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1 Department of Gastroenterology and Hepatology, Kinki University School of
Medicine, 377-2, Ohno-Higashi, Osaka-Sayama, Osaka 589-8511, Japan.
2 Present address: Department of Ultrasound, The Second Affiliated Hospital, Sun
Yat-sen University, 107 Yanjiangxi Rd., Guangzhou 510-120, China.
3 Present address: Department of Ultrasound, The Third Affiliated Hospital, Sun
Yat-sen University, Shipai, Guangzhou 510-630, China.
4 Abdominal Ultrasound Unit, Kinki University School of Medicine, Osaka-Sayama,
Osaka 589-8511, Japan.
Received October 9, 2002;
accepted after revision December 10, 2002.
Address correspondence to M. Kudo.
Abstract
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SUBJECTS AND METHODS. Sixty-seven patients with a total of 107 examinations on 91 hepatocellular carcinoma nodules underwent coded harmonic angio, a technique of coded phase-inversion harmonic sonography, using the IV microbubble contrast agent Levovist before and after percutaneous radiofrequency ablation. The intratumoral blood vessels and tumor parenchymal stain were detected in the early arterial phase and the late vascular phase, respectively. The results of contrast-enhanced imaging with coded harmonic angio were compared with those of three-phase dynamic CT.
RESULTS. Before treatment, all examined 107 hepatocellular carcinoma nodules were found to be hypervascular on contrast-enhanced imaging with coded harmonic angio. After radiofrequency ablation, contrast-enhanced coded harmonic angio detected persistent signal enhancement in 41 examined nodules (38.3%), whereas this technique showed no intratumoral enhancement in the remaining 66 (61.7%) examined nodules. Compared with dynamic CT, the sensitivity, specificity, and diagnostic accuracy of contrast-enhanced coded harmonic angio were 95.3%, 100%, and 98.1%, respectively. With contrast-enhanced coded harmonic angio, we found that it was difficult to identify the safety margin that can be detected on dynamic CT.
CONCLUSION. Contrast-enhanced imaging with coded harmonic angio may provide an alternative approach that has high diagnostic agreement with dynamic CT in assessing the therapeutic effect of radiofrequency ablation in hypervascular hepatocellular carcinomas, in spite of having limitations in identifying the safety margin.
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Because radiofrequency ablation is usually performed under the guidance of sonography [12–15], it would be preferable to evaluate the treatment response using sonographic techniques. The advances in IV sonographic contrast agents offer the potential for sonography to be used to distinguish viable tissue from ablated tumor [16, 17]. However, although contrast agents are used, conventional color Doppler sonography and power Doppler sonography can reveal only the viable tumor foci in treated hepatocellular carcinoma with low sensitivity [18, 19].
Many new sonographic techniques have been developed for using the signals from the microbubbles of contrast agents [6, 19–24]. Consequently, improvements have been made in depicting the intratumoral vascularity or assessing the therapeutic effects of nonsurgical treatments for liver tumors [21–25]. Phase- and pulse-inversion harmonic sonography is a recently developed technique that proved to be superior to second harmonic sonography and conventional color and power Doppler sonography for providing high-spatial resolution and no Doppler-related artifacts [26–28]. Coded harmonic angio software (General Electric Medical Systems, Milwaukee, WI) combines phase-inversion harmonic sonography with coded technologies that transmit a coded pulse sequence, decode the pulse sequence in receiving signals, and provide an increased detection of weak blood signals within the tumor.
In our study, we used the coded harmonic angio technique with the IV contrast agent Levovist (Schering, Berlin, Germany) to investigate the value of contrast-enhanced imaging with coded harmonic angio in assessing the therapeutic responses after percutaneous radiofrequency ablation in hepatocellular carcinomas.
