotic liver and found an overall sensitivity of 55% relative to the pathologic findings in the explanted liver. In that study, many lesions smaller than 2 cm in diameter were not seen on MR imaging. Similarly, the detection of small hepatocellular carcinomas using triphasic CT remains problematic, with only 59% of patients with tumors and 37% of hepatocellular carcinoma nodules being identified prospectively in a large series of recipients of transplanted livers [5]. An initial investigation of double-contrast MR imaging showed it to be a promising technique but again found limited success in the detection of small tumors [6].
The purpose of our study was to assess the clinical sensitivity of a modified double-contrast MR imaging technique in the detection of hepatocellular carcinoma in patients with a cirrhotic liver by correlating the prospective interpretation of MR imaging with pathologic findings in the explanted liver. In particular, we believed that the detection of small lesions might be increased using improved gradient coil technology and a three-dimensional gradient-recalled echo sequence that allows the acquisition of thin-slice images.
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MR Imaging
All MR imaging was performed at 1.5 T on a high-performance gradient system
(Symphony; Siemens, Erlangen, Germany) with a combination of spinal and phased
array body coils for transmission and reception of signals. All images were
acquired in the axial plane during breath-holding and included unenhanced
axial true fast imaging with steady-state free precession (TR/TE, 5.7/2.8),
T2-weighted fast spin-echo (2650/80; echo-train length, 29), and T1-weighted
in-phase (166/4.5; flip angle, 80°) and opposed-phase (144/ 2.4; flip
angle, 80°) sequences. A rectangular field of view and a slice thickness
(8-10 mm) optimized to suit each patient's body habitus were chosen and
remained constant for each sequence.
Superparamagnetic iron oxide (Endorem; Laboratoire Guerbet, Aulnay-sous-Bois, France) diluted in 100 mL of a 5% glucose solution was administered IV over a period of 30 min. One of two doses (either 7.5 or 15 µmol/kg of body weight) was used because some of the patients were taking part in a dose-finding study, the results of which have confirmed that lesion-to-liver contrast-to-noise ratios were similar at both doses [7, 8]. After the infusion of the superparamagnetic iron oxide solution, we acquired T2-weighted gradient-recalled echo MR images (165/15; flip angle, 30°). Immediately after this sequence, a rapid bolus of gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) or gadodiamide (Omniscan; Nycomed Amersham, Amersham, United Kingdom) was administered at a dose of 0.1 mmol/kg of body weight followed by 20 mL of saline flush. After delays of 10, 40, and 120 sec, three-dimensional T1-weighted gradient-recalled echo images with fat suppression (3.4/1.6; flip angle, 15°) and an effective slice thickness of 2.5-3.0 mm were acquired. This technique produced double-contrast MR images with superparamagnetic iron oxide and gadolinium in the arterial, portal venous, and equilibrium phases of enhancement.
Analysis of MR Imaging
All MR images were prospectively analyzed by one of two experienced
observers before orthotopic liver transplantation was performed. No patients
were excluded from the study because of technique failure. Lesions that were
visible on T2-weighted images after superparamagnetic iron oxide
administration and were also hypervascular on the T1-weighted arterial phase
images acquired after gadolinium administration were considered to be
displaying characteristics typical of hepatocellular carcinomas. Because
superparamagnetic iron oxide affects the signal intensity of normal liver
parenchyma on both T1- and T2-weighted images, hypervascularity was diagnosed
if the lesions showed a visibly greater signal intensity than the adjacent
liver parenchyma or if the lesions were visible only during the arterial phase
of enhancement. Lesions identified after superparamagnetic iron oxide
administration that were not hypervascular and those that were hypervascular
but were not identified after superparamagnetic iron oxide administration were
reported as highly suspicious and were considered to be hepatocellular
carcinomas for the purpose of statistical analysis.
Sensitivity, specificity, and positive and negative predictive values were calculated for each patient. Because of the possibility of multiple lesions in each patient, it was not feasible to define specificity and negative predictive values per lesion, but sensitivity and positive predictive values per lesion were calculated.
Pathologic Correlation
Pathologic examination of the explanted livers was performed by a single
experienced pathologist. The interval between MR imaging and liver
transplantation ranged from 3 to 245 days (median, 51 days). The explanted
liver was sliced into axial sections approximately 1 cm thick, and a
pathologic examination was performed for all suspicious macroscopic nodules.
Nodules were considered suspicious if they varied in size or color from the
surrounding regenerative nodules. The pathologist recorded the size and
position of tumors using the same template of cross-sectional liver anatomy
used by the radiologists reporting the MR imaging results.
