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Ultrasonography |
1 From the Department of Gastroenterology and Hepatology (H.D., M.K., H.O., Y.S., Y.M., H.C., T.K.) and Abdominal Ultrasound Unit (H.D., K.M.), Kinki University School of Medicine, 377-2 Ohno-Higashi, Osaka-Sayama, Osaka 589-8511, Japan. Received January 24, 2001; revision requested March 5; revision received April 20; accepted May 22. Address correspondence to M.K. (e-mail: m-kudo@med.kindai.ac.jp).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Fifty HCC nodules were examined with contrast-enhanced coded phase-inversion harmonic US before and after treatment. Intratumoral vascularity was assessed with continuous imaging in the early arterial phase and with interval-delay scanning to depict tumor parenchymal flow during the blood pool phase. Vascular findings at US were compared with those at dynamic computed tomography (CT).
RESULTS: In 50 HCC nodules before treatment, positive enhancement of tumor vessels and tumor parenchymal flow (stain) were observed in 47 (94%) and 46 (92%), respectively. Either tumor vessel or stain was visualized with coded harmonic US in 49 of 50 nodules. Eighty-one coded harmonic US studies were performed in 49 posttreatment HCC nodules. Compared with dynamic CT, the sensitivity, specificity, and accuracy of coded harmonic US in helping to detect positive enhancement in pretreatment HCC were 98% (49 of 50), 100% (50 of 50), and 98% (49 of 50), respectively. After treatment, positive enhancement of tumor vascularity was observed in 39 (48%) of 81 posttreatment studies, and no enhancement was observed in others (52%). Coded harmonic US demonstrated partial and no enhancement of tumor vascularity in four and one nodule, respectively; after transcatheter arterial embolization with iodized oil, evaluation of tumor vascularity with dynamic CT was difficult because of the presence of oil.
CONCLUSION: With enhancement, coded harmonic US depicted tumor vascularity by showing tumor vessels in a real-time fashion at continuous imaging and tumor parenchymal flow at interval-delay scanning.
Index terms: Computed tomography (CT), comparative studies, 761.1211 • Computed tomography (CT), helical, 761.12115 • Liver neoplasms, CT, 761.12115, 761.323 • Liver neoplasms, therapy, 761.1264 • Liver neoplasms, US, 761.12981, 761.12988 • Microbubbles • Ultrasound (US), comparative studies, 761.12981, 761.12988 • Ultrasound (US), contrast media, 761.12988 • Ultrasound (US), harmonic study, 761.12989
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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After successful treatment, tumor enhancement disappears at contrast-enhanced CT and angiography, or intratumoral flow signal disappears at color or power Doppler US. On theother hand, color or power Doppler US is reported to be less sensitive in revealing tumor residuals or recurrence of HCC after TAE or PEI or both (3–5), although it is less invasive compared with contrast-enhanced CT and angiography. Nevertheless, detection of recurring regions of HCC after TAE or percutaneous treatment with US is extremely important, since additional local therapy usually is performed with US guidance.
Through efforts to improve sensitivity in detecting tumor flow by using both US instruments and contrast agents (6,7), real-time gray-scale harmonic US imaging has become available owing to the recent development of the coded excitation mode (Coded Harmonic Angio, CHA; GE Medical Systems, Milwaukee, Wis). This mode is based on a combination of phase-inversion harmonic US imaging and coded technology. It boosts weak signals from microbubbles and suppresses unwanted signals or frequencies by first encoding and then decoding a pulse sequence when it receives the signals. With the use of a contrast agent, coded harmonic US depicts signals from microbubbles in very slow flow without Doppler-related artifacts. Consequently, it might be a more accurate way to demonstrate residual viable tumor flow in HCC after therapy. The purpose of our study, therefore, was to assess the reliability of contrast-enhanced real-time gray-scale US in evaluating posttreatment response of HCC.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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In seven patients with multiple HCCs, the two largest lesions were selected for this study. The other 36 patients had a solitary nodule. Thus, a total of 50 nodules were pooled for the study. The number and size of tumor nodules were established on the basis of US findings. The maximum diameter of HCC nodules ranged from 1 to 10 cm (mean, 3.2 cm ± 2.7 [SD]). The final diagnosis of HCC was determined according to US-guided biopsy findings in 39 nodules. The diagnoses in other cases were based on clinical laboratory data that included positive results for hepatitis B surface antigen or hepatitis C antibody tests and a serum 
-fetoprotein level greater than 20 µg/L (20 ng/mL) with an increasing trend (range, 31–35 µg/L [31–5,435 ng/mL]; mean, 743 µg/L [743 ng/mL]; 28 patients), along with typical vascular findings at CT during hepatic arteriography and during arterial portography and/or a typical vascular and signal intensity pattern at MR imaging in the remaining 11 nodules.