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From November 1999 to March 2001, 87 patients with hepatocellular
carcinomas underwent sonographically guided percutaneous radiofrequency
ablation in our department. Of them, 12 patients with a history of treatment
with transcatheter arterial embolization or percutaneous microwave coagulation
therapy were excluded from this study, and eight patients whose tumors showed
hypovascularity before radiofrequency ablation by contrast-enhanced imaging
with coded harmonic angio were also excluded. The remaining 67 patients (47
men, 20 women; age range, 43–85 years; mean age, 66 years) formed the
population of this study. The sizes and number of the hepatocellular
carcinomas were established on the basis of sonographic findings. In 51 of the
67 patients, solitary tumors were studied in 32 patients. Two (n =
14) or three tumors (n = 5) were studied in 19 patients only before
and after the first session of radiofrequency ablation. In the remaining 16
patients, the hepatocellular carcinomas were studied before and after the
first and the second sessions of radiofrequency ablation. Thus, a total of 107
examinations of 91 tumor nodules were studied. The maximal diameter of the
tumors ranged from 1 to 5 cm (mean ± SD, 2.43 ± 1.06 cm). Of the
107 examined nodules, 90 were no larger than 3 cm, and the remaining 17 were
from 4 to 5 cm in maximal diameter. All patients had liver cirrhosis (64
patients had positive results for the hepatitis C antibody, and three patients
had positive results for the hepatitis B surface antigen). The levels of liver
dysfunction were categorized into Child-Pugh class A in 58 patients,
Child-Pugh class B in eight, and Child-Pugh class C in one. The diagnosis of
hepatocellular carcinoma was determined by sonographically guided biopsy
(n = 8) or on the basis of laboratory data, including findings of
hepatitis-related liver cirrhosis, elevated levels of 
-fetoprotein
(> 20 ng/mL; mean, 690 ng/mL), or prothrombin induced by vitamin K absence
(> 40 mAU/mL; mean, 1493 mAU/mL) with a remarkable rising trend; and
typical imaging findings on three-phase dynamic CT (n = 107), digital
subtraction angiography (n = 52), MR imaging (n = 59), CT
angiography (n = 27), or CT arterial portography (n = 27).
In this study, typical imaging findings for hepatocellular carcinoma included
high attenuation of the nodules on early phase dynamic CT or CT angiography,
low attenuation on delayed phase dynamic CT, perfusion defect on CT arterial
portography, early arterial supply, and dense tumor stain on digital
subtraction angiography, or high signal intensity on T2-weighted MR imaging
[24].
All patients had contraindications to surgery because of severe liver dysfunction, inappropriate location of the tumor, advanced age, associated diseases, or refusal to undergo the operation. This information was based on consensus agreement with the surgical department.
Imaging
Five to seven days before and after percutaneous radiofrequency ablation,
contrast-enhanced imaging with coded harmonic angio was performed for each
nodule of hepatocellular carcinoma using a LOGIQ 700 EXPERT unit (General
Electric Medical Systems) with a 2- to 4-MHz electrical curved array wideband
transducer. First, fundamental B-mode sonography was performed. An ideal plane
was chosen for clearly showing the tumor and the surrounding liver parenchyma.
Then coded harmonic angio mode was switched on, and we set the mechanical
index at 0.6–0.8 [24].
The pulse repetition frequency was set at 7 kHz. The dynamic range was set at
69–72 dB, and the gain was set at 40 dB with single focus at the middle
of the tumor. Ten seconds after administration of the contrast agent (when the
first signal from the microbubbles appeared in the liver), the patients were
required to hold their breath to ensure that we did not lose sight of the
targeted tumor and to diminish the motion artifact. In the early arterial
phase (10–40 sec after administration of Levovist), continuous imaging
with coded harmonic angio was performed for 20–30 sec on the ideal plane
with a gradual change of the plane to scan the entire tumor for showing blood
vessels in a real-time fashion (vessel image). Then, the still images were
saved to the hard disk of the machine by recalling them from the cine-loop
memory. In the late vascular phase (1–3 min after administration of
Levovist), automatic intermittent pulses (interval time, 2–3 sec) or
manual interval-delay imaging (sudden switching on of the coded harmonic angio
mode after a 5- to 10-sec freeze) was performed to show the tumor parenchymal
stain. A gradual change of the scanning plane was performed to observe the
whole tumor.
