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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, Zhongshan Hospital, Shanghai
Medical University, 180 Fenglin Rd., Shanghai, 200032, China.
3
Section of Abdominal Ultrasound, Kinki University School of Medicine, Osaka
589-8511, Japan.
Received July 14, 2000;
accepted after revision August 29, 2000.
Address correspondence to M. Kudo.
Abstract
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SUBJECTS AND METHODS. Thirty-two hepatocellular carcinoma lesions in 26 patients (age range, 44-85 years; mean age, 66 years) were examined with Levovist-enhanced intermittent harmonic imaging before and after therapy. A Toshiba Powervision 8000 was used. A subtraction image was obtained by digitally subtracting the last-frame harmonic image from the first-frame image when multishot mode was preset. Results of contrast-enhanced CT were compared with the results of subtraction harmonic imaging.
RESULTS. Before therapy, an enhancement pattern of tumor vascularity was seen for 93.8% (30/32) of hepatocellular carcinoma nodules on subtraction harmonic imaging. After therapy, subtraction harmonic imaging showed 46.7% (14/30) enhancement (incomplete tumor necrosis) and 53.3% (16/30) no enhancement (complete tumor necrosis). When dynamic CT was the gold standard, the sensitivity, specificity, and accuracy of subtraction harmonic imaging were 93.3%, 100%, and 96.7%, respectively. Intratumoral flow signals in hepatocellular carcinoma after therapy on harmonic imaging were used as a guide to target additional percutaneous therapy.
CONCLUSION. Digital subtraction contrast-enhanced harmonic imaging can depict tumor vascularity in hepatocellular carcinoma after therapy sensitively and accurately. Because it is easy to perform and provides real-time needle insertion guidance, it may be preferable to perform after localized therapy to monitor treatment response, which will reduce unnecessary CT scanning.
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Color Doppler sonography and power Doppler sonography are well-known imaging techniques that noninvasively reveal tumor vascularity. These techniques have been used to evaluate the treatment response of patients with hepatocellular carcinoma after transcatheter arterial embolization, percutaneous ethanol injection, or radiofrequency ablation [7,8,9,10]. However, conventional color or power Doppler sonography is not sensitive enough to provide a reliable assessment of tumor vascularity, especially in small or deeply seated hepatic tumors [11, 12].
Recently, microbubble contrast agents that enhance Doppler signals have been available for clinical use with sonography. Levovist (Schering, Berlin, Germany), which is a galactose-based microbubble contrast agent, has been licensed for routine clinical use in many countries, including Japan. The microbubbles (size range, 2-8 µm; mean diameter, 3 µm) are small enough to traverse the pulmonary capillary bed but sufficiently large to remain in the blood pool. Contrast agents for sonography are unique in that they interact with the imaging process. At low acoustic power, the microbubbles reflect ultrasound echoes. At higher acoustic power (although still within accepted limits for diagnostic imaging), harmonic signals appear, and the microbubbles can be destroyed or disrupted, resulting in transient gray-scale enhancement [13]. The increased echogenicity of these agents enables improved detection of tumor vascularity in focal liver lesions [14,15,16]. Second, harmonic imaging is a new sonographic technique that uses special properties of microbubbles to facilitate visualization of slow blood flow without motion artifacts [17,18,19]. If the ultrasound transmission is performed intermittently—namely, intermittent harmonic imaging—it enables visualization of capillary blood flow and tumor perfusion flow noninvasively [20]. It may be sensitive to revealing residual blood flow in tumors after therapy, which is extremely useful for performing further percutaneous therapy under sonographic guidance. Although the flow dynamics of Levovist are quite different from those of iodinated contrast agents for CT, intratumoral perfusion flow revealed by intermittent harmonic imaging in the early arterial phase is considered to be equivalent to that on arterial phase dynamic CT images. The purpose of this study was to assess the usefulness of contrast-enhanced intermittent harmonic imaging in evaluating the treatment response of patients with hepatocellular carcinoma by comparing the results with those obtained using arterial phase CT.
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The number and size of tumor nodules were established on the basis of
sonographic findings. The maximum diameter of lesions ranged from 1.0 to 6.0
cm (mean ± SD, 2.5 ± 1.4 cm). All patients had liver cirrhosis
(19 had hepatitis C-related cirrhosis, three had hepatitis B-related
cirrhosis, and four had alcoholic cirrhosis). The degree of liver dysfunction
was classified as Child-Pugh class A in 19 patients, Child-Pugh class B in
four patients, and Child-Pugh class C in three patients. All patients
underwent dynamic CT before treatment, and all lesions were hypervascular on
dynamic CT. The final diagnosis of hepatocellular carcinoma was made at
percutaneous biopsy under sonographic guidance in five patients. The diagnosis
in other patients was based on clinical laboratory findings, including
positive findings of hepatitis B antigen or hepatitis C antibody and serum
-fetoprotein level greater than 20 ng/mL with a rising trend (range,
24-39,170 ng/mL; mean, 3067 ng/mL) (n = 19), along with typical
vascular findings on CT angiography and CT during arterial portography
(n = 13), and typical vascular and intensity patterns on MR imaging
(n = 5).
