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1 Clinical Laboratory, Yokohama City University School of Medicine, 3-9 Fukuura,
Kanazawa-ku, Yokohama 236-0004, Japan.
2 Third Department of Internal Medicine, Yokohama City University School of
Medicine, Yokohama 236-0004, Japan.
3 Second Department of Surgery, Yokohama City University School of Medicine,
Yokohama 236-0004, Japan.
4 Gastroenterological Center, Yokohama City University Medical Center, Yokohama,
232-0024, Japan.
Received April 22, 2002;
accepted after revision June 11, 2002.
Address correspondence to K. Numata.
Abstract
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SUBJECTS AND METHODS. We examined 30 patients with 56 hepatocellular carcinomas using real-time contrast-enhanced harmonic gray-scale sonography after injection of a galactose—palmitic acid contrast agent and compared the results with the findings of contrast-enhanced helical CT. We performed percutaneous ablation therapy guided by this modality for treatment of viable hepatocellular carcinoma lesions that could not be detected using conventional sonography.
RESULTS. High detection rates of viable hepatocellular carcinoma lesions were obtained using real-time contrast-enhanced harmonic gray-scale sonography (52/56 lesions, 93%); these rates were comparable to those of helical CT (54/56 lesions, 96%). Nine (90%) of the 10 lesions that were not detected on conventional sonography but were depicted on real-time contrast-enhanced harmonic gray-scale sonography (incomplete local treatment, n = 4; small new lesion, n = 6) were successfully treated with percutaneous ablation therapy guided by this method.
CONCLUSION. Real-time contrast-enhanced harmonic gray-scale sonography improved the sensitivity for the detection of viable hepatocellular carcinoma lesions. Percutaneous ablation therapy guided by this modality may be useful in patients with hypervascular hepatocellular carcinoma lesions that cannot be detected using conventional sonography.
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Recent improvements in spatial and contrast resolution have made it possible to evaluate the viability of hepatocellular carcinoma with a higher frame rate (seven frames per second) compared with the previous mode. Although both the new and previous modes are based on phase-inversion technology, this new contrast mode can be used not only to depict bubble disruption, but also to detect flow motion by deliberately adjusting the time interval between the transmission pulses. Therefore, even when not much contrast agent is left in the blood flow, this new mode still detects a sufficient flow signal. Accordingly, with this new contrast mode, we could identify advanced hepatocellular carcinoma lesions as hypervascular enhancement in the arterial phase at a high frame rate. This real-time observation made it possible to detect some hepatocellular carcinoma lesions not detected on conventional sonography. We could treat these small viable hepatocellular carcinoma lesions under guidance with this novel real-time contrast-enhanced harmonic gray-scale sonography.
In this study, we evaluated the detectability of tumor viability in hepatocellular carcinoma lesions using a novel contrast-enhanced wideband harmonic gray-scale sonography technique at a high frame rate (seven frames per second) and compared the results with the findings of helical CT. We also evaluated the usefulness of real-time percutaneous ablation therapy under guidance with this method for patients with small hypervascular hepatocellular carcinoma lesions not detected on conventional sonography.
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In the 12 patients who were not treated previously, 11 patients with 15 hepatocellular carcinoma lesions were diagnosed after aspiration biopsy. The remaining patient with one lesion was diagnosed on the basis of vascular findings on CT during hepatic arteriography and during arterial portography. Eighteen patients with 40 nodules had recurrent hypervascular hepatocellular carcinoma lesions previously diagnosed after biopsy. Aspiration biopsies were performed with a 21-gauge fine needle (Sonopsy; Hakko, Tokyo, Japan) under conventional sonographic guidance. The size of the hepatic lesions was assessed on real-time contrast-enhanced harmonic gray-scale sonography or helical CT. The maximal diameter of the tumors ranged from 6 to 48 mm with a mean maximal diameter of 21 ± 9 mm (± SD). All patients had cirrhosis, and the diagnosis was made histologically, clinically, or both. The causes of the cirrhosis were alcohol (n = 2); hepatitis B (n = 2); hepatitis C (n = 24); and non-B, non-C hepatitis (n = 2). According to Child's classification [15], 11 patients had class A cirrhosis, 12 had class B, and seven had class C. Informed consent was obtained from all patients.
Real-Time Contrast-Enhanced Harmonic Gray-Scale Sonography
Real-time contrast-enhanced harmonic gray-scale sonography was performed
with a Sonoline Elegra (Siemens Medical Systems, Issaquah, WA) with a 3.5-MHz
convex probe. First, we examined the detection of hepatocellular carcinoma
lesions using native tissue harmonic gray-scale imaging (transmit, 1.6, 1.8,
or 2.0 MHz; receive, 3.2, 3.6, or 4.0 MHz, respectively) (Figs.