The IV sonographic contrast agent Levovist was used in this study. Levovist is a suspension of galactose in sterile water. The main components are 99.9% D-galactose and 0.1% palmitic acid. The suspension was prepared by vigorously shaking the powder with 5 mL of sterile water for 5–10 sec. After standing for 2 min for equilibrium and the dissolving of larger bubbles, the 7-mL suspension in a concentration of 400 mg/mL was administrated as a bolus through a 20-gauge cannula placed in the antecubital vein at a speed of 1 mL/sec and, soon after, flushed by 10 mL of normal saline. Injection of Levovist was used for each nodule. If more than one nodule was studied simultaneously, a different vial of Levovist was injected with an interval time no less than 10 min.
Three-phase dynamic CT was performed on all patients 5–7 days before and after radiofrequency ablation (the same time that contrast-enhanced imaging with coded harmonic angio was performed). A single-detector helical CT system (X-vigor, Toshiba Medical Systems, Tokyo, Japan) was used with 100 mL of iopamidol (Ioparmiron, Nihon Schering, Osaka, Japan). The iodine concentration of Ioparmiron is 370 mg/mL. After injection of the contrast agent at a rate of 3 mL/sec, repeated acquisitions were performed at 30, 60, and 180 sec to obtain images during the hepatic arterial, portal venous, and delayed phases, respectively. The scans were obtained through the liver in a craniocaudal direction with a 7-mm collimation, 7-mm/sec table speed (pitch 1.0) during a single breath-hold acquisition, and 7-mm reconstruction interval.
Therapeutic Technique
Radiofrequency ablation was performed using a radiofrequency generator and
a Le Veen needle (RTC 2000, RadioTherapeutics, Sunnyvale, CA). The emission
power, tissue impedance value, and treatment time were displayed on the
generator monitor. The needle has a 25-cm-long stainless steel shaft insulated
by a plastic membrane and eight or 10 retractable lateral hooks with maximal
exposed deployment of 2.0, 3.0, or 3.5 cm. A different deployment diameter was
chosen according to the maximal diameter and location of the tumor. Before the
procedure was started, a local anesthetic was administered with lidocaine,
along with an intramuscular injection of a sedative with the patient conscious
if necessary. Two dispersive pads, each with a 100-cm2 surface
area, were attached to the patient's thighs for grounding. The whole procedure
from the puncture of the needle to the end of the radiofrequency ablation was
performed under real-time guidance using the following sonography machines: a
PowerVision 8000 (Toshiba Medical Systems) with a convex array transducer or a
LOGIQ 700 EXPERT unit with a curved array transducer. For hepatocellular
carcinomas smaller than or equal to 3 cm in maximal diameter, the
radiofrequency needle was positioned at the center of the tumor. For those
that were 3–5 cm in maximal diameter, one session of radiofrequency
ablation comprised three complete procedures of ablation with the needle
positioned in the deep, middle, and superficial parts of the tumor. The
initial emission power was set at 30, 40, and 50 W, respectively, for needles
of 2.0, 3.0, and 3.5 cm in deployment diameter. Then, the emission power was
gradually increased to 60, 75, and 90 W, respectively. The radiofrequency
energy was applied for 12–15 min or automatically stopped when power
"rolloff" occurred.
If residual tumor was detected on dynamic CT or contrast-enhanced coded harmonic angio performed within 5–7 days after radiofrequency ablation, a further session of radiofrequency ablation was performed. Additional contrast-enhanced coded harmonic angio and dynamic CT were performed on only 16 hepatocellular carcinomas after the second session of radiofrequency ablation, using the same protocol described previously.
