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Triple Arterial Phase Dynamic MRI with Sensitivity Encoding for Hypervascular Hepatocellular Carcinoma: Comparison of the Diagnostic Accuracy Among the Early, Middle, Late, and Whole Triple Arterial Phase Imaging

¹ Department of Radiology, Institute of Clinical Medicine, University of Tsukuba, Tennodai 1-1-1, Tsukuba, Ibaraki 305-8575, Japan.
² Department of Radiology, Brigham and Women's Hospital, Boston, MA 02115.
³ Department of Radiology, Asahikawa Medical College, Asahikawa 078-8510, Japan.
⁴ Department of Diagnostic Imaging, National Hospital Organization Mito Medical Center, Mito, Ibaraki 311-3117, Japan.

Received February 12, 2004; accepted after revision June 7, 2004.

 
Address correspondence to K. Mori (moriken{at}md.tsukuba.ac.jp).

Abstract

Top Abstract Introduction Materials and Methods Results Discussion References

 
OBJECTIVE. We assessed and compared the diagnostic accuracy of the early, middle, late, and whole triple arterial phase MRI with sensitivity encoding (SENSE) for the detection of hypervascular hepatocellular carcinoma (HCC).

MATERIALS AND METHODS. Thirty-one patients with 102 HCCs underwent dynamic MRI with SENSE. The findings of CT examinations, combined with those of visceral angiography or histopathologic examination, were used as the gold standard. After acquisition of T1- and T2-weighted images, gadolinium-enhanced triple arterial, portal, and delayed phase images were obtained. Acquisition of the triple arterial phase imaging was started at the timing of peak aortic enhancement and completed within a single breath-hold. Acquisition time for each phase was 8.4 sec. Four image sets including the early, middle, late, and whole triple arterial phase imaging were interpreted separately by four observers. The mean values of area under alternative-free-response receiver operating characteristic (AFROC) curve and of sensitivity were compared among the four image sets.

RESULTS. The mean values of area under AFROC curve were 0.52, 0.66, 0.53, and 0.68 and of sensitivity were 45%, 64%, 48%, and 65% for the image sets with the early, middle, late, and whole triple arterial phase imaging, respectively. Both mean values were significantly higher for the image sets with the middle and whole triple arterial phase imaging than for those with the early and late arterial phase imaging.

CONCLUSION. The middle arterial phase imaging with k-space centered at 12.6 sec after the peak aortic enhancement was optimal for detecting HCC and showed diagnostic accuracy equivalent to that of the whole triple arterial phase imaging.

Introduction

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Because of their hypervascularity, hepatocellular carcinomas (HCCs) can be most sensitively detected on contrast-enhanced arterial phase imaging. For this purpose, dynamic helical CT and MRI generally have been performed in patients with chronic liver damage or cirrhosis. In many previous studies, the acquisition time of the whole liver imaging was so long that the arterial phase imaging could be performed only once within a single breath-hold [1–10]. In recent years, however, MDCT and parallel imaging methods such as sensitivity encoding (SENSE) for MRI were developed and enabled acquisition of images of the whole liver within 8–11 sec [11–14]. This shorter acquisition time was reasonable for detection of HCCs because the duration of the optimal arterial phase was reported to be quite short, ranging from 7 to 19 sec (mean, 12.2 sec) with a helical CT [15]. Because the acquisition timing for the optimal arterial phase imaging to detect hypervascular HCC was unknown, multiarterial phase imaging with MDCT and MRI was performed by some investigators. Murakami et al. [11] and Ichikawa et al. [12] performed receiver operating characteristic (ROC) analyses of double arterial phase imaging with MDCT. Both groups of investigators concluded that the late arterial phase imaging showed greater sensitivity and area under the ROC curve than the early arterial phase imaging did. Meanwhile, it was controversial whether early arterial phase imaging was necessary to detect HCCs. Although Murakami et al. [11] emphasized double arterial phase imaging as superior to late arterial phase imaging alone, Ichikawa et al. [12] concluded that no significant difference was observed between the double and the late arterial phase imaging. As for MRI, Yoshioka et al. [13] reported that double arterial phase MRI with SENSE showed greater sensitivity and positive predictive value (PPV) than did conventional single arterial phase MRI. Takahashi et al. [14] performed the quantitative analysis of triple arterial phase dynamic MRI with SENSE and concluded that the peak enhancement of HCC was observed in the second or third arterial phase; however, no ROC analysis was performed in their studies.

