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Ultrasonography |
1 From the Department of Radiology and Institute of Radiation Medicine, Seoul National University Hospital, 28, Yongon-dong, Chongno-gu, Seoul 110-744, South Korea. From the 1999 RSNA scientific assembly. Received September 7, 1999; revision requested October 14; revision received November 12; accepted November 16. Supported in part by a grant from the 1999 Korean Highly Advanced National Projects on the Development of Biomedical Engineering and Technology. Address correspondence to B.I.C. (e-mail: choibi@radcom.snu.ac.kr).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Twenty hepatic hemangiomas in 20 patients and 41 malignant hepatic tumors in 23 patients (33 metastases and eight HCCs) were evaluated with pulse-inversion harmonic US. US images were obtained before injection and every 10–15 seconds after injection of a 4-g bolus (300 mg/mL) of SH U 508A (a microbubble contrast agent) for 5 minutes. The contrast-enhancement patterns of 61 hepatic lesions were assessed.
RESULTS: Of 20 hemangiomas, 19 revealed peripheral enhancement, which was globular in 14 (70%) and rimlike in five (25%), with centripetal fill-in; the remaining one (5%) showed homogeneous enhancement. In 33 metastases, the enhancement was rimlike in 16 (48%), homogeneous in seven (21%), and stippled in two (6%); in the remaining eight metastases (24%), no enhancement was seen. Of eight HCCs, four (50%) showed homogeneous enhancement and the remaining four (50%) showed heterogeneous enhancement. Centripetal fill-in of lesions with intratumoral enhancement was not seen in any malignancy.
CONCLUSION: Pulse-inversion harmonic US with a microbubble contrast agent is potentially useful for the specific diagnosis of hemangiomas that demonstrate characteristic enhancement features.
Index terms: Angioma, gastrointestinal tract, 761.3194 • Liver neoplasms, 761.323 • Liver neoplasms, secondary, 761.3327, 761.3320 • Liver neoplasms, US, 761.12988, 761.323, 761.3327, 761.3320 • Ultrasound (US), contrast media, 761.12988 • Ultrasound (US), harmonic study • Ultrasound (US), technology, 761.12988
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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The use of microbubble agents can improve the detection and characterization of tumor vascularity in hepatic tumors at color or power Doppler US studies (4–12); however, there are several limitations in Doppler US studies with microbubble agents, such as "blooming" artifacts (13) and insensitivity to slow flow (4). Contrast agents greatly increase intratumoral Doppler ultrasound signals in hepatocellular carcinomas (HCCs) (5–9). In hemangiomas, however, color or power Doppler US show either no internal vascularity or sparse peripheral flow, even after injection of a microbubble contrast agent (4–6,10,11). This is probably due to the insensitivity of the Doppler method with 2–3-MHz Doppler carrier frequency to slow capillary flow within the hemangioma (4).
Recently, the pulse-inversion harmonic US technique was introduced. It is a technique used to display the amplitude of the harmonic signals that result from the nonlinear echoes. Rather than using frequency filtering only when receiving, with this method nonlinear propagation is used when transmitting, as well. Two identical pulses with reverse polarity are transmitted in the medium; adding the two resultant returned signals cancels the fundamental linear components and preserves the nonlinear harmonic components (14). Pulse-inversion harmonic US is presently a gray-scale mode; the effect is to simply brighten the gray-scale image.
Interval-delay scanning or a triggered imaging method (15–17) at pulse-inversion harmonic US with a microbubble contrast agent can provide strong gray-scale enhancement. In contrast with Doppler US studies, pulse-inversion harmonic US with the interval-delay scanning technique can depict signals from microbubbles in very slow flow without Doppler-related artifacts. We expected that pulse-inversion harmonic US with a microbubble contrast agent could effectively depict the typical enhancement patterns of various hepatic tumors. The purpose of this study was to evaluate contrast-enhancement patterns in hepatic hemangiomas, hepatic metastases, and HCCs at pulse-inversion harmonic US with a microbubble contrast agent.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Because dynamic contrast-enhanced study was possible in only one scanning plane, a representative section was selected in each patient before scanning. In seven patients with metastases, multiple lesions (two to six lesions) were included in one scanning plane; 25 lesions were examined in these seven patients. In the remaining 36 patients, one lesion was scanned in each patient. Thus, 20 hemangiomas, 33 metastases, and eight HCCs were included in our study.