1B,
2A,
3A). In this study, we
considered these imaging protocols to be conventional sonography.
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After IV bolus injection of half a vial of the 300 mg/mL concentration of galactose—palmitic acid mixture contrast medium (Levovist; Schering, Berlin, Germany), the liver was scanned using real-time contrast-enhanced harmonic gray-scale sonography (transmit, 2.8 MHz; receive, 5.6 MHz) at five—13 frames per second. We usually used seven frames per second. The transmission power was 100%, and the mechanical index values were 1.0-1.6. The focus position was just below the bottom of the tumor. If the tumor could not be detected on conventional sonography, we set the focus position at the middle portion of the liver. Levovist is a suspension of galactose (99.9%) stabilized with 0.1% palmitic acid. A 3.5-mL dose of this agent was injected at 0.5 mL/sec via a 22-gauge cannula placed in an antecubital vein. After a bolus injection of Levovist, 5% glucose was continuously infused at 5 mL/min. The patients were asked to inhale gently and then hold their breath for approximately 30 sec (20-50 sec after contrast medium injection) while the tumor vessels and tumor enhancement were examined (observation of the arterial phase) (Figs. 1C, 2B, 3C).
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During the arterial phase, if the tumor enhancement could not be seen, we moved the focus position quickly from the middle portion of the liver to the suitable portion for obtaining the hypervascular enhancement of the tumor.
After observation of the arterial phase, we froze the image. We then reviewed the images frame by frame from cine loop memories and stored them on magnetooptic disks. This procedure took approximately 15-35 sec (mean, 25 sec). We used this time to allow the contrast agent to pool in the hepatic parenchyma. We scanned the whole tumor and observed tumor enhancement 60-120 sec after injection of the contrast agent while the patients held his or her breath for a few seconds (observation of the portal phase). We subsequently froze the image again. We also reviewed these images on a frame-by-frame basis with a cine loop and stored them on magnetooptic disks for hard-copy printing.
Finally, 4 min after injection of the contrast agent, we examined the tumor for presence or absence of contrast agent in a sweep scan (observation of the late phase). If the patient had more than one lesion, the same procedure was repeated after another injection of the contrast agent. The full examinations were recorded on S-VHS videotape. Before treatment, the intratumoral vascularity was analyzed. We evaluated the images for the presence of intratumoral vessels during the arterial phase. Lesions were judged to exhibit hypervascular enhancement if their enhancement was much greater than that of the surrounding liver parenchyma during the arterial phase. Hypervascular enhancement was further subdivided into homogeneous and heterogeneous patterns of enhancement according to findings in both the arterial and portal phases. The enhancement pattern of the lesion in the late phase relative to the enhancement pattern in the surrounding liver parenchyma was subdivided into perfusion defect and residual enhancement. Findings were evaluated subjectively by two sonographers who were unaware of the findings of contrast-enhanced helical CT.
Helical CT
Dual-phase helical CT was performed in all patients with a Proceed SE
system (General Electric Medical Systems, Milwaukee, WI). First, an unenhanced
helical sequence through the liver was performed. Next, after IV infusion of
100 mL of iohexol (Omnipaque; Sanofi Winthrop Pharmaceuticals, New York, NY)
into an antecubital vein at a rate of 3 mL/sec, an arterial phase sequence was
performed after a delay of 25 sec, followed by a portal venous phase sequence
beginning 80 sec after starting the contrast medium infusion. All images were
obtained in helical mode with 7- or 10-mm collimation and a table-feed speed
of 7 or 10 mm/sec. Images were reconstructed at 7- or 10-mm intervals.
Findings were evaluated subjectively by two observers who were unaware of the
findings of the real-time contrast-enhanced harmonic gray-scale sonography. We
considered helical CT as the gold standard. When the remaining iodized oil
masked the enhancement of hepatocellular carcinoma lesions, we performed
CO2-enhanced sonography and considered this modality to be the gold
standard [14].
Percutaneous Ablation Therapy Guided by Real-Time Contrast-Enhanced
Harmonic Gray-Scale Sonography
We used a real-time scanner with 3.5-MHz convex probes (Sonoline Elegra;
Siemens Medical Systems) and a lateral attachable apparatus for needle
guidance (Universal Needle Guide Kit S; Siemens Medical Systems). Under
guidance with this modality, we targeted viable hepatocellular carcinoma
lesions, namely, those displaying, hypervascular enhancement with intratumoral
vessels 20-180 sec after injection of contrast agents (Figs.
