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1
Department of Radiology, Medical College of Wisconsin, Froedtert Memorial
Lutheran Hospital, 9200 W. Wisconsin Ave., Milwaukee, WI 53226.
2
Diagnostic Imaging Associates, Mercy Hospital, 400 University Ave., Des
Moines, IA 50314.
Received December 10, 1999;
accepted after revision February 8, 2000.
Address correspondence to W. D. Foley.
Abstract
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MATERIALS AND METHODS. Two sequential acquisitions were performed during a single breath-hold followed by a third acquisition beginning 60 sec after injection. Injection-to-scan delay for the first acquisition was the individual patient's circulation time, which was determined by a preliminary mini bolus. The mean attenuation of the upper abdominal aorta, portal vein, and hepatic parenchyma were determined for each imaging pass in 20 patients with cirrhosis and 20 patients without cirrhosis. Tumor-to-liver contrast for hypervascular primary and metastatic neoplasm was evaluated in a different set of 16 cirrhotic patients and nine noncirrhotic patients. Three-dimensional CT arteriograms were obtained from first-pass data.
RESULTS. Three distinct circulatory phases (hepatic artery, portal vein inflow or late arterial, and hepatic venous) were seen in cirrhotic and noncirrhotic patients. Maximum tumor-to-liver contrast for hypervascular primary and metastatic neoplasm occurred during the second pass for both cirrhotic (p < 0.006) and noncirrhotic (p < 0.001) patients. A three-dimensional hepatic-mesenteric CT arteriogram of normal or anomalous hepatic vessels without venous overlay was obtained from first-pass data in all patients.
CONCLUSION. Rapid-sequence hepatic helical CT allows selection of the optimal time interval for hypervascular tumor detection. A new paradigm for rapid hepatic CT acquisition—namely, hepatic arterial, portal vein inflow, and hepatic venous phases—is recommended to replace hepatic artery dominant and portal venous phases.
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Hepatic circulation has two major components, arterial and portal venous, and a rapidly injected contrast bolus will opacify the liver in two stages, in an initial hepatic artery phase followed by a portal venous phase. Improved detectability of hypervascular neoplasms during the hepatic artery dominant phase is attributed to selective enhancement of prominent arterial neovasculature during the relatively short temporal window before subsequent hepatic enhancement via portal venous inflow of the contrast agent.
Multirow detector CT scanners have recently been introduced into clinical CT practice. Major attributes that are improved are the z-axis coverage speed and the longitudinal resolution. These improvements translate into rapid hepatic imaging using an image thicknesses comparable with or less than that used with a monoslice helical CT system.
This study was performed on a new multirow detector CT scanner (LightSpeed; General Electric Medical Systems, Milwaukee, WI). The aims of this study were twofold. First, the ability of a new injection-acquisition technique to separate three distinct circulatory phases (that is, hepatic artery, portal venous inflow, hepatic venous) was evaluated. Second, the optimal phase for detecting hypervascular neoplasms was determined.
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A mini bolus was administered (5 mL/sec for 4 sec), and axial scanning at the level of the celiac artery was performed to measure aortic and hepatic arterial contrast arrival time. The acquisition technique with the mini bolus was conventional: 1-sec axial scanning every 2 sec with scanning beginning 10 sec after the beginning of injection for a 20-sec acquisition interval (Fig. 1). A time-attenuation curve was constructed and time to aortic peak was determined. For the subsequent multipass helical acquisition, time to aortic peak became the start time for image acquisition. A contrast bolus of 60% iodinated contrast material was injected at a rate of 5 mL/sec for 30 sec for the multipass acquisition.
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Because the cephalad-caudal dimension of the average liver is 16 cm, a table speed of 15 mm per rotation (18.375 mm/sec) was used for the first two phases of helical acquisition. This table speed allows coverage of the average liver in 9 sec. For the first pass, a 2.5-mm image thickness was used, and for the second pass a 5-mm image thickness was used. For the first pass, a table speed per rotation of 15 mm, a beam collimation of 10 mm, and a detector collimation of 2.5 mm result in a pitch of 1.5 according to the conventional definition of pitch (table speed per rotation/beam collimation) and a pitch of 6 according to a modified definition of pitch (table speed per rotation/detector collimation). For the second pass, a table speed per rotation of 15 mm, a beam collimation of 20 mm, and a detector collimation of 5 mm result in a pitch of 0.75 according to the conventional definition and a pitch of 3 according to the modified definition. Both the first and second pass with an intergroup delay of 4 sec were accomplished during a single breathhold using a cephalad-to-caudal scan acquisition for the first pass and caudal-to-cephalad acquisition for the second pass (Fig. 2).