In this study, typical findings for HCC included a high-attenuating mass at early-phase CT during hepatic arteriography, a perfusion defect at CT during arterial portography, and a high-signal-intensity mass at T2-weighted MR imaging with a hypervascular pattern at dynamic MR imaging.
Contrast-enhanced US Examination
In this study, a suspension of monosaccharide microparticles (galactose) in sterile water (SH U 508A, Levovist; Schering, Berlin, Germany) was used as the US contrast agent. Microbubbles with an average diameter of 2–8 µm, which can traverse the pulmonary capillary bed and enhance the signal of hepatic blood flow, were stabilized in the microparticle suspension. Before US examination, the agent was prepared by shaking it vigorously with 5 mL of water for 5–10 seconds. After allowing the agent to stand for 2 minutes for equilibration, a total of 2.5 g (6 mL of 400 mg/mL concentration) of SH U 508A was injected manually through a 20-gauge cannula inserted in an antecubital vein at a speed of 1 mL/sec and was flushed with an additional 10 mL of normal saline.
Coded harmonic US was performed by using a machine (Logiq 700 MR Expert; GE Medical Systems) with a 2–4-MHz curved-array wide-band transducer. The acoustic power of the coded harmonic US was set at the default setting with a mechanical index of 0.6–0.8. Prior to injection of the contrast agent, a scanning plane displaying both the tumor and some surrounding liver parenchyma with fundamental B mode was chosen before switching to coded harmonic US. After injection of SH U 508A and when the first microbubble signal intensity appeared in the liver parenchyma, the patient was instructed to hold his or her breath. Images in the ideal scanning plane were displayed in a real-time fashion by slightly changing the scanning plane to portray the whole area of the nodule. Immediately after real-time continuous imaging of the tumor vessels for about 20 seconds, interval-delay scanning (8–10) or manual flash imaging by changing the scanning plane was performed to demonstrate tumor parenchymal flow in the blood pool phase (less than 5 minutes after injection of SH U 508A). Since the enhancement effect of SH U 508A can be seen 10–15 seconds after injection and lasts only 3–4 minutes, the time required for the contrast-enhanced study was approximately 3 minutes.
All the data were recorded continuously on videotapes, and still images from cine loops were stored on magneto-optical disks.
Therapeutic Techniques
The therapeutic methods selected for HCC in this study were TAE, RF ablation, and PEI techniques. Before TAE, hepatic angiography was first performed. Then, a mixture of iodized oil (Lipiodol; Guerbet, Aulnay-sous-Bois, France) and a chemotherapeutic agent (epirubicin, Farmorubicin; Kyowa Hakko, Tokyo, Japan), together with a gelatin sponge, were injected through a catheter whose tip was placed superselectively into the segmental or subsegmental arteries feeding the tumor.
RF ablation and PEI therapies were performed with US guidance (PowerVision 8000; Toshiba Medical Systems, Tokyo, Japan) and a convex probe (PVN-375AT; Toshiba Medical Systems) or a unit with a curved-array transducer. An RF generator system (RF 2000; Radiotherapeutics, Sunnyvale, Calif) and needle electrode (LeVeen; Radiotherapeutics) were used for RF ablation therapy. The needles for PEI were multiple-side-hole 21-gauge needles (Ethanoject; Hakko Shoji, Tokyo, Japan).