Contrast Medium
The contrast agent used in this study was Levovist, which is composed of
galactose and a small quantity of palmitic acid. When mixed with water,
Levovist produces microbubbles of air covered by a thin stabilizing layer of
palmitic acid. The suspension was produced by shaking vigorously for 7-10 sec.
After 2 min of equilibration, a total of 2.5 g of Levovist (8.5 mL with 300
mg/mL concentration) was administered manually via a 20-gauge cannula placed
in an antecubital vein at a speed of 1 mL/sec by a bolus injection and flushed
through with 10 mL of normal saline.
Sonographic Techniques
A commercially available sonography system, Powervision 8000 (Toshiba
Medical Systems, Tokyo, Japan), with commercially available hardware for
intermittent harmonic mode and digital subtraction function was used to
evaluate the tumor vascularity of hepatocellular carcinoma before and after
therapy. Digital subtraction procedures are also performed automatically in
the machine; no additional analysis using workstation or special software is
necessary. The transducer used was PVN-375AT (Toshiba Medical Systems) convex
array, which transmitted an ultrasound beam at 3.0-4.4 MHz in B mode and 3.0
MHz in color or power Doppler mode with a mechanical index of 1.0, and
transmitted an ultrasound beam at 2.3 MHz and received at 4.6 MHz in harmonic
B mode with a mechanical index of 1.0. In the intermittent transmission mode,
the system transmits pulses at low acoustic power output (mechanical index,
<0.1) for real-time monitoring between triggered scans at high power output
(mechanical index, 1.0-1.2) (Fig.
1). Optionally, images could be displayed on a dual monitor. One
monitor is the real-time monitor of the second harmonic image with low
mechanical index, which theoretically does not destroy microbubbles, and the
other monitor displays the intermittent image instantaneously, which shows
tumor parenchymal flow. This technique allows the acquisition of several rapid
sequences at one trigger with high acoustic power and stores every image of
this sequence for later review. Consequently, digital subtraction of the
contrast harmonic B-mode image is automatically obtained by subtracting the
last-frame image from the first-frame image
[20]. Because destruction of
microbubbles creates strong gray-scale enhancement, it is possible to subtract
the frame image formed after microbubble destruction (nearly unenhanced image)
from that obtained with contrast enhancement. All triggered images are stored
in the memory, which is analogous to the cine-loop feature, and transferred to
magneto-optic disks when the memory is full.
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Before injection of Levovist, fundamental B-mode imaging and color or power Doppler sonography were performed to show the nodule. Consequently, harmonic imaging was switched on. Shortly after the injection of Levovist, when the first bubble signals appeared in the liver parenchyma, the patient was requested to hold his or her breath, and the intermittent mode was set with different interval times (1, 3, and 5 sec) for every nodule. After the freeze of the display, cine-loop memory images were reviewed.
Therapeutic Techniques
In the transcatheter arterial embolization technique, hepatic angiography
was performed first. Then a mixture of an iodized oil (Lipiodol; Andre
Guerbet, Aulnay-sous-Bois, France) and a chemotherapeutic drug, epirubicin
(Farmorbicin; Kyowa Hakko, Tokyo, Japan), together with a gelatin sponge, were
injected via a catheter whose tip was advanced superselectively into the
segmental or subsegmental arteries feeding the tumor.
Six to 10 days after the transcatheter arterial embolization, a CT examination including unenhanced and contrast-enhanced three-phase dynamic helical CT (X-Vigor; Toshiba Medical Systems) with an IV bolus injection of 100 mL of contrast media was performed to evaluate the retention of iodized oil and to detect the enhancing area in the lesion. Contrast-enhanced harmonic imaging was performed at the same time.
Radiofrequency ablation and percutaneous ethanol injection were always performed under sonographic guidance with LOGIQ 700 EXPERT Series (General Electric Medical Systems, Milwaukee, WI) with a 2-4-MHz convex probe. A radiofrequency generator system (RF 2000; Radiotherapeutics, Sunny Vale, CA) and needle electrode (Le Veen needle, Radiotherapeutics) were used for radiofrequency ablation therapy. Percutaneous ethanol injection was performed with multiple side-hole 21-gauge needles (Ethanoject; Hakko Shoji, Tokyo, Japan). Contrast-enhanced harmonic imaging and dynamic CT were performed 1 week after the end of combined treatment.
Image Analysis
To minimize the deviation between operators, all contrast-enhanced harmonic
imaging studies were performed by the same operator using the same examination
protocol. All the data were recorded continuously on videotapes. Still
pictures of each lesion were documented in magneto-optic disks.
The videotapes of all contrast-enhanced harmonic studies of each lesion were reviewed by two physicians (other than the sonographer) who prospectively assessed the outcome of treatment without knowledge of the dynamic CT results. Vascular findings on digital subtraction harmonic B-mode images were classified into two patterns—enhancement or no enhancement—depending on the tumor vascularity relative to the surrounding liver parenchyma. Enhancement was defined as tumor perfusion flow of the same degree as or a higher degree than that of surrounding liver parenchyma. No enhancement was defined as tumor shown as a vascular defect when liver parenchymal perfusion was observed on subtraction images. No enhancement was considered to be complete tumor necrosis. In contrast, any perfusion flow signal in the treated lesion on subtraction harmonic images (enhancement) was considered to be incomplete therapy. Lesions that were nonenhancing before treatment were excluded from the analysis of treatment results because failure in to depict intratumoral flow signals before treatment would impede the evaluation of changes in tumor vascularity after therapy.