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The acquisition interval for the first pass and second pass varied from 6.5 sec for a 12-cm cephalad-caudal hepatic span and 12 sec for a 22-cm hepatic cephalad-caudal span. In each patient, hepatic cephalad-caudal span was determined either from a preliminary digital radiograph or, if necessary, from unenhanced axial scans.
After the first two passes, a third abdominal scan sequence was performed with a 22.5-cm per rotation table speed (28 cm/sec) using an image thickness of 5 mm obtained by data interpolation with a detector collimation of 3.75 mm. This third imaging pass began 60 sec after the beginning of contrast injection (Fig. 2).
The objectives of the multipass acquisition protocol were thin-section CT arteriography and hypervascular tumor detection with the first pass, hypervascular tumor detection with the second pass, and detection of hypovascular hepatic neoplasm and extrahepatic disease with the third pass. Water was used as the oral gastrointestinal contrast material to enable three-dimensional arteriography of the hepatic and mesenteric arterial system.
Circulatory Phase Separation
To test the ability of the multipass CT acquisition technique to separate
the hepatic arterial from the portal venous and the hepatic venous phases, a
group of 20 patients without cirrhosis and a group of 20 patients with
cirrhosis were retrospectively evaluated.
The cirrhotic patients were evaluated as potential transplant recipients or were undergoing surveillance studies for primary hepatocellular carcinoma. In these patients, cirrhosis was established by morphologic appearance and biopsy. This patient group comprised 16 men and four women ranging in age from 46 to 84 years (mean age, 52 years).
The noncirrhotic group comprised patients evaluated for suspected hypervascular metastatic hepatic neoplasms and patients with positive titers for hepatitis virus but without macroscopic or biopsy evidence of cirrhosis. These patients comprised 12 men and eight women ranging in age from 16 to 77 years (mean age, 54 years). No hypervascular primary or metastatic neoplasms were detected in this patient group.
None of the patients in the noncirrhotic or cirrhotic group had overt cardiorenal disease requiring medical therapy. Cirrhotic patients had portal systemic varices and splenomegaly and, in some patients, ascites.
Serial attenuation measurements of the aorta, portal vein, and liver were acquired. These measurements were acquired at the midpoint of each imaging pass at the level of the hepatic hilum. The aortic region of interest (ROI) occupied the full cross-sectional area of the opacified aortic lumen, and a circular ROI of the same dimensions was placed at one point in the left hepatic lobe and two points in the right hepatic lobe free of artifacts or enhanced vessels. The size of the ROI was determined in each individual patient by aortic dimensions and varied slightly among patients. A hepatic ROI at the midpoint of each of the three passes was computed from the average of these three measurements in each patient. The portal vein ROI was elliptic and obtained from the portal vein at the level of the hepatic hilum (Fig. 3).
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For both the noncirrhotic and cirrhotic groups, the mean attenuation values for each of the three structures at each selected time point were determined. Time-attenuation curves of the aorta, portal vein, and liver corresponding to the midpoints of each of the three passes were obtained. The significance of differences in vascular or hepatic enhancement between the two groups was determined by Student's t test.
Tumor-to-Liver Contrast
Sixteen cirrhotic patients with hypervascular primary neoplasm and nine
noncirrhotic patients with hypervascular hepatic neoplasm, both primary and
metastatic neoplasms in eight and solitary focal nodular hyperplasia in one,
were evaluated. These patients comprised a consecutive group of patients with
hypervascular hepatic tumors evaluated during the study period.
In the cirrhotic patient group, hepatocellular carcinoma was present in 15
patients and cholangiocarcinoma in one patient. Hepatocellular carcinoma was
multifocal in seven patients. Diagnosis of hepatocellular carcinoma was
established at percutaneous or intraoperative biopsy in 14 patients, and by
typical imaging appearances on dynamic CT in association with elevated
-fetoprotein level in one patient. In the cirrhotic patient with
cholangiocarcinoma, diagnosis was established by operative biopsy. In the
cirrhotic group, individual lesion size varied from 1.2 to 15 cm with a mean
of 3.0 cm. The number of lesions varied from one to more than 10 (two
patients) for an average of three lesions per patient. This patient group
comprised 14 men and two women ranging in age from 46 to 84 years (mean age,
67 years).