The 20 hemangiomas were proved by means of two-phase (hepatic arterial and portal venous phases) contrast-enhanced spiral CT (n = 15), dynamic contrast-enhanced MR imaging (n = 5), and US follow-up that demonstrated no change in the lesion size for at least 6 months (n = 20). Metastases (15 patients with 33 lesions) were proved with percutaneous needle biopsy in all 15 patients; however, these patients underwent biopsy of only one lesion each. The remaining 18 lesions were considered to be metastases on the basis of CT findings that were similar to those of the histologically confirmed lesion in the same liver. The histologic diagnoses of the 33 metastases were pancreatic carcinoma (n = 14), colorectal carcinoma (n = 12), malignant stromal tumor of the duodenum (n = 3), breast carcinoma (n = 2), gastric carcinoma (n = 1), and islet cell carcinoma of the pancreas (n = 1). Eight patients had a diagnosis of HCC proved by means of clinical laboratory data (positive findings of hepatitis B or hepatitis C surface antigen and serum 
1-fetoprotein level greater than 100 µg/L), along with typical angiographic findings during transcatheter arterial chemoembolization.
All 23 patients with metastasis or HCC underwent contrast-enhanced spiral CT within 1–12 days of the contrast-enhanced pulse-inversion harmonic US examination. Among them, four patients with nine metastatic lesions (eight from pancreatic carcinoma and one from pancreatic islet cell carcinoma) and all eight patients with HCC underwent two-phase spiral CT; the remaining 11 patients with 24 metastatic lesions underwent single-phase (portal venous phase) spiral CT alone.
Imaging
The US contrast agent used in the present study, SH U 508A (Levovist; Schering, Berlin, Germany), is a suspension of galactose microparticles in sterile water. This agent has gained regulatory approval in many countries but had not gained regulatory approval in the United States at the time this article was written. The microbubbles (2–8 µm in diameter; mean diameter, 3 µm), which are stabilized in the microparticle suspension, can traverse the pulmonary capillary bed.
Before the US examination, this agent was prepared by shaking the SH U 508A granules with 11 mL of sterile distilled water for 5–10 seconds for injection. A milky suspension of galactose microparticles and microbubbles was created by disaggregation of the granules. After standing for 2 minutes for equilibration, SH U 508A was injected intravenously as a bolus in a 4-g dose at a concentration of 300 mg/mL, with a 10-mL normal saline flush, by using a 20- or 22-gauge peripheral intravenous cannula.
Pulse-inversion harmonic US was performed by one examiner (T.K.K.) with an ATL HDI 5000 unit (Advanced Technology Laboratories, Bothell, Wash) and a 2–5-MHz curved linear-array transducer. The acoustic power of pulse-inversion harmonic US was set at the default (maximal) setting. Before injection of the contrast agent, we chose a scanning plane that included the tumor and obtained a pulse-inversion harmonic US image. After injection of the contrast agent, we obtained serial pulse-inversion harmonic US images for 5 minutes. All images were obtained as static cine loops and not as part of a real-time examination. We performed interval-delay scanning with 10–15-second intervals: We froze the display between each scanning time and unfroze it for a very short period (including one or two frames) at each scanning time. During the entire scanning, we held the transducer still and unfroze during the same stage of the patient's respiration (inspiration or expiration) to keep the same scanning plane. The time delay from injection and the time at which the image was obtained were recorded. All images were stored digitally on the hard disk in the US scanner and were transferred to a personal computer.