2C and
3C). We promptly inserted a
15- or 20-cm-long, 21-gauge puncture needle with a closed conical tip and
three terminal side holes (PEIT needle; Hakko) or a 20-cm-long, 17-gauge,
radiofrequency electrode with a 2- or 3-cm-long exposed metallic tip
(Cool-tip; Radionics, Burlington, MA) into this lesion while the patient held
his or her breath for a few seconds. We confirmed that the PEIT needle or
radiofrequency ablation electrode was positioned correctly in the lesion, and
then we injected 99.5% absolute ethyl alcohol
(Fig. 1D) or performed
radiofrequency ablation (Fig.
2C).
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Percutaneous ethanol injection therapy guided by real-time contrast-enhanced harmonic gray-scale sonography was performed at intervals of once or twice a week. In one ethanol injection treatment session, we commonly used one or more PEIT needles, and ethanol was injected into the tumor at one or more locations until the lesion was completely filled. Immediately after ethanol injection or radiofrequency ablation, we again evaluated the absence or presence of residual viable lesions using real-time contrast-enhanced harmonic gray-scale sonography after injection of half a vial of Levovist. If residual intratumoral vessels were observed in the arterial phase, we inserted an additional PEIT needle into them or we repositioned the tip of the radiofrequency ablation electrode. When residual intratumoral vessels were not observed in the arterial phase, we observed the absence or presence of hypervascular enhancement in the portal phase of real-time contrast-enhanced harmonic gray-scale sonography.
When hypervascular areas were observed in the tumor, we considered them to be residual hepatocellular carcinoma lesions. When the treated lesion showed a nonenhancing area in the portal phase and this area covered more than the hypervascular enhancement seen in the arterial or portal phase of real-time contrast-enhanced harmonic gray-scale sonography before treatment, we finished the treatment (Figs. 2D and 3D). However, high echoic changes caused by these treatments made acoustic shadows behind the treated area and disturbed accurate diagnosis of adequate tumor necrosis. Therefore, 1 week after the last treatment, we evaluated the adequate tumor necrosis in the lesion using this technique (Fig. 3E). When a perfusion defect with an oval or round shape and distinct margins was observed in the portal phase, we recognized adequate tumor necrosis of the lesion [8] and we finished treating the patient.
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Serum 
-Fetoprotein Levels
Serum -fetoprotein levels (normal, <7 ng/mL) were measured before
and after treatment. Before therapy, serum -fetoprotein levels ranged
from 4 to 13,406 ng/mL (mean, 1114 ng/mL).
Statistical Analysis
Numeric data were expressed as means ± SDs. Group data were compared
with a one-way analysis of variance. Differences within one group were
evaluated by the paired t-test. Relationships between nominal
variables and rates were analyzed by the chi-square test. A p value
of less than 0.05 was considered statistically significant.
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The detection rates of viable portions of hepatocellular carcinoma lesions using the two modalities are shown in Table 1. Helical CT detected two more lesions (3%) than real-time contrast-enhanced harmonic gray-scale sonography, but the difference in detection between the two modalities was not significant.
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Conventional sonography detected 47 (84%) of 56 hepatocellular carcinoma lesions. Real-time contrast-enhanced harmonic gray-scale sonography detected six additional lesions (primary detected lesion, n = 1; recurrent new lesions, n = 5) and one lesion with incomplete local treatment that were not detected on conventional sonography. Real-time contrast-enhanced harmonic gray-scale sonography was a more sensitive means of detecting hepatocellular carcinoma lesions than was conventional sonography (p < 0.05 using chisquare test). This method also detected viable portions in three lesions with incomplete local treatment that could not be distinguished on conventional sonography. Therefore, 10 viable hepatocellular carcinoma lesions that were not recognized as viable lesions on conventional sonography were shown to be hypervascular on real-time contrast-enhanced harmonic gray-scale sonography.
Seven of these 10 lesions were initially detected through homogeneous enhancement with intratumoral vessels in the arterial phase of real-time contrast-enhanced harmonic gray-scale sonography (Figs. 1C and 2B). The remaining three lesions were initially detected as perfusion defects by sweep scanning in the late phase and confirmed as homogeneous enhancement with intratumoral vessels in the arterial phase of real-time contrast-enhanced harmonic gray-scale sonography (Figs. 3B and 3C).