The accuracy of the radiology reports was established by correlation with the pathology reports. We performed a retrospective analysis of the MR imaging characteristics of the true hepatocellular carcinomas identified and attempted to identify the cause of the false-negative and false-positive findings.
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Unenhanced T1- and T2-weighted MR imaging revealed 17 (68%) of the 25 tumors. On T1-weighted MR images, 12 tumors were hyperintense, eight were isointense, and five were hypointense relative to the adjacent liver parenchyma. On T2-weighted MR images, nine tumors were hyperintense, 15 were isointense, and one was hypointense. No hepatocellular carcinomas were seen on the unenhanced images only. Of the 25 tumors correctly identified, 19 (76%) were visible after the administration of superparamagnetic iron oxide and exhibited arterial phase enhancement after the administration of gadolinium; they, therefore, were typical of hepatocellular carcinomas. The remaining tumors displayed enhancement on only one of these sequences and were reported as highly suspicious for hepatocellular carcinomas. Four (16%) of the 25 correctly identified carcinomas were hypervascular nodules that were not visible on superparamagnetic iron oxide-enhanced images. Two tumors (8%) were visible after superparamagnetic iron oxide administration but were not hypervascular during the arterial phase, although one of these tumors displayed rim enhancement during the portal venous phase.
Fourteen false-positive lesion reports were made in eight patients. In all 14 cases, the abnormality was an area of arterial phase hypervascularity measuring 10 mm or smaller (mean size, 8 mm). Only one of the 14 lesions was visible on the T2-weighted superparamagnetic iron oxide-enhanced images. Four of the eight patients had multiple lesions, some of which were pathologically confirmed as hepatocellular carcinomas. However, the remaining four had no other abnormalities visible on MR imaging, and no hepatocellular carcinomas were subsequently identified at pathology.
Seven of the 32 hepatocellular carcinomas were not identified on MR imaging. In one patient, a nodule with an uptake of superparamagnetic iron oxide typical of healthy liver tissue was identified as an area of increased enhancement during the portal venous phase. The nodule measured 24 mm and was reported as being suspicious for a neoplasm but atypical for hepatocellular carcinoma according to our imaging criteria. Subsequent pathologic examination revealed the nodule to be a densely sclerotic hepatocellular carcinoma. Although identified prospectively, this lesion was considered a missed hepatocellular carcinoma for the purposes of our analysis.
The remaining six false-negative lesions all measured between 3 and 11 mm (mean size, 7.3 mm), and all occurred in four patients with other (between three and seven) hepatocellular carcinomas that were detected on double-contrast MR imaging. Through our retrospective review of the images of these patients, we were able to identify three of the lesions as areas of increased vascularity without a corresponding abnormality on superparamagnetic iron oxide-enhanced images. None of the 13 patients in whom no suspicious lesions were identified on double-contrast MR imaging were subsequently found to have hepatocellular carcinoma.
Sensitivity, specificity, and positive and negative predictive values per patient and per lesion are summarized in Table 2. Because of the possibility of patients having more than one lesion, the number of true-negative lesions could not be determined, so we could not define specificity and negative predictive values per lesion.
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-fetoprotein levels and regularly scheduled sonographic examinations
have been proposed for the surveillance of patients with cirrhosis.
Unfortunately, an increased -fetoprotein level is neither sensitive nor
specific enough to be used alone as a screening test for hepatocellular
carcinoma. Sonography has a high specificity, but two recent studies in which
the pathologic findings of the explanted liver tissue were correlated with
imaging findings estimated the sensitivity of sonography to be between 33% and
46% [9,
10]. In particular, sonography
has thus far been unreliable for revealing lesions smaller than 2 cm. Other researchers have investigated the efficacy of helical CT in the detection of hepatocellular carcinoma. Baron et al. [11] found a CT sensitivity exceeding 90%; however, that was a retrospective study of patients in whom the diagnosis of hepatocellular carcinoma had already been established. Because correlation with the pathologic findings of the explanted liver was not performed, the rate of false-negative results could not be estimated, so the sensitivity of imaging may be spuriously increased. Prospective CT screening studies using multiple-phase enhancement and pathologic correlation of the explanted liver have reported the sensitivity of CT to be 37% [5], 46% [10], or 71% [12]. This wide range may be explained by differences in patient selection or by variations in the pathologic gold standard used in the different studies. However, all these studies also found a low sensitivity of CT for lesions smaller than 2 cm. Potential improvements using multidetector CT with thinner slices have yet to be established in this context.