The purposes of this study were to clarify the acquisition timing for optimal arterial phase imaging for the detection of hypervascular HCCs by ROC analysis of the triple arterial phase dynamic MRI and to decide whether triple arterial phase imaging is superior to optimal arterial phase imaging alone.

Materials and Methods

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Patients
From May 2002 to March 2003, 113 consecutive patients with suspected HCCs underwent gadolinium-enhanced triple arterial phase dynamic MRI. Of these patients, 42 were diagnosed as having hypervascular HCCs, either by histopathologic examination after partial hepatectomy (n = 1) or by at least two of the following three typical findings on CT examinations combined with visceral angiography (n = 41): nodular perfusion defect on CT during arterial portography (CTAP), nodular enhancement on CT hepatic arteriography (CTHA), and nodular deposition of iodized oil on CT after transarterial chemoembolization. Of the 41 patients who underwent visceral angiography, 11 were excluded from our study population because the image quality of CTAP or CTHA was degraded by one of the following factors: a tumor thrombus in the portal vein or its branches (n = 4), too many (more than 15) lesions were detected to analyze (n = 4), the same patient was examined twice during the period (n = 2), or no lesion was detected (n = 1). Thus, the final study group comprised 31 patients with 102 foci of hypervascular HCC. The patients included 26 men and 5 women who ranged in age from 47 to 86 years (mean age, 68 years). The 102 foci of HCC ranged from 4 to 200 mm (mean, 17.7 mm). The time interval between MRI and surgery or CT examinations combined with visceral angiography was 3–71 days (mean, 25.6 days). Of the 30 patients diagnosed as having HCCs by CT examinations combined with visceral angiography, 28 underwent CTAP, CTHA, and iodized-oil CT; one underwent CTAP and CTHA and one underwent CTAP and iodized-oil CT. All patients included in the present study gave informed consent, and examinations were in accord with the Declaration of Helsinki principles.

MRI
All patients were examined with a 1.5-T unit (Gyroscan NT Intera; Philips Medical Systems) using a phased-array body coil (Synergy body coil, Philips Medical Systems. All images were acquired using the SENSE technique with a reduction factor of 2 during breath-holding. Before the administration of gadolinium, a T1-weighted fast-field-echo (FFE) sequence (TR/TE, 168/4.6; flip angle, 70°; matrix, 130–138 x 512; acquisition time, 8.4 sec) and a T2-weighted turbo spin-echo (TSE) sequence with fat suppression (TR/TE, 1800/90; matrix, 300–316 x 512) were performed. Subsequently, a single-level dynamic FFE sequence (TR/TE, 14/1.5; flip angle, 60°; matrix, 128 x 256) with test injection was performed at the level of the right diaphragm to determine the delay time to start the triple arterial phase dynamic MRI. For the test injection, 1 mL of gadolinium (0.5 mmol/mL gadodi-amide; Omniscan; Daiichi Pharmaceutical) was injected at a rate of 2.5 mL/sec with a power injector (Sonicshot 50; Nemotokyorindou) followed by a 20-mL saline flush at a similar rate. A time–intensity curve was generated for the region of interest in the aorta. In the triple arterial phase dynamic MRI, 14 mL of gadolinium and 20 mL of saline were injected at a rate of 2.5 mL/sec and the image acquisition was started from the time of the peak aortic enhancement revealed in the test injection. T1-weighted FFE images with parameters identical to those of the unenhanced study were acquired three times (the early, middle, and late arterial phases) in an arterial phase within a single breath-hold. The acquisition time for each phase was 8.4 sec. Thus, the early, middle, and late arterial phase imaging was started at 0, 8.4, and 16.8 sec, respectively, after the peak aortic enhancement. The duration of the breath-holding needed to obtain the whole triple arterial phase imaging was 25.2 sec. The mean delay time to the peak aortic enhancement was 20.1 sec (range, 14.0–26.0 sec). Accordingly, the mean total delay times for the early, middle, and late arterial phase imaging were 20.1, 28.5, and 36.9 sec, respectively. Portal and equilibrium phase imaging was also performed at 70 and 180 sec, respectively, after the injection of gadolinium. Field of view, section thickness, and intersection gap were adjusted to cover the entire liver for each patient, and ranged from 32–40 cm, 8–9 mm, and 0.8–3 mm, respectively.