The first-line therapeutic strategy for HCC in this study was TAE or RF ablation. TAE with iodized oil mixed with a chemotherapeutic agent was selected as the first-choice treatment when the nodules were multiple (n = 7) and/or the nodule was larger than 2.5 cm in diameter (n = 21). Conversely, RF ablation was selected as the first-line treatment when the nodule was solitary and less than 2.5 cm in diameter (n = 15).
The therapeutic effect was evaluated with both coded harmonic US and contrast-enhanced triple-phase dynamic helical CT 7 days after TAE or 5–7 days after RF ablation therapy. If residual vascularity was seen on either coded harmonic US or contrast-enhanced CT scans, RF ablation therapy was performed according to the volume and location of residual tumor area. When the location of the tumor was not indicated for RF ablation because of safety or a technical issue, such as the tumor being located adjacent to the gallbladder or at the caudate lobe, PEI was used as an additional treatment to TAE. As a result, in 21 of 28 patients who underwent TAE with iodized oil, additional treatment by using RF ablation (n = 19) and PEI (n = 2) was performed. Additional RF ablation was performed following incomplete first-line RF ablation (n = 11).
After these treatments, SH U 508A–enhanced coded harmonic US and dynamic CT were similarly repeated until complete tumor necrosis was achieved. Therefore, 81 studies with SH U 508A in 43 patients with 50 HCC nodules were performed for posttreatment evaluation.
Image Analysis
To minimize the procedural variations, pretreatment and posttreatment contrast-enhanced coded harmonic US was performed by the same physician (H.D.) by using the same examination protocol. The imaging data were recorded on videotapes for subsequent review by two other independent experienced specialists (M.K., K.M.) other than the physician who performed the examination. Differences in detection of tumor vascularity were resolved by consensus. The two readers were blinded to each other’s findings. The intraobserver agreement between two blinded readers was also evaluated. Whether or not there was any flash artifact related to the coded harmonic US scan was also evaluated.
Vascular findings evaluated with coded harmonic US included tumor vessels demonstrated with continuous imaging in the early arterial phase (about 15–40 seconds after injection of SH U 508A) and tumor parenchymal flow (stain) demonstrated with interval-delay scanning during the blood pool phase (less than 5 minutes after injection of SH U 508A). Positive enhancement of intratumoral vessels with continuous imaging or intratumoral parenchymal flow with interval-delay scanning was defined as strong transient gray-scale enhancement appearing within the tumor. Positive enhancement was interpreted as hypervascular or viable tumor flow in nodules after treatment. In contrast, no enhancement of intratumoral vessel or intratumoral parenchymal flow was defined as a no-bubble signal within the tumor, while the surrounding liver parenchyma was filled with bubble signals. No enhancement of tumor vessels or tumor parenchymal flow was interpreted as complete tumor necrosis.
Vascular findings with both continuous imaging and interval-delay scanning were compared with findings at contrast-enhanced CT by one author (M.K.). The cause of false-negative cases with coded harmonic US was evaluated. Furthermore, the sensitivity in detecting tumor vascularity between continuous imaging and interval-delay scanning was also compared.
CT examination included precontrast and postcontrast-enhanced triple-phase dynamic helical CT (Toshiba X-Vigor; Toshiba Medical Systems) at 30, 60, and 180 seconds after an intravenous bolus injection of 100 mL of iopamidol with an iodine concentration of 370 mg/mL (Iopamiron; Nihon Schering, Osaka, Japan). The rate of intravenous injection of contrast media was set at 3.0 mL/sec with an automatic power injector for all examinations. For dynamic CT, parameters were 7-mm section thickness, pitch of 1.5, and 7-mm reconstruction interval. At contrast-enhanced CT, two radiologists (H.O., H.C.) evaluated tumor enhancement by using the comparison of all triple-phase dynamic CT scans with nonenhanced CT scans. These two radiologists specialized in liver imaging and did not have knowledge of the contrast-enhanced coded phase-inversion harmonic US results. The interpretation of CT scans was performed by using hard copies retrospectively.