Two-phase spiral CT examinations were performed with various spiral CT scanners. Each patient received 120 mL of nonionic contrast material (iopromide [Ultravist 370; Schering]) intravenously at a rate of 3 mL/sec. Hepatic arterial phase and portal venous phase scans were obtained 30 and 65 seconds, respectively, after the initiation of the injection of contrast material. Single-phase spiral CT scans were obtained 65 seconds after the initiation of the injection of contrast material with the same injection protocol.
MR imaging examinations were performed with a 1.0-T system (Magnetom Expert; Siemens Medical Systems, Erlangen, Germany). The imaging sequences included breath-hold T2-weighted turbo spin-echo imaging (3,500/138 [effective] [repetition time msec/effective echo time msec], and an echo train length of 29) and breath-hold precontrast and serial contrast-enhanced T1-weighted fast low-angle shot imaging (160/6.6 [repetition time msec/echo time msec], 70° flip angle) immediately and at 1, 3, and 5 minutes after injection of contrast material (Magnevist; Schering).
Analysis
US images were displayed on a computer screen and were evaluated by two readers (J.K.H., B.I.C.) who were blinded to the diagnosis of the tumors, with decisions made by means of consensus. CT and MR images were evaluated by one reader (H.S.H.) who was blinded to the diagnosis of the tumors and the US findings.
The reviewers determined the diameters and echogenicity of the tumors on nonenhanced US images. They also evaluated the pattern of contrast agent enhancement of each tumor. All observations of the enhancement patterns were totally subjective; no quantitative substantiation was performed. In pulse-inversion harmonic US, the contrast-enhancement pattern was determined by evaluating images obtained during the early phase of enhancement, which was typically 20–40 seconds after the injection of contrast agent, when the enhancement of the tumor had just commenced. The contrast-enhancement pattern on CT images was determined by evaluating the hepatic arterial phase images. In patients who underwent single-phase (portal venous phase) CT alone, the enhancement pattern was not evaluated. On MR images, the enhancement pattern was determined by evaluating images obtained immediately or 1 minute after injection of the contrast agent.
The enhancement patterns of the tumor were classified as peripheral globular (discontinuous ring of contrast-enhanced peripheral globules), rimlike (continuous ring of peripheral contrast agent enhancement), homogeneous, heterogeneous, stippled (tiny dotlike areas of enhancement distributed throughout the entire tumor), and no enhancement (Fig 1). In tumors with peripheral globular or rimlike enhancement, the presence of progressive centripetal fill-in was also determined. The enhancement patterns on US images were also correlated with the lesion size.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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The most common enhancement pattern at pulse-inversion harmonic US with SH U 508A was peripheral globular enhancement with progressive centripetal fill-in, which was found in 14 lesions (70%) (Fig 2). Rimlike enhancement with progressive centripetal fill-in was seen in five lesions (25%) (Fig 3). The progression of centripetal fill-in of lesions with intratumoral enhancement was seen as progressive enhancement from the tumor margin toward the tumor center over several image acquisitions and continued until 48–231 seconds (mean, 86 seconds) after injection. The remaining lesion (5%), which was 37 mm, had homogeneous enhancement (Table). Although the intensity of enhanced portions of the tumor diminished progressively for 78–149 seconds (mean, 107 seconds) after injection, the lesion continued to show some enhancement until 5 minutes after injection in all 20 lesions.
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Metastases
The tumor diameters as measured on US images were 10–114 mm (mean, 25 mm). Twenty-seven lesions were equal to or less than 30 mm, and the remaining six lesions were larger than 30 mm. The echogenicity compared with that of the adjacent liver parenchyma was low in 19 lesions, mixed in three lesions, and high in 11 lesions.
Intratumoral enhancement was seen in 25 lesions (12 patients) at pulse-inversion harmonic US with SH U 508A. The most frequent enhancement pattern was rimlike enhancement, which was seen in 16 lesions (eight patients) (Fig 4). Homogeneous enhancement and stippled enhancement were seen in seven lesions (four patients) and two lesions (one patient), respectively. One patient had lesions with rimlike enhancement and lesions with homogeneous enhancement. The remaining eight lesions (three patients) had no enhancement (Table).