More lesions are detected on multiphase imaging with gadolinium enhancement than on unenhanced MR imaging [13]. Even so, contrast-enhanced MR imaging studies with pathologic correlation of the explanted liver have shown a disappointing sensitivity for the detection of small hepatocellular carcinomas [4]. Studies evaluating the relative accuracy of multiphase enhanced CT and MR imaging have suggested that MR imaging was more sensitive and more accurate for lesion detection and characterization than CT [10, 14].
Another advantage that CT has over MR imaging is that CT can be used to exploit the inability of most hepatocellular carcinomas to take up the tissue-specific superparamagnetic iron oxide contrast agents. Superparamagnetic iron oxide is taken up by the Kupffer's cells of the liver and increases local magnetic field inhomogeneity, which leads to rapid spin dephasing, shortening of T2 signal, and loss of the liver signal on T1-, T2-, and T2*-weighted MR imaging. Lesions that do not contain active Kupffer's cells include metastases, and most hepatocellular carcinomas do not lose signal in the presence of superparamagnetic iron oxide and therefore become more conspicuous relative to the normal liver parenchyma. Superparamagnetic iron oxide-enhanced imaging has been found to aid in the differentiation of benign and malignant hepatocellular liver lesions [15] and to be more sensitive than unenhanced imaging in the detection of hepatocellular carcinoma [16]. However, the technique may be less sensitive than dynamic gadolinium-enhanced MR imaging [17].
In double-contrast MR imaging with gadolinium and superparamagnetic iron oxide, we hope to exploit both the increased signal intensity of hypervascular lesions shown on T1-weighted images after gadolinium administration and the increased contrast between the tumor and normal liver parenchyma shown on T2-weighted images after superparamagnetic iron oxide administration, thereby using two abnormal features of tumors to increase the probability of their detection (Fig. 1A, 1B, 1C, 1D, 1E). Although superparamagnetic iron oxide also causes a degree of signal reduction in healthy liver parenchyma on T1-weighted images, this signal reduction does not hamper the enhancement effect of gadolinium, so recognition of hypervascular nodules is unimpaired. An initial study confirmed that double-contrast MR imaging improved the detection of hepatocellular carcinoma compared with superparamagnetic iron oxide-enhanced imaging alone and that double-contrast MR imaging significantly improved the detection of subcentimeter tumors, although the sensitivity remained disappointing [6]. Since that study was conducted, improvements in phased array body coils and the advent of higher performance gradients have allowed the acquisition of single-breath-hold three-dimensional data sets that encompass the whole liver with increased spatial and contrast resolution. The addition of fat-suppression techniques increases the dynamic range of T1-weighted contrast-enhanced MR images and increases the conspicuity of gadolinium-enhanced structures [18]. We believed that these technologic improvements may lead to increased sensitivity of double-contrast MR imaging in the detection of hepatocellular carcinomas.
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By correlating the findings on double-contrast MR imaging prospectively reported by radiologists experienced in MR imaging with pathologic findings in the explanted liver in all patients, we sought to prove the true efficacy of this technique in the detection of hepatocellular carcinomas in clinical practice. Consensus reporting was not performed; therefore, our results reflect both the performance of this technique and the interpretation of the images that the technique produced. We found that 13 (93%) of the 14 patients who had hepatocellular carcinomas were correctly identified. The remaining patient had a sclerotic hepatocellular carcinoma that was identified but was described as atypical for hepatocellular carcinoma because of its enhancement during the portal venous phase. Our overall sensitivity was 78% on a lesion-by-lesion basis.
Although differences in patient selection make direct comparisons difficult, our result compares favorably with the overall sensitivity of 53% reported by researchers who conducted a recent single-contrast MR imaging study and who then correlated their imaging findings with the pathologic findings in explanted tissue [4]. In our study, detection of 1- to 2-cm lesions was substantially improved using double-contrast MR imaging; this technique revealed 12 (92%) of 13 of lesions in this size range. Of these 12 lesions, nine showed the typical combination of hypervascularity and no superparamagnetic iron oxide uptake, two showed superparamagnetic iron oxide uptake with hypervascularity, and one was not hypervascular but showed no superparamagnetic iron oxide uptake. This detection rate compares favorably with six (50%) of 12 hepatocellular carcinomas measuring 1-2 cm detected using the single-contrast imaging technique of Krinsky et al. [4]. Another single-contrast MR imaging study reported a sensitivity of 77% but included only a small number of hepatocellular carcinomas [10].
