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Ultrasonography |
1 From the Department of Gastroenterology and Hepatology (H.D., M.K., H.O., Y.S., Y.M.) and Section of Abdominal Ultrasound (K.M.), Kinki University School of Medicine, 377-2 Ohno-Higashi, Osaka-Sayama, Osaka 589-8511, Japan. Received June 12, 2000; revision requested July 24; final revision received February 15, 2001; accepted February 26. 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-eight patients with 65 HCC nodules were examined by using intermittent harmonic power Doppler US and digital subtraction harmonic B-mode US, both with intravenous administration of SH U 508A. Vascular findings at early arterial phase harmonic US were classified as positive enhancement or nonenhancement, depending on the tumor vascularity relative to the surrounding liver parenchyma. These results were compared with those of three-phase helical dynamic computed tomography (CT).
RESULTS: For hypervascular HCCs, there was excellent depiction of tumor vessels and tumor stain with the two intermittent harmonic US methods. The sensitivity and specificity for depiction of tumor vascularity were 93% (41 of 44 nodules) and 100% (21 of 21), respectively, with intermittent harmonic power Doppler US and 86% (38 of 44) and 100% (21 of 21), respectively, with subtraction US, as compared with these values at dynamic CT. Attenuation was an important factor in the depictability of tumor vascularity at harmonic US.
CONCLUSION: Contrast-enhanced intermittent harmonic US enables noninvasive demonstration of tumor vessels and especially tumor stain in HCC.
Index terms: Liver neoplasms, 761.323 • Liver neoplasms, US, 761.12981, 761.12983, 761.12984, 761.12988 • Ultrasound (US), contrast media • Ultrasound (US), harmonic study, 761.12981, 761.12983, 761.12984, 761.12988
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Second-harmonic US is a recently developed US technique that involves the use of the nonlinear backscatter property of resonant microbubbles produced by an intravenously administered contrast agent. Color and power Doppler harmonic US studies are reported to be excellent for eliminating clutter noises and depicting slow blood flow in smaller vessels (11–14). Intermittent transmission of the ultrasound beam allows the contrast agent to be visualized in small vessels—even capillaries in the appropriate circumstances. This is because contrast agent bubbles often are destroyed by the ultrasound power used for medical imaging. With continuous insonation, flow is seen only in the larger vessels, because the bubbles are continuously destroyed in these vessels and thus never reach the smaller downstream vessels.
If US is performed intermittently, such as with a delay of 1 second or longer between ultrasound pulses, the bubbles can flow into the small vessels and potentially into the capillaries before they are imaged and destroyed (15–19). The detection of tumor parenchymal flow is very important in the differential diagnosis of liver tumors and in the evaluation of HCC response to treatment. The purpose of this study was to assess the effectiveness of contrast agent–enhanced intermittent harmonic power Doppler US in depicting tumor vessels and, especially, tumor parenchymal flow in HCC.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Seven patients had hepatitis B surface antigen, and 47 had hepatitis C antibody. The remaining four patients had a diagnosis of alcohol-related liver cirrhosis. Seven patients had two hepatic lesions; thus, a total of 65 nodules were included. Thirty-three of these nodules were studied before treatment; the other 32 nodules were studied after transcatheter arterial embolization, radio-frequency ablation, or percutaneous ethanol injection therapy. The sizes of the nodules were measured at fundamental B-mode US and ranged from 1 to 6 cm (mean, 2.5 cm) in diameter. The depth of the nodules was defined as the distance between the superficial edge of the nodule and the abdominal wall at fundamental B-mode US. The final diagnosis of HCC was made at biopsy or surgical resection in 10 cases. The diagnoses in the other cases were made before treatment on the basis of clinical laboratory data, including positive findings of hepatitis B antigen or hepatitis C antibody and a serum 
1-fetoprotein level greater than 20 ng/mL (20 µg/L) with a rising trend; typical vascular findings at CT angiography and/or CT during arterial portography; and/or typical vascular and signal intensity patterns at MR imaging. In this study, the typical imaging findings of HCC included a high-attenuating mass at early-phase CT angiography, a perfusion defect at CT during arterial portography, a high-signal-intensity mass at T2-weighted MR imaging, and/or a hypervascular mass at dynamic MR imaging.