The order of evaluation was randomized. The criteria used for evaluating treatment response on dynamic CT scans were as follows: A complete response was diagnosed when a hypoattenuating area portraying nonenhancement was present in both the arterial and portal venous phases in nodules after treatment. Conversely, an incomplete response was diagnosed when incomplete retention of iodized oil with hypoattenuating areas showing enhancement was present in the arterial phase in nodules—after TAE with iodized oil, after TAE with iodized oil combined with RF ablation, or after TAE with iodized oil combined with PEI therapy—and when enhanced areas within the tumor were present in nodules after RF ablation therapy. If enhancement could not be evaluated at dynamic CT because of the presence of iodized oil, the nodules were classified as a "categorization failure." These categorizations of the CT enhancement pattern after treatment were determined by consensus by the two radiologists.
Results of use of coded harmonic US in detection of pretreatment tumor vascularity in 50 HCCs were compared with those with triple-phase dynamic CT. Sensitivity and specificity of coded harmonic US were calculated, and statistical analysis was performed by using the paired Student t test. A P value of less than .05 was considered statistically significant.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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For hypervascular HCC, intratumoral arterial vessels were shown at the same scanning plane by using continuous scanning. If the scanning plane was changed slightly, both tumor vessels and parenchymal flow (stain) could clearly be demonstrated by the destruction effect of SH U 508A, which was pooled in the new plane of tumor. Tumor parenchymal flow could also be demonstrated by interval-delay scanning with the same phenomenon (Fig 1).
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After effective treatment, no enhancement of tumor vessels or tumor parenchymal flow was demonstrated at coded harmonic US in 42 of 81 studies in nodules (Fig 2). In contrast, partial enhancement of either tumor vessels or tumor parenchymal flow suggested residual viable tumor in 39 of 81 studies in nodules (Fig 3). Vascular findings of HCC after treatment are shown in Table 2. Among 81 contrast-enhanced studies of posttreatment HCC nodules, partial enhancement of tumor vessels or tumor parenchymal flow was observed in 48% (39 studies) and in 46% (37 studies), respectively. All in all, 39 studies with SH U 508A revealed residual viable tumor signals at coded harmonic US, and additional US-guided percutaneous therapies were performed thereafter.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The recently introduced phase-inversion harmonic US technique is a microbubble-specific approach that overcomes the conflicts between requirements of contrast and resolution in harmonic imaging to provide greater image clarity. In phase-inversion harmonic US, two identical pulses with reverse polarity are transmitted to the tissue in rapid succession. The scanner detects and summates the echoes from these two successive pulses. As a result, linear scattering from tissue results in a signal void while nonlinear signals from microbubbles stand out. Phase-inversion harmonic US depicts signals from microbubbles with good accuracy and with spatial resolution devoid of Doppler-related artifacts (16–19). Phase-inversion harmonic US displays the amplitude of the harmonic signals resulting from nonlinear echoes by simply brightening the gray-scale image. Furthermore, with the concurrent use of the newly developed encoding technology, signals from microbubbles are much more evident and easier to differentiate from the gray-scale background.
The microbubble agent SH U 508A is a blood-pool Doppler-enhancing agent and is known to be well tolerated with a good safety profile (7). SH U 508A has gained clinical approval in many countries worldwide. The behavior of microbubbles in an ultrasound beam is complex. At lower acoustic power, the microbubbles reflect ultrasound echoes. At higher acoustic power (though still within accepted limits for diagnostic imaging), harmonic signals appear and the microbubbles can be destroyed or disrupted, which manifests a strong transient gray-scale enhancement (16,20).