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Among nine lesions (four patients) in which two-phase spiral CT was performed, eight lesions (three patients) from pancreatic carcinoma showed no enhancement during both the hepatic arterial and the portal venous phases; at pulse-inversion harmonic US, seven of these eight showed no enhancement, and one showed rimlike enhancement. The remaining one lesion (one patient) from islet cell carcinoma of the pancreas showed homogeneous enhancement on the hepatic arterial phase CT image and the pulse-inversion harmonic US image. There was no enhancement in any of the 24 lesions (11 patients) at single-phase (portal venous phase) CT alone.
Hepatocellular Carcinomas
The tumor diameters as measured on US images were 19–80 mm (mean, 40 mm). Three HCCs were equal to or less than 30 mm, and the remaining five were larger than 30 mm. The echogenicity compared with that of the adjacent liver parenchyma was low in four, mixed in three, and high in one lesion.
Of eight HCCs, four (50%) showed homogeneous enhancement and the remaining four (50%) showed heterogeneous enhancement at pulse-inversion harmonic US with SH U 508A. None of eight HCCs showed peripheral rimlike or globular enhancement in the early phase. Irregular linear structures that represent contrast-enhanced vessels were found within the tumor in three lesions (38%) (Fig 5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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It is now understood that the US field, if its peak pressure is sufficiently high, is capable of disrupting a bubble shell and hence destroying it (20,21). The effect from sudden loss of correlation due to the sudden disappearance of a reflector (ie, microbubble) has been referred to as stimulated acoustic emission (22). The disruption of the bubbles creates a transient but very strong echo that is rich in harmonics; however, it causes the bubble to disappear. Stimulated acoustic emission does not rely on the movement of the microbubble and can be observed equally well with stationary microbubbles. This fact can be exploited as a way of detecting microcirculation with very slow flow. Because signals from stimulated acoustic emission are highly nonlinear, they can be detected effectively with harmonic US. In harmonic US with a frequency-filtering approach, however, much information is likely to be lost because signals from stimulated acoustic emission are distributed in a broad spectrum of frequency. Pulse-inversion harmonic US is therefore highly advantageous for imaging nonlinear signals from stimulated acoustic emission, in that the broadband frequency information is preserved.
The blood in the microvasculature is, however, moving very slowly and has not had time to reperfuse the bed before the next US frame is created. It is therefore necessary to interrupt the scanning process for a sufficient time (interval-delay imaging) to allow the agent to wash into the capillary tissue (15–17). Each transmitted US pulse in interval-delay imaging will produce the best possible harmonic signals because it can be arranged to allow areas of slow flow to fill with intact microbubbles during the imaging pause. This transient response, a signal with high amplitude, is exploited highly effectively with pulse-inversion harmonic US.
The optimal interval delay between each US pulse is to our knowledge not known yet and may depend on the flow velocity in the vasculature in examined tissue. Burns et al (15) reported that the signals from normal liver increased with increasing interval delays of up to about 5 seconds in harmonic gray-scale US. However, this result may not be applied to the scanning of hepatic hemangiomas because the flow velocity in the capillary tissue has been known to be extremely slow (0.03–0.08 cm/sec) (23). For example, if the blood in the capillary tissue in a hemangioma moves at 0.05 cm/sec and the scanning section is 5 mm thick, it will take approximately 10 seconds for the blood to fully reperfuse the scanning section. Therefore, in the present study, interval delays of 10–15 seconds were used. Further studies in which different interval delays are compared in imaging hemangiomas are needed.
The peripheral globular or rimlike enhancement with progressive centripetal fill-in in hemangiomas was striking on the interval-delay pulse-inversion harmonic US scans obtained with a microbubble contrast agent. While this enhancement pattern was seen in 95% of hemangiomas, no malignant lesion showed this enhancement pattern. In six hemangiomas (30%), the pattern of enhancement on pulse-inversion harmonic US images was not identical with that on CT or MR images: rimlike (25%) or homogeneous (5%) enhancement on US images and peripheral globular enhancement on CT or MR images. This is probably due to the difference in the interval between image acquisition and injection of the contrast agent. Since we scanned the lesion intermittently, briefly appearing peripheral globular enhancement might be missed and rimlike or homogeneous enhancement might be depicted first instead.