Imaging
The microbubble contrast agent used in this study was SH U 508A (Levovist; Schering, Berlin, Germany), which consists of galactose microparticles (99.9%) and palmitic acid (0.1%). When mixed with water, this agent produces microbubbles of air covered by a thin stabilizing layer of palmitic acid. Before the US examinations, this agent was prepared by shaking it for 10 seconds with 7 mL of sterile water. After the suspension was allowed to stand for 2 minutes for equilibration, a total of 2.5 g of SH U 508A (concentration, 300 mg/mL) was administered, by means of manual bolus injection via a 20-gauge cannula inserted into an antecubital vein, at a rate of 1 mL/sec and flushed with 10 mL of normal saline solution.
A commercially available US system (PowerVision 8000; Toshiba Medical Systems, Tokyo, Japan) with a PVN-375AT convex array (Toshiba Medical Systems) was used to evaluate the vascularity of HCCs. The system transmits an ultrasound beam at 3.0–4.4 MHz in the fundamental B mode and at 3.0 MHz in the color or power Doppler mode, it transmits an ultrasound beam at 2.3 MHz and receives the reflected beam at 4.6 MHz in the harmonic B mode, and it transmits an ultrasound beam at 2.1 MHz and receives the reflected beam at 4.2 MHz at harmonic power Doppler US.
In the intermittent transmission modes, the system transmits pulses at low-acoustic-power output for real-time monitoring between acquisitions of triggered scans at high power output (17). Optionally, images can be displayed on a dual-monitor system, which consists of a real-time monitor that displays tissue harmonic images at low power and low mechanical index (which theoretically do not destroy microbubbles) and another monitor that displays the multishot intermittent contrast harmonic images captured instantaneously—that is, it demonstrates only still images, which show tumor parenchymal flow. The second monitor displays images that depict tumor parenchymal flow by displaying images obtained at a higher power and higher mechanical index than those used to display images on the real-time monitor. These images are obtained only intermittently but at a power and mechanical index high enough to destroy the bubbles when they are imaged. Because these intermittent contrast harmonic images are obtained infrequently (at selectable time intervals), bubbles can flow into the small parenchymal vessels—even the capillaries—before they are imaged and destroyed.
The machine has multishot technology with an automatic digital subtraction function. This multishot technology enables the acquisition of several rapid sequences of images at one trigger with high acoustic power and stores every image of this sequence for later review. Digital subtraction images of the multishot intermittent scans can be obtained on the same US equipment in a real-time fashion. The theory behind this is as follows: After a waiting interval to allow the contrast agent to flow into the small downstream vessels, ultrasound pulses at high power and high mechanical index are transmitted to destroy the bubbles; this process produces the resonance and destruction image (ie, image of parenchymal flow). The first image depicts the maximum vascularity as many bubbles are destroyed, whereas the second and third images depict less vascularity because the rapid sequence pulse does not allow enough flow of the microbubbles into the small downstream vessels.
If several frame images are obtained at one trigger, the last frame image depicts only the background tissue with very little blood flow, because most of the bubbles have already been destroyed. Because the interval of this train of pulses is short enough, approximately 40–50 msec, little or no patient motion will have occurred. Therefore, the last frame image of this short sequence of images can be subtracted from the first frame image, with the resultant image displaying only vascular space, which contains contrast agent (15,17). The US unit used in this study (PowerVision 8000; Toshiba Medical Systems) has presettings that allow these subtraction images to be obtained automatically when the multishot subtraction mode is selected.
For every nodule, the patient received a total of two vials of contrast agent. One vial, which contained 2.5 g of SH U 508A (total injected amount, 7 mL), was used for harmonic power Doppler US, and the other vial was used for harmonic B-mode US with intermittent transmission. After contrast agent injection, both harmonic imaging examinations were performed for 2 minutes. There was an interval of at least 10 minutes between the two injections.