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In 44 lesions that were identified by conventional sonography, the treatments we performed included transcatheter arterial embolization (n = 6), percutaneous ethanol injection (n = 19), and radiofrequency ablation (n = 7); 12 lesions received no therapy. Two lesions not detected on real-time contrast-enhanced harmonic gray-scale sonography or on conventional sonography underwent transcatheter arterial embolization. In the remaining nine patients with 10 lesions that were not recognized as viable lesions on conventional sonography but were shown to be hypervascular on realtime contrast-enhanced harmonic gray-scale sonography, treatment was performed with percutaneous ablation therapy guided by real-time contrast-enhanced harmonic gray-scale sonography. The maximal diameters of these 10 lesions were 8-20 mm (mean maximal diameter, 14 ± 4 mm).
Percutaneous ablation therapy guided by real-time contrast-enhanced harmonic gray-scale sonography was performed in eight patients with nine recurrent tumors that were detected during follow-up and in the remaining one patient with one primary lesion. Seven lesions were successfully treated using percutaneous ethanol injection guided by real-time contrast-enhanced harmonic gray-scale sonography; the remaining two lesions were successfully treated using radiofrequency ablation therapy guided by real-time contrast-enhanced harmonic gray-scale sonography. Four of seven patients who underwent percutaneous ethanol injection guided by real-time contrast-enhanced harmonic gray-scale sonography were treated as outpatients (Figs. 1A,1B,1C,1D and 3A,3B,3C,3D,3E), and the remaining three underwent the procedure as inpatients. One or more treatment sessions were performed in each percutaneous ethanol injection treatment series. The total volume of ethanol injected during percutaneous ethanol injection therapy ranged from 2.2 to 18.6 mL (mean ± SD, 9.4 ± 5.4 mL), and the volume used in each session ranged from 1.4 to 5.8 mL (3.1 ± 1.3 mL).
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One week after percutaneous ablation therapy guided by real-time contrast-enhanced harmonic gray-scale sonography, all treated lesions showed a perfusion defect in the portal phase of real-time contrast-enhanced harmonic gray-scale sonography (Fig. 3E). Helical CT performed 1 week after treatment revealed no lesions with areas of high attenuation in the arterial phase.
Serum -fetoprotein levels were evaluated before and after the
percutaneous therapy procedures guided by real-time contrast-enhanced harmonic
gray-scale sonography in the six patients in whom serum levels were elevated
before treatment. Serum -fetoprotein levels decreased in all six
patients who showed adequate tumor necrosis on real-time contrast-enhanced
harmonic gray-scale sonography after therapy; levels after treatment returned
to normal (<7 ng/mL) in two patients, decreased to a slightly elevated
level in three patients (10-50 ng/mL), and decreased to levels greater than 50
ng/mL in the remaining patient.
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With the progression of cirrhosis, echo signals in the liver become heterogeneous, preventing the identification of some nodules on conventional sonography. When using conventional sonography, it has also been difficult to determine the residual viable portion of hepatocellular carcinoma after treatment with transcatheter arterial embolization, percutaneous ethanol injection, or both, because of the similar appearance of necrosis and viable tumor tissue [21, 22]. CO2-enhanced sonography can detect both the viable portion in treated percutaneous ethanol injection lesions and new hepatocellular carcinoma lesions that are not detected on conventional sonography. Recently, using CO2-enhanced sonography, we have shown that the recurrence of small new hepatocellular carcinoma lesions not detected on conventional sonography increased during follow-up after treatment. We have also evaluated the usefulness of CO2-enhanced sonography and percutaneous ethanol injection under CO2-enhanced sonography for the detection and treatment of the viable portion of the lesion and of small lesions not detected with conventional sonography in patients with unresectable hepatocellular carcinomas [14]. However, this method needs intraarterial CO2 injection.
In this study, we used a novel mode of real-time contrast-enhanced harmonic gray-scale sonography to detect viable hepatocellular carcinoma lesions that are not detected on conventional sonography. Using this contrast mode improved both spatial and contrast resolution, allowing the identification of viable hepatocellular carcinoma lesions as hypervascular enhancement with intratumoral vessels in the arterial phase at a high frame rate. We were able to detect viable hepatocellular carcinoma lesions not detected on conventional sonography, and we could treat these lesions in real time by percutaneous therapy under guidance with this modality. Improved sensitivity also made it possible for us to perform this examination after injection of a smaller volume of contrast agent compared with the volume needed with the previous mode.