In this study, tumor vascularity demonstrated by using coded harmonic US included findings of tumor vessels at continuous imaging and tumor parenchymal flow at interval-delay scanning. Both approaches are based on the destruction of microbubbles. However, real-time continuous imaging shows signals from mobile microbubbles per se, while interval-delay scanning demonstrates signals from mobile and stationary microbubbles. At continuous imaging, only the newly refreshed microbubbles give rise to signal enhancement, since all microbubbles within the scanning plane are destroyed continuously with the acoustic power of diagnostic ultrasound wave. In contrast, interval-delay scanning involves destruction of the accumulated microbubbles within the tumor parenchyma during a given interval, which causes them to release high-intensity signals. As such, microbubbles are not required to be mobile for detection. Therefore, interval-delay scanning allows accurate detection of blood in smaller vessels, such as the capillary bed, and in vessels where the flow velocity is too low to be detected with the Doppler US flow technique.
HCC is often a hypervascular tumor that derives its blood supply primarily from the hepatic artery. The typical vascular patterns of HCC manifest high attenuation relative to the liver parenchyma in the arterial phase at dynamic CT (21,22), with high-velocity signals detected at Doppler US (23). Thus, continuous imaging in the early arterial phase portrays microbubbles entering the tumor, usually in a pulsatile fashion, after SH U 508A administration. The enhancement degree of tumor vessels demonstrated at continuous imaging depends on the tumor vascularity, frame rate, and microbubble concentration. For very hypervascular HCC, tumor vessels can be demonstrated extensively by using coded harmonic US, whereas minimal tumor vessels or only some spot signals can be demonstrated in relatively hypovascular HCC or in HCC after incomplete treatment. However, any intratumoral enhanced signal intensity detected in the early arterial phase at continuous imaging appears to indicate the presence of microbubbles, namely intratumoral blood flow. In contrast with the Doppler technique, artifacts are absent at coded harmonic US. Positive enhancement of tumor vessels at continuous imaging can be interpreted as intratumoral flow, namely tumor neovasculature of HCC.
In this study, no false-positive cases were found, compared with dynamic CT in nodules before and after treatment. The specificity was 100% (39 of 39). However, the sensitivity was 92%; 46 of 50 HCC nodules before treatment demonstrated tumor parenchymal flow at interval-delay imaging. In detecting tumor parenchymal flow, three of four false-negative nodules were subphrenic lesions (two lesions located in segment 8 near the inferior vena cava) or a relatively hypovascular lesion (one lesion that was isoattenuating in the arterial phase of dynamic CT). Furthermore, two of four false-negative nodules were deeply located lesions, with a depth more than 8 cm from the transducer. However, on the basis of the overall evaluation, there was only one false-negative nodule before treatment (Table 1). Similarly, on the basis of the overall evaluation, two false-negative nodules after treatment were subphrenic lesions (Table 2).
As mentioned previously, interval-delay scanning demonstrates tumor parenchymal flow on the basis of destruction of intratumoral microbubbles refreshed during the delayed interval. Therefore, the degree of positive enhancement of tumor parenchymal flow depends on the tumor vascularity, delayed interval, and microbubble concentration within the scanning plane. Thus, interval-delay scanning would be more suitable than real-time scanning for demarcating the area of viable tumor, thus providing direct guidance for additional US-guided percutaneous therapy. There were no flash artifacts related to normal respiration or from referred cardiac pulsations in the left lobe of the liver unless the transducer sweep was rapid. This was another beneficial point compared with other Doppler-related techniques.
Positive enhancement of tumor parenchymal flow was also a sign of intratumoral flow (sensitivity, 92%), and no false-positive cases were found in 39 HCC lesions after effective treatment (specificity, 100%).