Prior to SH U 508A injection, fundamental B-mode US and color or power Doppler US were performed to identify the nodule. Then harmonic imaging began. At contrast agent injection, a mark was typed on the screen, and the video clock was reset to zero. Shortly after the injection of SH U 508A, when the first bubble signals began to appear in the liver parenchyma, the patient was asked to hold his or her breath, and the intermittent mode was set at a different interval (1, 2, and 3 seconds) for every nodule. The interval delay time was set manually. After the freeze of the displayed images, the optimal image was selected by reviewing the images from the cine-loop memory. All data were recorded continuously on videotapes. Still images of each lesion were displayed on the computer workstation and stored on magnetico-optical disks.
Analysis
The side effects associated with SH U 508A injection that were experienced during and after the procedures were reviewed in all patients. To minimize variation from different operators, the contrast-enhanced harmonic imaging studies were performed by the same operator (H.D.) and by using the same examination protocol. Two other authors (M.K., K.M.) reviewed the videotapes and evaluated the tumor vascularity results at harmonic US. Vascular findings at intermittent harmonic power Doppler US and digital subtraction harmonic B-mode US were classified into two patterns—positive enhancement and nonenhancement—depending on the tumor vascularity relative to that of the surrounding liver parenchyma. Positive enhancement was defined as that when the tumor vessels and tumor parenchymal flow showed the same or a higher degree of enhancement relative to that of the surrounding liver parenchyma. Nonenhancement was defined as that when the tumor was shown as a vascular defect when liver parenchymal perfusion was observed on intermittent US images.
Depictability of tumor vascularity was compared between nodules less than 7 cm and those greater than 7 cm in depth from the abdominal wall. Statistical analysis of differences in sensitivity and specificity for the depiction of tumor vascularity between nodules less than 7 cm in depth and those more than 7 cm in depth from the transducer was performed by using the 
2 test. A P value of less than .05 was considered to indicate a statistically significant difference.
For every nodule, CT, including precontrast and contrast-enhanced three-phase dynamic helical scanning (X-Vigor; Toshiba Medical Systems), was performed 30, 60, and 180 seconds after intravenous bolus injection of 100 mL of iopamidol (370 mg per milliliter of iodine) (Iopamiron; Nihon-Schering, Osaka, Japan) at the same time as contrast-enhanced harmonic US. The tumor vascularity of each lesion at dynamic CT was assessed by two other physicians (H.O., Y.S.) without knowledge of the harmonic US results and used as the standard of reference. At harmonic US, we evaluated whether the tumor vasculature and parenchymal stain could be demonstrated during the early arterial phase. During the early arterial phase, all three interval delay images—namely, 1-second interval images for 3 seconds (three frame images), 2-second interval images for 6 seconds (three frame images), and 3-second interval images for 9 seconds (three frame images)—were obtained. Thus, a total of nine frame images were obtained.
Similarly, we analyzed whether tumor enhancement could be demonstrated during the arterial dominant phase of dynamic CT. Thus, the effectiveness of contrast-enhanced harmonic US in depicting tumor vascularity was compared with that of CT. In this study, a simple variable—whether positive enhancement was observed—was compared between dynamic CT and harmonic US. Statistical analysis of the difference between the demonstration of tumor vascularity at contrast-enhanced harmonic power Doppler US and that at subtraction harmonic B-mode US was performed by using the 2 test.
The enhancement pattern of the tumor (ie, time after injection and grade of enhancement), as compared with that of the surrounding liver parenchyma, was analyzed subjectively by reviewing a videotape. Similarly, the most adequate period to observe tumor vasculature and tumor parenchymal flow was assessed on the basis of the clarity of tumor delineation by reviewing a videotape.