Image Analysis
We evaluated four image sets. All of them included unenhanced T1-weighted FFE and T2-weighted TSE images and gadolinium-enhanced portal and equilibrium phase T1-weighted FFE images. In addition, gadolinium-enhanced early arterial phase imaging was included in Set 1, middle arterial phase imaging was included in Set 2, late arterial phase imaging was included in Set 3, and whole triple arterial phase imaging composed of the early, middle, and late arterial phase imaging was included in Set 4 (Table 1). Four observers who were unaware of the results of the other observers, of the results of histopathologic examination, and of the findings on CT examination combined with visceral angiography reviewed the four image sets in the following order: Set 1, Set 3, Set 2, and Set 4. This order was chosen because the lesion-to-liver contrast-to-noise ratio was expected to be highest in the middle arterial phase imaging according to the previous study by Takahashi et al. [14]. Only one image set was evaluated per session and the following session was held more than 1 week later to minimize any learning bias. The observers marked all possible hypervascular HCCs on hard copies, assigning each one a confidence rating on a four-point scale: "1" was defined as probably not a lesion; "2" as a possible lesion; "3" as a probable lesion; and "4" as a definite lesion. At the time of scoring, the observers were aware that those lesions among the 102 foci of hypervascular HCC that were assigned a confidence level of 3 or 4 were considered true-positive lesions.

To characterize the three different times of arterial phase imaging in terms of vascular appearance, we assessed the extent of opacification for the portal vein and hepatic vein in each arterial phase imaging. For the evaluation of the portal venous enhancement, 30 patients without any evident arterioportal shunts were included, except for a patient with an early dense opacification of the right portal vein due to an obvious arterioportal shunting.

Statistical Analysis
Alternative-free-response ROC (AFROC) curves were generated by using ROCKIT 0.9B software (Metz CE) for each image set and for each observer [16]. Unlike the conventional ROC method, which allows only one response per image, the AFROC method enables an observer to analyze the responses for all the lesions, and all 102 foci of hypervascular HCC were analyzed in this study. The area under each curve (A1) indicated the overall diagnostic accuracy of the image sets and observers. Sensitivity and PPV for each image set and for each observer were calculated using those lesions with a confidence level of 3 or 4 as true-positive lesions. The mean values of A1, sensitivity, and PPV were compared among the four image sets using one-way analysis of variance followed by Tukey's multiple-comparison test. A p value of less than 0.05 was considered significant. The interobserver variability for lesion detection with each image set was assessed with kappa statistics. A kappa value of 0.01–0.20 was considered slight agreement, of 0.21–0.40 was considered fair, of 0.41–0.60 was considered moderate, of 0.61–0.80 was considered substantial, and of 0.81–1.0 was considered almost perfect.

Results

Top Abstract Introduction Materials and Methods Results Discussion References

 
All 31 patients could sustain the 25.2-sec (3 times of 8.4 sec) breath-hold during the triple arterial phase imaging, and those three dynamic images were of high quality (Figs. 1A, 1B, 1C, 1D, 1E, 1F, 1G, 1H, 1I, and 1J). The individual observers' and mean A1 values of each image set are shown in Table 2. The mean A1 values were significantly greater for Sets 2 and 4 than for Sets 1 and 3. The individual observers' and mean sensitivities of each image set are shown in Table 3. The mean sensitivity was also significantly greater for Sets 2 and 4 than for Sets 1 and 3. There was no significant difference in mean A1 values and mean sensitivities between Sets 2 and 4. The individual observers' and mean PPVs are shown in Table 4. Although the mean PPV tended to be greater for Sets 2 and 4 than for Sets 1 and 3, no significant difference was observed among the four image sets by one-way analysis of variance. The kappa values between each pair of the four observers for each image set are shown in Table 5. All values indicated a fair or moderate degree of agreement.

View larger version (138K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —53-year-old man with solitary hepatocellular carcinoma. All MR images shown were obtained using sensitivity encoding technique. Transverse unenhanced T1-weighted fast-field-echo MR image (TR/TE/flip angle, 168/4.6/70) shows hypointense tumor measuring 45 mm in diameter in segment VII.

View larger version (116K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —53-year-old man with solitary hepatocellular carcinoma. All MR images shown were obtained using sensitivity encoding technique. Transverse gadolinium-enhanced early, middle, and late arterial phase T1-weighted fast-field-echo MR images (TR/TE/flip angle, 168/4.6/70) show early enhancement of tumor, which is most apparently observed in middle arterial phase image (C).

View larger version (131K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C. —53-year-old man with solitary hepatocellular carcinoma. All MR images shown were obtained using sensitivity encoding technique. Transverse gadolinium-enhanced early, middle, and late arterial phase T1-weighted fast-field-echo MR images (TR/TE/flip angle, 168/4.6/70) show early enhancement of tumor, which is most apparently observed in middle arterial phase image (C).