Imaging Analysis
The entire sonographic examination was recorded on videotape. The
videotapes were reviewed by at least three radiologists who had no knowledge
of the results of dynamic CT. On contrast-enhanced imaging with coded harmonic
angio, the presence of the intratumoral blood signals on either the vessel
image or the tumor parenchymal stain image was considered as hypervascular or
residual tumor due to inadequate treatment. In contrast, the absence of the
intratumoral blood signal was evaluated as hypovascular or complete response
to the treatment. Furthermore, if complete response of the tumor was obtained
and the edge of the tumor could be identified in the ablated area on the
B-mode image, an adequate safety margin of sufficient peripheral coagulated
area (≥ 5 mm from the edge of the tumor to the edge of the ablated area at
the entire tumor plane) [29]
was assessed to ensure adequate treatment of the tumor
(Fig. 1).
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Three-phase dynamic CT scans were interpreted by two other radiologists who had no knowledge of the results of contrast-enhanced coded harmonic angio. Compared with peripheral liver parenchyma, a high- or iso-attenuating mass on either arterial or portal phase CT was considered as viable tumor. Conversely, absence of tumor perfusion as manifested by low attenuation on three phases of dynamic CT was regarded as indicating hypovascularity or complete response to radiofrequency ablation. In addition, a safety margin was assessed in the tumors that showed hypovascularity after radiofrequency ablation. If the edge of the original tumor was recognized after radiofrequency ablation in comparison with the original CT scans, a distance that was no less than 5 mm from the edge of the tumor to the edge of the ablated area on all slices of dynamic CT where the tumor was present was defined as an adequate safety margin (Fig. 1).
When a discrepancy occurred among the interpreters, reevaluation and discussion were done for agreement.
The detectability of residual tumor using contrast-enhanced coded harmonic angio was compared with the detectability of the tumors using dynamic CT. The sensitivity and specificity of contrast-enhanced coded harmonic angio in detecting residual tumor were determined using dynamic CT as a gold standard. The detectability of the safety margin by contrast-enhanced coded harmonic angio was compared with that on dynamic CT. The chi-square test was used to analyze the data. A p value of less than 0.05 was defined to be a statistically significant difference.
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Contrast-enhanced coded harmonic angio showed residual tumor enhancement in 34 (37.4%) of 91 hepatocellular carcinomas after the first session of radiofrequency ablation (Figs. 2A, 2B, 2C, 2D, 2E, 2F). Of the 16 hepatocellular carcinomas also assessed after the second session of radiofrequency ablation, contrast-enhanced coded harmonic angio showed residual tumor enhancement in seven nodules (43.8%). Thus, contrast-enhanced coded harmonic angio showed residual tumor enhancement in 41 (38.3%) of the 107 examined hepatocellular carcinoma nodules. A greater conspicuity of these enhancing blood signals from residual tumor was seen on blood vessel images (40/41) obtained in the early arterial phase than on the interval-delay image obtained in the late vascular phase (38/41). All the 41 examined nodules were shown to have an enhancing portion of the viable tumor on arterial phase dynamic CT. The appearance of residual tumors shown on contrast-enhanced coded harmonic angio were consistent with that of enhancement on dynamic CT in all 41 examined nodules. Contrast-enhanced coded harmonic angio showed neither intratumoral blood vessels nor tumor parenchymal stain within the remaining 66 (61.7%) examined hepatocellular carcinomas, whereas dynamic CT showed an enhancing portion in two of them on the arterial and portal phase scans. Hence, the sensitivity, specificity, and accuracy of contrast-enhanced coded harmonic angio were 95.3%, 100%, and 98.1%, respectively. The positive predictive value by contrast-enhanced coded harmonic angio was 100%, and the negative predictive value was 97.0% for detecting residual tumor after percutaneous radiofrequency ablation in hepatocellular carcinoma.