The clarity of tumor delineation was evaluated on the basis of whether the tumor margin could be clearly demarcated from the surrounding liver parenchyma—that is, whether tumor-to-nontumor contrast was clear. The intensity of tumor parenchymal flow, which was graded on the basis of enhancement grade at subjective analysis, was compared according to the different interval delay times (1–3 seconds).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Positive enhancement (Fig 1) was demonstrated at harmonic power Doppler US in 32 of 33 HCCs before treatment and in nine of 32 HCCs after treatment. Positive enhancement was demonstrated at digital subtraction harmonic B-mode US in 31 of 33 HCCs before treatment and in seven of 32 HCCs after treatment. However, dynamic CT depicted hypervascularity in all 33 untreated HCCs and in 11 of 32 treated HCCs, which suggested incomplete response to therapy. Nonenhancement (Fig 2) was demonstrated in 24 of 32 HCCs at harmonic power Doppler US and in 27 of 32 HCCs at subtraction US, in contrast to 21 of 32 HCCs at dynamic CT. The tumor vascularity depiction rates with intermittent harmonic power Doppler US and subtraction harmonic US are listed in Table 1.
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For positive enhanced HCCs at harmonic US, tumors were enhancing earlier and better than the surrounding liver during the early arterial phase, without exceptions. For every positive enhanced nodule, a gradual increase in enhancement was observed when the intermittent interval was increased from 1 to 3 seconds, although these evaluations were subjective and qualitative rather than quantitative (Fig 3).
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Values of hypervascular HCC nodule depictability, as classified into two groups according to depth from the abdominal wall at US, are listed in Table 2. Differences in the sensitivity of both harmonic US modalities were statistically significant between the two groups of nodules classified according to depth (P < .01). Differences in the accuracy of both harmonic US modalities also were statistically significant between the two groups (P < .01). For nodules within 7 cm in depth, harmonic US depicted tumor vascularity with high sensitivity and accuracy, as compared with dynamic CT. However, for deeply located nodules, harmonic US was found to be limited in the depiction of tumor vascularity, as compared with dynamic CT.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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SH U 508A, a galactose-based US contrast agent, has been widely studied and reported to be well tolerated with intravenous injection and thus useful clinically (21). When mixed with water, it produces microbubbles ranging from 1 to 8 µm in diameter (mean, 1.3 µm), which is small enough to pass through capillary beds.
Intermittent harmonic US makes use of two fortuitous properties of US contrast agents. First, at the second harmonic frequency, the signal from the bubble is similar, and in some circumstances equal to, the signal at the fundamental frequency; this is in contrast to tissue, which has a markedly lower signal at the second harmonic frequency than at the fundamental frequency. These characteristics allow one to more easily discriminate the signal from the bubble from the signal of the tissue at the second harmonic frequency. Second, at power levels within the diagnostic range, the bubbles can be destroyed to yield a signal that is much larger than the signal from a bubble that is not destroyed. At intermittent harmonic US with bubble destruction, intermittent transmission with a flexible interval is used to destroy, with high acoustic power, most of the bubbles in a region of interest and to allow enough inflow of bubbles in the scanning plane owing to fresh blood inflow during the nontransmission period (15–17,22). Therefore, intermittent harmonic power Doppler US is a combination of intermittent transmission and harmonic power Doppler technology, which enables one to map a parameter that is directly related to the number of scatters in the blood (ie, the total integrated power of the Doppler spectrum enhanced by the microbubbles).
At digital frame subtraction US, only the blood flow echoes created from the collapse of microbubbles while echoes from tissue are effectively canceled can be extracted. Furthermore, the dual-monitor system makes it possible to observe tumor parenchymal flow in the same scanning plane, because the real-time monitor displays harmonic images at low acoustic power without destroying microbubbles.