In the noncirrhotic patient group with primary and metastatic neoplasm, two patients had cholangiocarcinoma, four patients had metastatic carcinoid tumor, two patients had metastatic islet cell tumor, and one patient had focal nodular hyperplasia. Diagnosis of cholangiocarcinoma was established by operative biopsy in two patients, carcinoid tumor by operative biopsy in one patient and by serial enlargement of multifocal hepatic lesions with proven primary carcinoid in three patients, and islet cell tumor by operative biopsy in one patient and by interval enlargement of multifocal hepatic lesions in one patient with hypervascular primary pancreatic tumor. Diagnosis of focal nodular hyperplasia was established by typical CT appearances in a patient with no known primary tumor. In this noncirrhotic group, lesions ranged from 1 to 14 cm in diameter with a mean diameter of 5.3 cm. The number of lesions per patient varied from one to more than 10 (one patient).
Tumor-to-liver contrast was determined by difference in attenuation measurements from ROIs placed within the most enhanced portion of the neoplasm and the adjacent normal hepatic parenchyma. A single representative lesion was evaluated in each patient. ROI measurements from all tumors were obtained during each of the three imaging passes using an ROI identical in size and placement both in the neoplasm and adjacent liver (Fig. 4A,4B,4C).
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Tumor-to-liver contrast in Hounsfield units was determined for each hypervascular neoplasm during each of the three imaging passes in both the cirrhotic group with primary neoplasm and the noncirrhotic group with metastatic and primary neoplasm. The mean attenuation value of tumor-to-liver contrast during the first, second, and third passes in the cirrhotic group with hepatocellular carcinoma and the noncirrhotic group with hypervascular metastases were determined. Significance of differences was assessed using the Student's t test.
CT Angiography
From the first-pass hepatic imaging data with a 2.5-mm image thickness and
a 15-mm per rotation table speed, reconstructions with a 50% overlap were
generated and data were transmitted to an Advantage Windows workstation
(General Electric Medical Systems) to enable CT arteriography of the hepatic
and mesenteric arterial circulation. CT angiographic images were acquired
using a maximum-intensity-pixel, volume rendering, and multiplanar
reformation.
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In both the cirrhotic and noncirrhotic groups, the time axis of enhancement is normalized to the start point of acquisition—that is, the time to aortic peak as determined from the original mini bolus. In the noncirrhotic group, the time to aortic peak enhancement varied from 12 to 29 sec (mean, 19 sec) and in the cirrhotic group from 14 to 21 sec (mean, 18 sec). With time to aortic peak determined individually for each patient, each patient served as their own control in establishing an appropriate time point for the beginning of hepatic acquisition. Dependent on cephalad-caudal liver span, the midpoint of the first imaging pass varied from 3 sec for a 12-cm cephalad-caudal span to 6 sec for a 22-cm cephalad-caudal span. The double-pass acquisition for the short cephalad-caudal span of 12 cm was completed in 16 sec, whereas the second-pass acquisition for a 22-cm cephalad-caudal span occurred in 16-28 sec. Typical examples of triple-pass acquisition in a noncirrhotic patient (Fig. 6A,6B,6C) and a cirrhotic patient (Fig. 7A,7B,7C) are provided.
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Tumor-to-Liver Contrast
The difference in tumor-to-liver contrast between the second pass and first
and third imaging passes was significant for both patient groups: in the
cirrhotic group, the p value was less than 0.001, and in the
noncirrhotic group the p value was less than 0.006
(Fig. 8).
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The maximum tumor-to-liver contrast for all measured lesions occurred during the second pass. The same contrast behavior was observed for all hypervascular lesions in both the cirrhotic and the noncirrhotic groups. In all lesions, tumor-to-liver contrast decreased during the third-pass acquisition as compared with the second-pass acquisition (Figs. 9A,9B,9C and 10A,10B,10C). In six of 16 patients in the cirrhotic group, isoattenuation of lesions positively enhanced during the first- and second-pass acquisition occurred during the third-pass acquisition.
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In four of the seven patients in the noncirrhotic group, metastases that were hyperattenuating during the second acquisition pass became hypoattenuating to hepatic parenchyma during the third acquisition pass.
Presumed extrahepatic metastatic disease was noted in three of 16 patients with primary hepatocellular neoplasm in the cirrhotic group and in three of the nine patients with hypervascular neoplasm in the noncirrhotic group.
CT Angiography
CT angiography data were obtained in all patients with observed
hypervascular neoplasms in both the cirrhotic and noncirrhotic groups. CT
angiograms enabled detection of anomalous right and left hepatic arterial
branches (Fig. 11).
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Kopka et al. [7] used relatively arbitrary definitions of splenic enhancement, 10 H for the beginning of the hepatic arterial phase, and of hepatic enhancement, 20 H for the beginning of the portal venous phase. These researchers found that the arterial phase was 11-12 sec in duration and that CT scan acquisition timing was improved with an online bolus-tracking technique in comparison with arbitrary fixed scan delays. Bolus-tracking software individualizes injection-to-scan delay related to different patient circulation times. Kopka et al. did not discuss the visual separation of enhanced hepatic artery vessels from portal vein branches during the two acquisition phases.