A noted advantage of coded harmonic US is that US scans are less affected by iodized oil retention. Dynamic CT has been used extensively as an imaging technique for evaluation of tumor vascularity following treatment of HCC. However, the retention of iodized oil makes it difficult to evaluate treatment response for some HCC nodules after TAE with iodized oil. In this study, dynamic CT provided unreliable information in five lesions after TAE with iodized oil because of the complete retention of iodized oil. However, coded harmonic US demonstrated viable tumor signals (positive enhancement) in four lesions and no enhancement in one lesion. On the basis that it is exclusively specific in detecting tumor vessels or parenchymal flow, additional therapy was performed consequently, which resulted in a complete response. This evidence convincingly indicates that coded harmonic US may be a more suitable technique to detect intratumoral residual blood flow in HCC nodules after TAE with iodized oil (Figs 4, 5).
There are some limitations in our study. First, dynamic CT was used as a standard to evaluate the treatment response, as it is often used in the clinical setting. Histologic proof was not always obtained from completely treated lesions, since it is considered to be unreliable; a biopsy-proved necrosis does not equate with necrosis of the whole nodule. Further studies comparing coded harmonic US with dynamic MR imaging, which may be a better tool than dynamic CT for detecting intratumoral vascularity especially in the HCC nodules with accumulated iodized oil, would be necessary to confirm this issue. Second, interval-delay scanning in the same scanning plane is technically difficult with use of SH U 508A. Interval-delay scanning in the ideal scanning plane is based on the cooperation of examiner and patient and must be practiced before injection of the contrast agent. This problem should be solved by the introduction of newly developed next-generation contrast agents. Another drawback of this technique is that it is not possible to evaluate the treatment response of the nodule, which does not show a hypervascular pattern at pretreatment coded harmonic US.
In summary, with the use of SH U 508A, coded phase-inversion harmonic US depicted tumor vascularity and tumor parenchymal flow with increased sensitivity and specificity. When compared with dynamic contrast-enhanced CT, contrast-enhanced coded phase-inversion harmonic US may be performed favorably and may be more advantageous than dynamic enhanced CT in the evaluation of the posttreatment response of HCC after TAE with iodized oil. As a result, this technique provides useful information as to whether additional therapy is necessary or not. This technique will also be helpful for US-guided retreatment of residual viable tumor owing to its real-time character and noninvasiveness. Further study findings—especially in comparison with dynamic MR imaging findings, with follow-up study results, with histologic evidence, or with all three—may be needed to confirm our conclusions.
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FOOTNOTES |
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Abbreviations: HCC = hepatocellular carcinoma, PEI = percutaneous ethanol injection, RF = radio frequency, TAE = transcatheter arterial embolization
Author contributions: Guarantor of integrity of entire study, M.K.; study concepts, M.K.; study design, M.K., H.D.; literature research, H.D.; clinical studies, H.D.; data acquisition, H.D., H.O., Y.S., Y.M., H.C., T.K., K.M.; data analysis/interpretation, H.D., M.K.; statistical analysis, H.D.; manuscript preparation, H.D.; manuscript definition of intellectual content and revision/review, H.D., M.K.; manuscript editing and final version approval, M.K.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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K. Numata, T. Isozaki, Y. Ozawa, T. Sakaguchi, T. Kiba, T. Kubota, A. Ito, K. Sugimori, K. Shirato, M. Morimoto, et al. Percutaneous Ablation Therapy Guided by Contrast-Enhanced Sonography for Patients with Hepatocellular Carcinoma Am. J. Roentgenol., January 1, 2003; 180(1): 143 - 149. [Abstract] [Full Text] [PDF]
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D. Choi, H. K. Lim, S. H. Kim, W. J. Lee, H.-J. Jang, H. Kim, S. J. Lee, and J. H. Lim Assessment of Therapeutic Response in Hepatocellular Carcinoma Treated With Percutaneous Radio Frequency Ablation: Comparison of Multiphase Helical Computed Tomography and Power Doppler Ultrasonography With a Microbubble Contrast Agent J. Ultrasound Med., April 1, 2002; 21(4): 391 - 401. [Abstract] [Full Text] [PDF]
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