View larger version (128K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1D. —53-year-old man with solitary hepatocellular carcinoma. All MR images shown were obtained using sensitivity encoding technique. Transverse gadolinium-enhanced early, middle, and late arterial phase T1-weighted fast-field-echo MR images (TR/TE/flip angle, 168/4.6/70) show early enhancement of tumor, which is most apparently observed in middle arterial phase image (C).

View larger version (131K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1E. —53-year-old man with solitary hepatocellular carcinoma. All MR images shown were obtained using sensitivity encoding technique. Transverse gadolinium-enhanced portal phase T1-weighted fast-field-echo MR image (TR/TE/flip angle, 168/4.6/70) shows tumor as sligthtly hypointense area.

View larger version (148K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1F. —53-year-old man with solitary hepatocellular carcinoma. All MR images shown were obtained using sensitivity encoding technique. Transverse gadolinium-enhanced equilibrium phase T1-weighted fast-field-echo MR image (TR/TE/flip angle, 168/4.6/70) shows tumor as hypointense area.

View larger version (165K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1G. —53-year-old man with solitary hepatocellular carcinoma. All MR images shown were obtained using sensitivity encoding technique. Transverse unenhanced T2-weighted turbo spin-echo MR image (TR/TE/flip angle, 1800/90) shows tumor as hyperintense area.

View larger version (155K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1H. —53-year-old man with solitary hepatocellular carcinoma. All MR images shown were obtained using sensitivity encoding technique. Transverse CT during hepatic arteriography image shows enhancement of tumor.

View larger version (143K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1I. —53-year-old man with solitary hepatocellular carcinoma. All MR images shown were obtained using sensitivity encoding technique. Transverse CT during arterial portography image shows portal perfusion defect due to tumor.

View larger version (131K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1J. —53-year-old man with solitary hepatocellular carcinoma. All MR images shown were obtained using sensitivity encoding technique. Transverse CT scan after chemoembolization shows dense accumulation of iodized oil in tumor.

The portal vein was opacified in 10 (33%), 30 (100%), and 30 (100%) of 30 patients on the early, middle, and late arterial phase images, respectively. The hepatic vein was opacified in none (0%), 12 (39%), and 23 (74%) of 31 patients on the early, middle, and late arterial phase images, respectively.

Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
The optimal arterial phase imaging of the liver can be defined as the imaging that enables observers to detect hypervascular HCCs most sensitively and correctly. Thus, to clarify the optimal arterial phase imaging, it may be necessary to compare the sensitivities and areas under the ROC curve of multiple arterial phase images obtained at different delay times in a single patient. Initially, Murakami et al. [11] performed a comparative study of early and late arterial phase imaging with MDCT. In their study, the early arterial phase imaging was started at the timing of peak aortic enhancement, defined by a test injection, and the late arterial phase imaging was started 15.5 sec afterward. The authors concluded that the late arterial phase imaging showed significantly greater sensitivity and area under the ROC curve than did those of the early arterial phase imaging. Ichikawa et al. [12] also determined the late arterial phase imaging to be superior to the early arterial phase imaging. In the present study, the early, middle, and late arterial phase images were acquired within a single breath-hold using the SENSE technique at 0, 8.4, and 16.8 sec, respectively, after the peak aortic enhancement. The mean values of A1 and sensitivity for Set 2, including the middle arterial phase imaging, were significantly greater than those for Sets 1 and 3, including the early and late arterial phase imaging, respectively. Hence, the middle arterial phase imaging with delay time of 8.4 sec was optimal for the detection of hypervascular HCCs. This optimal delay time was shorter than the delay time of 15.5 sec in the study by Murakami et al. This discrepancy of delay times between MDCT and MRI could result from the difference in the duration of contrast material injection. In their study, the mean volume of 114 mL of iodine contrast material was injected at a rate of 5 mL/sec; thus, the mean duration of contrast material injection was 22.8 sec. In our study, a fixed dose of 14 mL of gadolinium was injected at a rate of 2.5 mL/sec; thus, the duration of gadolinium injection was 5.6 sec, or less than one-fourth of that in the study by Murakami et al. Even if the onset of the optimal arterial phase were simultaneous between MDCT and MRI, the arterial perfusion of contrast material would cease much earlier on MRI than on MDCT. The late arterial phase MRI therefore might be too late to qualify as an optimal arterial phase imaging.