Our previous double-contrast MR imaging study [6] reported an overall sensitivity of 80%. However, the true sensitivity is less than that because for some patients in that study, correlation with pathologic findings in the explanted liver was not performed. In the patient group whose imaging findings were correlated with the pathologic findings in the explanted liver, the sensitivity was 65%. Therefore, our current study shows an improvement in lesion detection.
The sensitivity of double-contrast MR imaging in the detection of subcentimeter hepatocellular carcinomas remained disappointing at 38% and was only marginally improved relative to our previous double-contrast MR imaging study [6] despite technologic improvements and the use of sequences with increased spatial resolution and reduced effective slice thickness. The missed lesions were all 11 mm or smaller and occurred in patients with multiple tumors, some of which were correctly identified (therefore, patient management was not affected). In the patients with missed lesions, the maximal interval between MR imaging and liver transplantation was only 47 days (median interval for the entire study population was 51 days), so we cannot attribute the misses to an increase in lesion size between the two examinations. Because some lesions were subtly visible on retrospective review, the misses might have resulted from satisfaction of search (i.e., having diagnosed one lesion, the observers may have been less rigorous in continuing to seek additional lesions). No patient with negative findings on double-contrast MR imaging was subsequently found to have a hepatocellular carcinoma.
In reviewing the imaging features of hepatocellular carcinomas, we found that unenhanced MR images were insensitive and nonspecific in the detection of hepatocellular carcinoma. Although 17 (53%) of 32 tumors were visible on unenhanced images, many tumors appeared as subtle abnormalities identified only after review of the contrast-enhanced images. A variety of T1 signal characteristics were obtained, but most frequently hepatocellular carcinomas were hyperintense compared with the normal liver parenchyma. The variability in T1 signal has been noted in previous studies [8, 19], but the cause of this variation has not been established. We identified fewer tumors on T2-weighted fast spin-echo MR images; however, these images more often showed the hyperintensity typical of hepatocellular carcinomas. Our results support those of Earls et al. [19], who concluded that the variable signal intensities made unenhanced MR images unreliable for the characterization of hepatocellular carcinomas because of an overlap between the appearance of carcinomas and the appearance of dysplastic nodules.
Contrast agents narrow the differential diagnosis of hepatocellular carcinoma and dysplastic nodules, but some overlap in their enhancement characteristics may be observed when either a superparamagnetic iron oxide or gadolinium contrast agent is used alone. Well-differentiated hepatocellular carcinomas may show some uptake of superparamagnetic iron oxide, and although most dysplastic nodules are hypovascular, a minority are hypervascular and a few hepatocellular carcinomas are hypovascular. Combining superparamagnetic iron oxide with gadolinium enhancement provides a more rigorous approach to lesion characterization. In our previous study [6], we were able to differentiate dysplastic nodules and hepatocellular carcinomas on the basis of their enhancement characteristics using both agents.
Nineteen of the 25 hepatocellular carcinomas that were correctly identified displayed typical enhancement features of arterial phase hypervascularity after gadolinium administration and failure to take up superparamagnetic iron oxide. Two more tumors failed to take up superparamagnetic iron oxide without displaying arterial phase vascularity. Review of the pathologic findings in these lesions showed that both had necrotic centers, which may explain their lack of arterial phase enhancement. One of these lesions showed no abnormality of enhancement on arterial, portal venous, or delayed MR imaging and was only correctly identified as a hepatocellular carcinoma on the superparamagnetic iron oxide-enhanced MR images (Fig. 2A, 2B, 2C, 2D).
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Arterial phase enhancement after gadolinium administration was seen in 23 of 25 hepatocellular carcinomas identified and was the most sensitive sign for the detection of hepatocellular carcinomas. Four hepatocellular carcinomas were identified on arterial phase MR imaging alone and appeared isointense on the preceding superparamagnetic iron oxide-enhanced MR sequence. Superparamagnetic iron oxide uptake is recognized as a feature of well-differentiated hepatocellular carcinomas [15]. Pathologically, two of these four lesions were well-differentiated, tumors, one was moderately differentiated, and one occurred in a patient with multiple tumors and was not specifically graded.
The 14 false-positive reports were based on findings of arterial phase enhancement (Fig. 3A, 3B). On pathologic examination of the explanted livers, none of these 14 nodules could be identified macroscopically. The lesions all measured 10 mm or less in diameter (mean, 8 mm), and 13 of 14 occurred in livers with diffusely nodular parenchyma. In retrospectively reviewing the images, we found that two lesions were areas of minimal enhancement that had been reported as low-confidence abnormalities, and one lesion was believed to represent an error in interpretation.