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Of the 64 examined hepatocellular carcinoma nodules that showed complete response to the treatment on dynamic CT, a 5-mm-thick safety margin was found in 40 (62.5%, 40/64) on dynamic CT, but in only four of them (6.3%, 4/64) on contrast-enhanced coded harmonic angio (Figs. 3A, 3B, 3C, 3D). This finding was because of the difficulty in identifying the tumor margin in the ablated area on B-mode sonography. The ability to recognize a safety margin is significantly lower on contrast-enhanced imaging with coded harmonic angio (p < 0.0001) than dynamic CT.
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Because percutaneous radiofrequency ablation is usually performed under sonographic guidance [12–15, 18, 19], sonographic evaluation of the therapeutic response seems preferable. However, residual tumors after radiofrequency ablation are difficult to detect because internal blood flows are slow and the signals are weak. Conventional color Doppler sonography or power Doppler sonography were unable to provide enough information on the degree of tumor necrosis after ablation because of their low sensitivity to blood signals, especially those with low velocity [18, 19].
Recently, various IV contrast agents have been developed that use different gases or shells [16, 17]. Levovist is the most widely used microbubble contrast agent at the present time. The small size of the microbubbles of Levovist make it possible to enhance the blood signals in abdominal organs by IV injection. At the same time, the small amount of palmitic acid acts as a surfactant and makes the microbubbles more stable, which permits longer observation time. Although contrast-enhanced color Doppler sonography and power Doppler sonography have improved detection of residual neoplastic tissue after percutaneous treatment of liver tumors [10, 18, 19], early attempts by Choi et al. [19] and Solbiati et al. [18] still failed to identify more than 50% of the tumor with residual enhancement after radiofrequency ablation.
Recently, many kinds of new technologies have been improved using the signals from contrast microbubbles [6, 19–28]. Phase-inversion harmonic sonography is a newly developed microbubble-specific technique in which two pulses (one with a 180° phase change) are sent in rapid succession into the tissue. The transducer receives the sum of the echo signals back from the two inverted pulses. Therefore, the signals from the harmonic component are boosted, and those from the fundamental component are suppressed. As previously reported, phase-inversion harmonic sonography is superior to conventional Doppler sonography and second harmonic sonography in the depiction of tumor vascularity [25–28]. However, although recent attempts by Meloni et al. [28] using contrast-enhanced phase-inversion harmonic sonography have increased the sensitivity in detecting the residual tumor after radiofrequency ablation up to 83.3%, further improvement in imaging detection is desired.
Coded harmonic angio is a breakthrough technology that combines phase-inversion harmonic sonography with coded technologies [30]. This technique boosts weak signals from microbubbles and suppresses unwanted signals or frequencies by transmitting a coded pulse sequence and decoding the pulse sequence in receiving signals. Coded harmonic angio shows a higher sensitivity to weak signals from the low-velocity blood flow and results in easier recognition of the blood signals on the gray-scale background. In our study, imaging with coded harmonic angio was performed with the use of Levovist. Two scanning methods were used after administration of Levovist. In the early arterial phase, continuous scanning was performed to depict the intratumoral blood signals in real time (vessel image). In the late vascular phase, interval delay scanning or intermittent scanning was performed to give the microbubbles time to flow into the capillary bed of the hepatocellular carcinoma. Using an interval delay scanning technique, we were able to show the tumor parenchymal stain, which appeared as a bright but momentary echo in the first frame after several seconds of freeze, by destroying the microbubbles staying in the tumor parenchyma [23, 31].
Contrast-enhanced imaging with coded harmonic angio accurately revealed the enhancement from the residual neoplastic portion in 38.3% (41/107) of the examined hepatocellular carcinoma nodules after radiofrequency ablation. Compared with dynamic CT, contrast-enhanced coded harmonic angio showed a high sensitivity of 95.3% in identifying the presence of residual tumor. Both the positive predictive value and the diagnostic specificity of contrast-enhanced coded harmonic angio are 100%.