Multirow detector CT scanners allow faster z-axis speed and improved longitudinal resolution, thus enabling faster hepatic CT acquisition and the capability for more imaging passes than can be achieved with the standard biphasic helical CT approach using a monoslice scanner. The current study shows that with careful initial timing of scanning to begin at the time of aortic arrival of the contrast bolus, three clear separate circulatory phases can be defined by triple-pass hepatic CT technique using the multirow detector scanner. The first pass is a hepatic arterial phase with either no or minimal admixture of enhanced portal venous blood. Minimal admixture can occur in patients with larger livers and longer acquisition times for each pass (e.g., hepatic cephalad—caudal span of 22 cm and an acquisition interval of 12 sec for each of the two initial passes). Although hypervascular tumor enhancement is evident on the first pass, the degree of enhancement is significantly improved on the second pass. In our study, lesion detectability was not influenced by detector collimation and image thickness because the minimum diameter and mean diameter of lesions in the cirrhotic group were 1.2 and 3.0 cm, respectively, and in the noncirrhotic group were 1.0 and 5.3 cm, respectively. We have termed the first pass the "hepatic arterial phase" and the second pass the "portal venous inflow phase" or the "late arterial phase." Both passes are included in the acquisition interval considered as the hepatic artery dominant phase during biphasic CT with a monoslice scanner.
Hypervascular hepatic neoplasms, either primary or secondary, are best delineated during the second pass—the late arterial or portal venous inflow phase. This presumably reflects the time interval for distribution of contrast-enhanced hepatic arterial blood into the tumor neovasculature and diffusion into the interstices of the tumor. The first pass (hepatic arterial phase) of the triple-pass acquisition technique provides a suitable imaging template for CT arteriography, whereas the second pass (portal venous inflow or late arterial phase) maximizes hypervascular tumor detection. Preoperative visualization of anomalous hepatic arterial branches is important in patients who are candidates for hepatic resection and cryoablation or arterial chemoembolization.
Larson et al. [8] evaluated gadolinium-enhanced hepatic MR imaging and found two separate early phases of hepatic enhancement, the hepatic arterial phase and the "sinusoidal phase." Although comparing the acquisition timing between the MR technique of Larson et al. and the triple-pass CT technique evaluated in this study is difficult, the described sinusoidal phase would appear comparable with the portal venous inflow, or the late arterial phase, of the triple-pass acquisition. Larson et al. also described improved detectability of hypervascular neoplasm during the sinusoidal phase as compared with the hepatic arterial phase.
The third pass of our acquisition technique began 60 sec after the beginning of the contrast injection. This corresponds in timing to the portal venous phase of a biphasic hepatic helical scan using a monoslice system. During this third pass, hepatic veins that have been unenhanced during the hepatic artery phase and portal venous inflow phase are enhanced. Because this finding corresponds in timing to conventional hepatic CT, it has been termed the "hepatic venous phase." Tumors that are hyperattenuating during the arterial phase and portal venous inflow phase may become isoattenuating or hypoattenuating during the hepatic phase (Fig. 4A,4B,4C). An alternative approach to selecting the timing of the hepatic phase would have been a preset time after the beginning of the first arterial phase imaging pass. This approach would have standardized the hepatic phase for each patient's circulation time.
The third pass is continued as a total abdominal survey, and depending on the clinical indication, imaging may be extended to an abdominal—pelvic study.
Multirow detector CT scanners allow hepatic imaging with thin image thicknesses timed to acquire data in distinct early arterial, portal venous inflow or late arterial, and hepatic venous phases. These different circulatory phases can only be separated by precisely timing the start of acquisition to the individual patient's circulation time. In our study, this was accomplished by administering a preliminary mini bolus. Bolus-tracking software is an alternative approach. Our study indicates that the late arterial or portal vein inflow phase is the optimal phase for detecting hypervascular primary and metastatic neoplasms. This phase is included only in the latter half of the hepatic artery dominant phase of a biphasic helical acquisition with a monoslice scanner. However, with this approach only half of the hepatic cephalad—caudal span will be imaged during the portal vein inflow phase when tumor-to-liver contrast is maximized. The utility of the early arterial phase is in providing a volume data set for CT arteriography of the hepatic and mesenteric circulation. This information is useful in patients who are candidates for surgical resection, surgical or percutaneous ablation therapy, or chemoembolization. The third imaging pass allows evaluation of isoattenuation or hypoattenuation of hypervascular lesions. In addition, in some patients, relatively hypovascular hepatocellular carcinomas and metastases from islet cell or carcinoid tumors may be detected only during this later acquisition pass. We have termed this phase the "hepatic venous phase" of a triple-pass acquisition technique. Using monoslice scanners, this phase has been termed the "portal venous phase," a relatively inaccurate description because portal venous enhancement is clearly evident on the hepatic artery dominant phase of a biphasic acquisition.