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The presence of hypervascular nodules that exhibit benign behavior on follow-up imaging and the difficulty in differentiating these nodules from small hepatocellular carcinomas have been noted previously [4, 20]. More recently, Jeong et al. [21] described a cohort of patients with cirrhotic livers and small nodules that were seen only on MR imaging because of their hypervascularity during the arterial phase of enhancement. These researchers found that only 13% of the nodules showed interval growth—all of which were confirmed to be hepatocellular carcinomas—whereas most of the nodules remained stable. The behavior of these nodules with superparamagnetic iron oxide administration may provide a useful indicator of their likely benignity. Of the 14 false-positive nodules in our current series, 13 (93%) showed uptake of superparamagnetic iron oxide. This feature was found in only four (16%) of the 25 hepatocellular carcinomas detected, which suggests that superparamagnetic iron oxide uptake in a small hypervascular nodule might indicate a decreased possibility of malignancy. In our review of the false-negative findings in our study, we found three subcentimeter hepatocellular carcinomas that showed superparamagnetic iron oxide uptake on T2-weighted MR imaging and minimal hypervascularity on T1-weighted imaging. Therefore, a degree of overlap exists between benign and malignant nodules.
Twenty-one of the 32 hepatocellular carcinomas present in this group of patients did not take up superparamagnetic iron oxide. This finding was highly specific for hepatocellular carcinoma although relatively insensitive. In our previous double-contrast MR imaging study [6], six false-positive lesions seen after superparamagnetic iron oxide administration were found to be either regenerative nodules or areas of fibrosis at pathology. This error did not occur in our current study, possibly because of the improved image quality of our T2-weighted gradient-echo MR imaging sequence and our increased experience in the interpretation of these images. Only one of the 14 hypervascular false-positive lesions was visible after superparamagnetic iron oxide administration, whereas 21 of 25 true-positive lesions were well depicted after superparamagnetic iron oxide administration. We suspect the 7-mm hypervascular false-positive lesion may have been a true hepatocellular carcinoma nodule missed at the pathologic examination of the explanted liver (Fig. 4A, 4B).
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The nodular texture of cirrhotic livers makes macroscopic identification of small hepatocellular carcinomas difficult. A previous study has shown that although pathology of the explanted livers is considered a gold standard, small lesions with no distinguishing macroscopic features may be missed at the initial pathologic examination resulting in artificial false-positive imaging findings [22]. The combination of arterial phase hypervascularity and failure to take up superparamagnetic iron oxide was considered typical behavior for hepatocellular carcinoma and was seen in 19 (76%) of the 25 hepatocellular carcinomas identified.
No doubt the use of two contrast agents adds to the cost of the investigation and increases the time needed to acquire and report the imaging results. These disadvantages need to be balanced against the value of earlier or more accurate diagnosis of hepatocellular carcinomas in patients with a cirrhotic liver. For these patients, the findings of double-contrast MR imaging are likely to result in an earlier offer of liver transplantation than would otherwise be the case, but it is difficult to show a significant improvement in the eventual outcome.
Several limitations of our study should be mentioned. In order to reflect routine clinical practice, we did not perform consensus reporting but evaluated the prospective interpretation of the MR images by a single observer. Therefore, our results reflect the performance of both the observer and the imaging technique. We were not always able to immediately compare the images with the pathologic examination of the explanted liver, so correlation may be imperfect in these cases. Our cohort contained only eight hepatocellular carcinomas measuring 10 mm or less, limiting the statistical strength of our analysis of this crucial group of lesions. Although no patient was known to have a hepatocellular carcinoma before imaging, all were high-risk patients with late-stage disease; this positive bias may limit the application of these results to screening populations. The use of two different doses of superparamagnetic iron oxide appears to add an unnecessary variable to the methodology. However, in a previous study [8] of patients without cirrhosis who had liver metastases, we found no difference in lesion-to-liver contrast-to-noise ratios at the lower dose, and these findings have now been confirmed in a series of patients with a cirrhotic liver, including some of those included in this study [7].
In summary, we found that the double-contrast MR imaging technique is an improvement over multiphase CT and single-contrast MR imaging for the detection of hepatocellular carcinoma. The combination of arterial phase hypervascularity and increased lesion conspicuity after superparamagnetic iron oxide administration is highly specific for the diagnosis of hepatocellular carcinoma in patients with a cirrhotic liver. Advances in technology have allowed better lesion detection than was possible in our previous double-contrast MR imaging study, but the identification of tumors that are 10 mm or smaller remains problematic.
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