In metastases, we found that the varied nature of the primary tumor results in different enhancement characteristics in metastatic tumors. The most common metastatic tumors, metastases from gastrointestinal adenocarcinomas, most frequently showed rimlike enhancement. Unlike in hemangiomas, rimlike enhancement in metastases was not accompanied by progressive centripetal fill-in.
HCCs showed homogeneous or heterogeneous enhancement. None of the malignancies with homogeneous or heterogeneous enhancement showed peripheral rimlike or globular enhancement in the early phase.
Because of the results of this study, we believe that the pattern of enhancement on pulse-inversion harmonic US images potentially has high sensitivity and specificity for the diagnosis of hemangioma. For accurate differentiation of hemangiomas from malignancies, it is very important to look for peripheral globular or rimlike enhancement in the early phase of contrast agent enhancement (typically 20–40 seconds after bolus injection of the contrast agent). Thereafter, one should observe progressive centripetal fill-in of contrast agent on successive scans to diagnose hemangioma.
This study is limited by the fact that the US observers could not be truly blinded to the diagnosis of the hepatic tumor because the baseline images may have shown typical appearances of the hepatic tumor. As compared with CT or MR imaging, the US technique used in this study has few limitations. The first limitation is that dynamic US scanning is possible in only one scanning plane. It is therefore not possible to characterize all lesions simultaneously in patients with multiple lesions. The second limitation is that interval-delay scanning in the same area is not easy for unskilled examiners. Sufficient practice of interval-delay scanning in the area that includes the tumor must be done before injection of the contrast agent for these examiners. On the other hand, US is superior to CT or MR imaging in that simple, immediate characterization of a newly detected focal hepatic lesion at US examination can be possible.
In summary, pulse-inversion harmonic US with SH U 508A is a useful imaging technique to evaluate dynamic contrast-enhancement patterns of various hepatic tumors. Since 95% of the hemangiomas showed peripheral globular or rimlike enhancement with progressive centripetal fill-in and malignant tumors did not show this enhancement pattern, this technique is potentially useful for the specific diagnosis of hemangiomas.
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, B.I.C.; study concepts and design, T.K.K.; definition of intellectual content, T.K.K., B.I.C.; literature research, T.K.K., B.I.C.; clinical studies, T.K.K.; data acquisition, T.K.K., H.S.H., S.H.P., S.G.M.; data analysis, B.I.C., J.K.H., H.S.H.; manuscript preparation, T.K.K.; manuscript editing, T.K.K., B.I.C.; manuscript review, B.I.C.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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J. H. Youk, J. M. Lee, and C. S. Kim Therapeutic Response Evaluation of Malignant Hepatic Masses Treated by Interventional Procedures With Contrast-Enhanced Agent Detection Imaging J. Ultrasound Med., September 1, 2003; 22(9): 911 - 920. [Abstract] [Full Text] [PDF]
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H. Maruyama, S. Matsutani, H. Saisho, Y. Mine, H. Yuki, and K. Miyata Extra-Low Acoustic Power Harmonic Images of the Liver With Perflutren: Novel Imaging for Real-Time Observation of Liver Perfusion J. Ultrasound Med., September 1, 2003; 22(9): 931 - 938. [Abstract] [Full Text] [PDF]
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Y. L. Wen, M. Kudo, R. Q. Zheng, Y. Minami, H. Chung, Y. Suetomi, H. Onda, M. Kitano, T. Kawasaki, and K. Maekawa Radiofrequency Ablation of Hepatocellular Carcinoma: Therapeutic Response Using Contrast-Enhanced Coded Phase-Inversion Harmonic Sonography Am. J. Roentgenol., July 1, 2003; 181(1): 57 - 63. [Abstract] [Full Text] [PDF]