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J. K. Willmann, J. E. Roos, A. Platz, T. Pfammatter, P. R. Hilfiker, B. Marincek, and D. Weishaupt Multidetector CT: Detection of Active Hemorrhage in Patients with Blunt Abdominal Trauma Am. J. Roentgenol., August 1, 2002; 179(2): 437 - 444. [Abstract] [Full Text] [PDF]
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S. Kawata, T. Murakami, T. Kim, M. Hori, M. P. Federle, S. Kumano, E. Sugihara, S. Makino, H. Nakamura, and M. Kudo Multidetector CT: Diagnostic Impact of Slice Thickness on Detection of Hypervascular Hepatocellular Carcinoma Am. J. Roentgenol., July 1, 2002; 179(1): 61 - 66. [Abstract] [Full Text] [PDF]
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 W. D. Foley Special Focus Session: Multidetector CT: Abdominal Visceral Imaging RadioGraphics, May 1, 2002; 22(3): 701 - 719. [Abstract] [Full Text] [PDF]
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T. Kim, T. Murakami, M. Hori, M. Takamura, S. Takahashi, A. Okada, S. Kawata, M. Cruz, M. P. Federle, and H. Nakamura Small Hypervascular Hepatocellular Carcinoma Revealed by Double Arterial Phase CT Performed with Single Breath-Hold Scanning and Automatic Bolus Tracking Am. J. Roentgenol., April 1, 2002; 178(4): 899 - 904. [Abstract] [Full Text] [PDF]
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F. R. Verdun, A. Denys, J.-F. Valley, P. Schnyder, and R. A. Meuli Detection of Low-Contrast Objects: Experimental Comparison of Single- and Multi-Detector Row CT with a Phantom Radiology, March 21, 2002; (2002) 2232010810. [Abstract] [Full Text]
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D. S. Katz and M. Hon CT Angiography of the Lower Extremities and Aortoiliac System with a Multi-Detector Row Helical CT Scanner: Promise of New Opportunities Fulfilled Radiology, October 1, 2001; 221(1): 7 - 10. [Full Text] [PDF]
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E. K. Fishman From the RSNA Refresher Courses: CT Angiography: Clinical Applications in the Abdomen RadioGraphics, October 1, 2001; 21(90001): S3 - 16. [Abstract] [Full Text] [PDF]
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H. Ji, J. D. McTavish, K. J. Mortele, W. Wiesner, and P. R. Ros Hepatic Imaging with Multidetector CT RadioGraphics, October 1, 2001; 21(90001): S71 - 80. [Abstract] [Full Text] [PDF]
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K. Wong, E. K. Paulson, and R. C. Nelson Breath-hold Three-dimensional CT of the Liver with Multi-Detector Row Helical CT Radiology, April 1, 2001; 219(1): 75 - 79. [Abstract] [Full Text]
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V. Raptopoulos and P. M. Boiselle Multi-Detector Row Spiral CT Pulmonary Angiography: Comparison with Single-Detector Row Spiral CT Radiology, December 1, 2001; 221(3): 606 - 613. [Abstract] [Full Text] [PDF]
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S. Takahashi, T. Murakami, M. Takamura, T. Kim, M. Hori, Y. Narumi, H. Nakamura, and M. Kudo Multi-Detector Row Helical CT Angiography of Hepatic Vessels: Depiction with Dual-arterial Phase Acquisition during Single Breath Hold Radiology, January 1, 2002; 222(1): 81 - 88. [Abstract] [Full Text] [PDF]
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F. R. Verdun, A. Denys, J.-F. Valley, P. Schnyder, and R. A. Meuli Detection of Low-Contrast Objects: Experimental Comparison of Single- and Multi-Detector Row CT with a Phantom Radiology, May 1, 2002; 223(2): 426 - 431. [Abstract] [Full Text] [PDF]
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), portal vein
(
), and hepatic parenchyma (
) at midpoints of first, second, and
third imaging passes in both patient groups. Zero on time scale corresponds to
beginning of first-pass acquisition, which was determined separately in each
patient as time from beginning of injection to aortic peak on mini bolus
study. Noncirrhotic patients.