HCC is often a hypervascular tumor that derives its blood supply primarily from the hepatic artery. The typical vascular patterns of HCC are high attenuation relative to the liver parenchyma during the early phase at dynamic CT (8,23,24), high velocity signals at color Doppler US (4), and a peripheral arterial supply and homogeneous or mosaic hypervascular pattern at US angiography (7). In this study, excellent depiction of the hypervascular pattern in HCCs was observed before treatment at intermittent harmonic US during the early arterial phase. The sensitivity and specificity of the two harmonic US modalities were relatively high, as compared with those of dynamic CT (Table 1). Thus, intermittent harmonic US has the potential to be very sensitive and accurate in the evaluation of HCC tumor vascularity.
We found that most of the false-negative nodules were greater than 7 cm in depth from the abdominal wall. Therefore, attenuation was the major factor that influenced the depictability of tumor vascularity at harmonic US, because increased attenuation occurred with increasing depth. Tanaka et al (25) reported that for deeply located HCCs, the use of SH U 508A led to improved sensitivity of fundamental color Doppler US in the depiction of tumor vessels. In their study, HCC nodules greater than 7 cm in depth were studied with fundamental color Doppler US. After administration of SH U 508A, 57% (four of seven) of negative HCC nodules were enhanced at fundamental color Doppler US. The contrast agent greatly improved the depictability of HCC tumor vascularity at fundamental and harmonic Doppler US. However, it was not always possible to visualize enhanced signals from fine vessels in deep areas at harmonic power Doppler US, because the intensity of backscattered signals from SH U 508A is weaker at the harmonic frequency than at the fundamental frequency (26,27). This is a limitation of harmonic US with SH U 508A that probably will not be a problem with newer agents.
In this study, the hypervascular pattern of HCC during the early arterial phase was clearly demonstrated with the two intermittent harmonic US modalities when the nodule was less than 7 cm in depth from the abdominal wall. Furthermore, different intermittent intervals enabled different degrees of tumor enhancement (Fig 3). The longer the interval delay was, the stronger the enhancement intensity became. These results suggest that a longer interval delay may enable demonstration of more detailed parenchymal flow in the tumor. In addition, changing the intermittent interval may enable one to evaluate the intranodular hemodynamics of HCC semiquantitatively.
On the other hand, in the present study, the hypovascular HCCs after effective therapy showed negative enhancement relative to the surrounding liver at harmonic US, with high specificity (ie, no false-positive cases). Because percutaneous treatment for HCC is becoming increasingly popular and most such treatments are performed with US guidance, it would be especially useful if the tumor vascularity or recurring region of HCC could be demonstrated on US tomographic images. Contrast-enhanced intermittent harmonic US had high sensitivity and specificity in depicting tumor vascularity in HCC in our study and therefore could be a promising imaging modality for evaluating HCC response to treatment.
A limitation of our study was that 55 of 65 HCCs were diagnosed clinically without pathologic proof. However, typical hypervascular patterns were seen before treatment at dynamic CT, digital subtraction angiography, or dynamic MR imaging in all lesions with a compatible clinical background. Despite this limitation, the results demonstrated in this study are potentially important because we were trying to compare the depictability of tumor vascularity at contrast-enhanced harmonic US with that at dynamic CT—not trying to demonstrate HCC-specific vasculature.
In summary, with administration of SH U 508A, intermittent harmonic power Doppler US and digital subtraction harmonic B-mode US with a dual-display system enabled the demonstration of tumor vessels and tumor parenchymal flow in HCC during the early arterial phase. We have concluded that the described noninvasive parenchymal flow imaging technique, intermittent harmonic US, may have an important role in evaluating the intranodular hemodynamics of HCC in the clinical setting.
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FOOTNOTES |
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Abbreviation: HCC = hepatocellular carcinoma
Author contributions: Guarantor of integrity of entire study, M.K.; study concepts and design, M.K., H.D.; literature research, H.D.; clinical studies, H.D.; data acquisition, all authors; data analysis/interpretation, H.D., M.K., K.M.; statistical analysis, H.D.; manuscript preparation, H.D.; manuscript definition of intellectual content and editing, M.K., H.D.; manuscript revision/review, M.K., K.M.; manuscript final version approval, M.K.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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