Kanematsu et al. [17] recently reported a prospective randomized trial to optimize the imaging delay for hepatic arterial and portal venous phase MRI. They concluded that the optimal arterial phase imaging could be obtained if the k-space was centered at 10–15 sec after the arrival of contrast material in the abdominal aorta. Their definition of the optimal arterial phase (e.g., intense splenic enhancement with the moiré pattern without intense hepatic enhancement) was less direct than was ours; however, their results were well in accord with ours. Taking into account the acquisition time of 8.4 sec for a single-phase imaging in our study, the center of the k-space was acquired at 12.6 sec after the peak aortic enhancement for the optimal middle arterial phase imaging, because the k-space was filled in a linear order in the present imaging sequence. Similarly, if the k-space trajectory is linear, the delay time of the optimal arterial phase imaging is determined by the following formula:

where DT is delay time after the peak aortic enhancement and AT is acquisition time of a single-phase imaging. In addition to determining the delay time, we evaluated the vascular appearance to characterize the optimal arterial phase imaging. According to our results, the portal vein was opacified in all of the patients and the hepatic vein in 39% on the optimal middle arterial phase imaging. Hence, the optimal arterial phase imaging can be characterized as the imaging where the portal vein is opacified but the hepatic vein either is not or is only slightly opacified.

It is controversial whether multiple arterial phase imaging is necessary to detect HCCs. Murakami et al. [11] emphasized that the double arterial phase imaging with MDCT showed superior sensitivity and area under the ROC curve compared with those of the late arterial phase imaging alone, because of the decrease in false-positive findings, caused especially by arterioportal shunts. In contrast, Ichikawa et al. [12] concluded that there was no significant difference in sensitivity and area under the ROC curve between the double arterial and the late arterial phase imaging alone. As Ichikawa had, we observed no significant difference in sensitivity and A1 value between Sets 2 and 4, which included the middle arterial phase imaging alone and the whole triple arterial phase imaging, respectively. Thus, we believe that the single optimal arterial phase is enough to detect HCCs on MRI. This does not mean, however, that the acceleration of acquisition time with a parallel imaging technique is no longer necessary, because the duration of the optimal arterial phase is quite short. Kopka et al. [15] reported the duration of the optimal arterial phase to be 7–19 sec (mean, 12.2 sec) using helical CT. The duration of the optimal arterial phase for dynamic MRI should be much shorter than that of CT, because the duration of the contrast material injection is much shorter. This speculation also is supported by the fact that the difference in the delay time of only 8.4 sec made a significant difference in the sensitivities and A1 values in our study. If a longer acquisition time were used without the SENSE technique, the contrast between hypervascular HCCs and liver parenchyma would be averaged and would decrease, resulting in poorer diagnostic accuracy. Yoshioka et al. [13] compared the double arterial phase MRI with SENSE and conventional dynamic MRI without SENSE among different patient populations and concluded that the double arterial imaging showed greater sensitivity and PPV than did conventional single arterial MRI.

There were some limitations in our study. First, the gold standard for the diagnosis of HCCs primarily was based on imaging. In previous studies, all lesions except those confirmed by biopsy were diagnosed by the combination of CTAP, CTHA, and iodized-oil CT. The combination of these techniques was reported to enable the depiction of hypervascular HCC with an accuracy approaching 100% [11]. Second, we did not perform any quantitative analyses. Takahashi et al. [14] had already performed a quantitative analysis of triple arterial phase dynamic MRI. They concluded that the peak enhancement of HCCs was observed on the second or the third arterial phase imaging, and that the signal-to-noise ratio of HCC and the contrast-to-noise ratio of HCC versus liver parenchyma tended to be highest on the second arterial phase imaging. Their results were well in accord with ours. Third, the through-plane resolution was 8–9 mm with intersection gaps. These extremely asymmetric voxels in the present study influenced the evaluation of small nodules under 8–9 mm in diameter, which shared the voxel with background tissue and were partially volumed. Dobritz et al. [18] reported the usefulness of 3D dynamic MRI of the liver with a parallel imaging technique. Further evaluation is needed to clarify the usefulness of this technique for detecting small lesions.

In conclusion, middle arterial phase imaging with a delay time of 8.4 sec after the peak aortic enhancement is more effective for the detection of hypervascular HCCs than early and late arterial phase imaging. The optimal acquisition timing of the center of the k space was 12.6 sec after the peak aortic enhancement. In addition, the optimal middle arterial phase imaging alone showed sensitivity and diagnostic accuracy similar to that of the whole triple arterial phase imaging.

References

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