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J Furuse, M Nagase, H Ishii, and M Yoshino Contrast enhancement patterns of hepatic tumours during the vascular phase using coded harmonic imaging and Levovist to differentiate hepatocellular carcinoma from other focal lesions Br. J. Radiol., June 1, 2003; 76(906): 385 - 392. [Abstract] [Full Text] [PDF]
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 J U Harrer, L Mayfrank, M Mull, and C Klotzsch Second harmonic imaging: a new ultrasound technique to assess human brain tumour perfusion J. Neurol. Neurosurg. Psychiatry, March 1, 2003; 74(3): 333 - 342. [Abstract] [Full Text] [PDF]
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M.-R. Orden, J. S. Jurvelin, and P. P. Kirkinen Kinetics of a US Contrast Agent in Benign and Malignant Adnexal Tumors Radiology, February 1, 2003; 226(2): 405 - 410. [Abstract] [Full Text] [PDF]
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A. von Herbay, C. Vogt, and D. Haussinger Pulse Inversion Sonography in the Early Phase of the Sonographic Contrast Agent Levovist: Differentiation Between Benign and Malignant Focal Liver Lesions J. Ultrasound Med., November 1, 2002; 21(11): 1191 - 1200. [Abstract] [Full Text] [PDF]
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T.-M. Chen, S.-N. Lu, J.-H. Wang, C.-H. Hung, and H.-D. Tung Relationship Between Flash Echo Gray Scale Imaging Features and Pathologic Findings in Hepatic Adenoma J. Ultrasound Med., July 1, 2002; 21(7): 821 - 824. [Full Text] [PDF]
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J. H. Kim, T. K. Kim, B. S. Kim, H. W. Eun, P. N. Kim, M.-G. Lee, and H. K. Ha Enhancement of Hepatic Hemangiomas With Levovist on Coded Harmonic Angiographic Ultrasonography J. Ultrasound Med., February 1, 2002; 21(2): 141 - 148. [Abstract] [Full Text] [PDF]
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B. I. Choi, A. Y. Kim, J. Y. Lee, K. W. Kim, K. H. Lee, T. K. Kim, and J. K. Han Hepatocellular Carcinoma: Contrast Enhancement With Levovist J. Ultrasound Med., January 1, 2002; 21(1): 77 - 84. [Abstract] [Full Text] [PDF]
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T. Albrecht, M. J. K. Blomley, S. R. Wilson, and P. N. Burns Characteristics of Hepatic Hemangiomas at Contrast-enhanced Harmonic US Drs Wilson and Burns respond: Radiology, July 1, 2001; 220(1): 269 - 270. [Full Text] [PDF]
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 M. J K Blomley, J. C Cooke, E. C Unger, M. J Monaghan, and D. O Cosgrove Science, medicine, and the future: Microbubble contrast agents: a new era in ultrasound BMJ, May 19, 2001; 322(7296): 1222 - 1225. [Full Text]
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H. Ding, M. Kudo, H. Onda, Y. Suetomi, Y. Minami, H. Chung, T. Kawasaki, and K. Maekawa Evaluation of Posttreatment Response of Hepatocellular Carcinoma with Contrast-enhanced Coded Phase-Inversion Harmonic US: Comparison with Dynamic CT Radiology, December 1, 2001; 221(3): 721 - 730. [Abstract] [Full Text] [PDF]
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M. J. Dill-Macky, P. N. Burns, K. Khalili, and S. R. Wilson Focal Hepatic Masses: Enhancement Patterns with SH U 508A and Pulse-Inversion US Radiology, January 1, 2002; 222(1): 95 - 102. [Abstract] [Full Text] [PDF]
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F. Forsberg, C. W. Piccoli, J.-B. Liu, N. M. Rawool, D. A. Merton, D. G. Mitchell, and B. B. Goldberg Hepatic Tumor Detection: MR Imaging and Conventional US versus Pulse-Inversion Harmonic US of NC100100 during Its Reticuloendothelial System-Specific Phase Radiology, March 1, 2002; 222(3): 824 - 829. [Abstract] [Full Text] [PDF]
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