To visualize tumor perfusion in our previous mode of contrast-enhanced wideband harmonic gray-scale sonography, we reduced bubble destruction and used a frame rate of two frames per second [7, 8], with which 30 (77%) of 39 lesions showed intratumoral vessels in the arterial phase. When we used the novel mode, 52 (93%) of 56 hepatocellular carcinoma lesions showed intratumoral vessels in the arterial phase. Clearer and more frequent visualization of intratumoral vessels was achieved when the frame rate was seven frames per second. This real-time observation of the arterial phase made the diagnosis of hepatocellular carcinoma easier when the lesion showed hypervascular enhancement with intratumoral vessels.
When we used the previous mode, we reported that contrast-enhanced wideband harmonic gray-scale sonography was useful for diagnosing the viability of hepatocellular carcinoma after treatment with transcatheter arterial embolization and was superior to helical CT for evaluating residual hepatocellular carcinoma because there was no limitation in perfusion of the image as a result of iodized oil deposition [8]. In patients in whom tumoral blood flow disappeared completely after transcatheter arterial embolization therapy or percutaneous ethanol injection, arterial inflow was not recognized in the arterial phase, and the hepatocellular carcinoma lesions showed no enhancement in the portal phase. Therefore, these hepatocellular carcinoma lesions that were not viable were recognized as perfusion defects with an oval or round shape and distinct margins in the portal phase. In contradistinction, residual hepatocellular carcinoma lesions were visualized in the portal phase as hypervascular areas in the tumor. Therefore, we could decide where to perform additional percutaneous ethanol injection. Observation of the portal phase was important to detect viable portions of hepatocellular carcinomas after treatment by transcatheter arterial embolization or percutaneous ethanol injection therapy. However, we could not perform percutaneous ablation therapies in real time because we could not observe the lesion at a high frame rate using the previous mode. Therefore, we had to treat these lesions under guidance with conventional sonography.
Using this novel mode of real-time contrast-enhanced harmonic gray-scale sonography, we could detect viable portions of hepatocellular carcinoma lesions precisely in the arterial phase and puncture the lesion under guidance with this method at a high frame rate. This real-time therapy may obviate ethanol injection or radiofrequency thermal ablation.
With sweep scanning in the late phase, real-time contrast-enhanced harmonic gray-scale sonography depicted 37 (71%) of the 52 hepatocellular carcinoma lesions as perfusion defects. This observation allows the detection of small hepatocellular carcinoma lesions that cannot be detected on conventional sonography. Fifteen (29%) of the 52 hepatocellular carcinoma lesions showed residual enhancement in the late phase. Large hypervascular hepatocellular carcinoma lesions showed residual enhancement in the late phase. We think this residual enhancement may be the result of the destruction of microbubbles of Levovist that flowed back again into the tumor vessels and their vascular spaces.
Our study has several limitations. First, when nodules are located deep below the skin surface, a corresponding reduction in the degree of sonographic signal attenuation occurs. The acoustic intensity may also be effectively reduced and become inadequate when the focus position is deep, resulting in less destruction of the microbubbles than expected. In this study, two nodules located at a depth of at least 10 cm from the skin surface were depicted as hypervascular on helical CT, whereas real-time contrast-enhanced harmonic gray-scale sonography showed no hypervascularity. Second, one lesion could not be treated using percutaneous ethanol injection guided by real-time contrast-enhanced harmonic gray-scale sonography. In this case, puncture of the tumor was impossible because the right portal vein was present on the convex probe puncture guideline. If a deeper angle of puncture could be achieved, we would be able to puncture the lesion while avoiding the portal vein. Improved attachable metallic devices for puncturing tumors are needed to treat these small lesions. We hope that the development of real-time contrast-enhanced harmonic gray-scale sonography using the sector type of probe will be achieved, because a deeper angle of the puncture guideline can be obtained with the sector type than with the convex type of probe. This development may make it possible to puncture small new lesions or residual lesions not detected on conventional sonography but detected on real-time contrast-enhanced harmonic gray-scale sonography.
In conclusion, real-time contrast-enhanced harmonic gray-scale sonography is a noninvasive procedure that can be performed on an outpatient basis. Percutaneous ablation therapeutic procedures guided by real-time contrast-enhanced harmonic gray-scale sonography can be used with outpatients because this method enables pinpoint puncture of the viable portion of hepatocellular carcinomas. However, we have performed this treatment in only a small number of cases, so we must examine a larger number of patients to evaluate the real utility of this treatment for patients with hepatocellular carcinoma lesions not detected on conventional sonography.
Acknowledgments
We thank Kanae Saito, Yoshiro Haruna, Yoshiro Okaya, Zuhua Mao, and
Christoph Simm of Siemens Ultrasound for providing technical advice, and
Kazuki Ito of Shizuoka General Hospital for providing additional
assistance.
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