On the other hand, on dynamic CT, the exact safety margin (enough ablated area surrounding the tumor) can be correctly evaluated by comparing identical tomographic slices in which the edge of low-attenuation area is at least 5 mm from the edge of the tumor. In other words, although it is difficult to differentiate ablated normal liver tissue from the ablated hepatocellular carcinoma nodule, it is possible to identify the safety margin in identical CT scans before and after radiofrequency ablation. As reported by Onda et al. [29], the local recurrence rate was significantly less in those tumors that showed complete response with an adequate safety margin (> 5 mm) than in those without an adequate safety margin on dynamic CT performed after radiofrequency ablation. It is important to obtain a safety margin after radiofrequency ablation to reduce the local recurrence rate. In our report, a safety margin that was more than 5 mm in thickness was defined as enough to ensure adequate treatment of the tumor. However, even on B-mode sonography, as well as on unenhanced sonography in the coded harmonic angio mode, it is almost impossible to identify the safety margin because of the difficulty in identifying the edge between the necrotic tumor and the ablated peritumoral liver tissue. Therefore, contrast-enhanced imaging with coded harmonic angio can only reveal whether residual tumor is present; it cannot be used to identify whether the safety margin is large enough.
As shown in our study, contrast-enhanced imaging with coded harmonic angio is now changing the therapeutic strategy to assess imaging with hepatocellular carcinoma (Figs. 4A, 4B). Before introduction of contrast-enhanced coded harmonic angio, dynamic CT was necessary after each session of radiofrequency ablation to evaluate the effect of the treatment. With contrast-enhanced coded harmonic angio, the therapeutic response can be correctly evaluated without performing CT. Thus, the cost and the exposure of patients to CT radiation can be decreased. However, even if complete response to radiofrequency ablation is shown on contrast-enhanced coded harmonic angio, final assessment on dynamic CT is still necessary for identifying the safety margin and determining whether an additional session of radiofrequency ablation is needed.
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There are several limitations in this study. First, only hepatocellular
carcinoma nodules that showed positive intratumoral vascularity on
contrast-enhanced imaging with coded harmonic angio before radiofrequency
ablation were included. Because of the inherent limitation of
contrast-enhanced sonography, including coded harmonic angio, it is impossible
to evaluate the treatment response of hypovascular hepatocellular carcinomas,
which was also observed in another study
[24]. Second, the histologic
proof of pretreatment of hepatocellular carcinoma was absent in most of the
study population. However, for the general clinical practice, elevated levels
of -fetoprotein and prothrombin induced by vitamin K absence as well as
the typical imaging findings and clinical background are satisfactory to make
a correct diagnosis of hepatocellular carcinoma. Third, instead of histology,
three-phase dynamic CT was used as the gold standard for evaluation of the
treatment response of hepatocellular carcinoma in this study, as in other
studies [5,
7–9,
12–15,
23,
24], because dynamic CT is
commonly used in clinical settings
[24]. Because a biopsy-proven
necrosis does not always represent the necrosis of the whole nodule as a
result of frequently experienced sampling error, findings from the biopsy may
be unreliable concerning the presence or absence of residual tumor and can
hardly be considered the gold standard
[24]. In addition, our study
observed only the short-term therapeutic response of hepatocellular carcinoma
after radiofrequency ablation. Certainly, with long-term follow-up, additional
foci of residual tumor can be uncovered. Thus, further studies are necessary
to evaluate this technique and compare it with other methodologies at a later
time in the follow-up.
In summary, contrast-enhanced imaging with coded harmonic angio can provide a useful and alternative approach that has high diagnostic agreement with dynamic CT in assessing the therapeutic effect on hypervascular hepatocellular carcinomas after radiofrequency ablation, in spite of a limitation in identifying the safety margin. This finding is of great value. The information regarding the residual tumor after radiofrequency ablation can be obtained with sonography because this modality is used as a guidance for percutaneous needle insertion therapy.
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