The outcome of harmonic imaging was then compared with that of dynamic CT. The criteria used for assessing tumor response on dynamic CT images were as follows: Complete tumor necrosis was diagnosed in cases of complete retention of iodized oil in the lesion for nodules after transcatheter arterial embolization, cases of complete retention of iodized oil in the lesion and a hypoattenuating halo at the periphery of the nodule that showed no contrast enhancement for nodules after transcatheter arterial embolization combined with radiofrequency ablation or percutaneous ethanol injection, and cases with a hypoattenuating area that showed no enhancement on arterial and portal venous phases for nodules after radiofrequency ablation or percutaneous ethanol injection. Conversely, incomplete tumor necrosis was diagnosed in cases of incomplete retention of iodized oil with hypoattenuating areas that showed enhancement in the arterial phase for nodules after transcatheter arterial embolization, transcatheter arterial embolization combined with radiofrequency ablation, or percutaneous ethanol injection and in cases in which enhancing areas were observed in the tumor after radiofrequency ablation or percutaneous ethanol injection.
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The most important time to reveal tumor vascularity in hepatocellular carcinoma was 10-30 sec after injection of Levovist (early arterial phase or arterial dominant phase). Before treatment, 93.8% (30/32) of hepatocellular carcinoma lesions were seen as hypervascular on contrast-enhanced subtraction of intermittent harmonic B-mode images, whereas the other two nodules (6.2%) showed no enhancement. The two nonenhancing nodules were less than 3 cm in diameter and were located in segment VII or VIII near the inferior vena cava. Both intercostal and subcostal approaches showed the nodules to be more than 8 cm in depth on sonography. Consequently, the response after treatment was evaluated in 30 hypervascular (enhanced) nodules with contrast-enhanced harmonic imaging after therapy.
Vascular findings on contrast-enhanced subtraction harmonic images after therapy are shown in Table 1. Enhancement patterns were seen in 14 nodules after treatment, all of which showed incomplete tumor necrosis on dynamic CT (Figs. 2A,2B,2C,2D and 3A,3B,3C,3D). The other 16 nodules showed no enhancement on subtraction image of intermittent harmonic B-mode images, among which 15 nodules showed complete tumor necrosis on dynamic CT (Fig. 4A,4B,4C,4D). Therefore, when dynamic CT was taken as a gold standard, the sensitivity, specificity, and accuracy of subtraction harmonic B-mode imaging were 93.3%, 100%, and 96.7%, respectively.
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In 11 of 14 lesions that showed intratumoral flow signals after therapy, flow signals on harmonic imaging were used as a guide to target additional percutaneous therapy for the residual viable tumor. The other two patients (three nodules) with enhanced nodules on harmonic imaging did not receive further treatment because of poor liver function. In those three nodules, the growth of residual viable tumors was confirmed at clinical follow-up. Patients with nonenhancing nodules were closely followed up with sonography, dynamic CT, or dynamic MR imaging for 5-8 months (mean ± SD, 5.9 ± 0.95 months). All nodules showed no enlargement on sonography during this time; no tumor enhancement appeared again on dynamic CT or dynamic MR imaging during this follow-up period.
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However, areas of residual tumor after radiofrequency ablation or
percutaneous ethanol injection are not distinguishable from necrotic tissue on
sonography [9,
23]. The sonographic findings
of gray-scale, color Doppler, and power Doppler scanning after radiofrequency
ablation or percutaneous ethanol injection do not correlate well with the
overall necrotic shape, or with the volume or extent of induced coagulation
necrosis [6,
9,
23]. Therefore,
contrast-enhanced CT or MR imaging is generally required to assess
effectiveness of the treatment. Absence of enhancement on contrast-enhanced CT
indicates disappearance of the blood supply and thus successful treatment.
Conversely, focal areas of persistent contrast enhancement usually indicate
viable tumor cells and the need for further treatment to achieve complete
tumor necrosis. In this study, pretreatment -fetoprotein values were
increased (range, 24-39, 170 ng/mL) in 19 patients. Although
-fetoprotein levels may be a good measure to evaluate longterm
treatment response, they are inadequate to evaluate short-term response to
determine whether additional therapy is necessary because the half-life of
-fetoprotein is quite long in vivo.
Although contrast-enhanced CT can depict residual area in tumors after radiofrequency ablation or percutaneous ethanol injection [6, 9, 24], it does not enable real-time guidance of percutaneous therapy. Furthermore, retention of Lipiodol in hepatocellular carcinoma lesions sometimes makes it difficult to distinguish the hyperattenuating area of contrast enhancement from that of Lipiodol when the retention of iodized oil in the tumor is incomplete [2, 4]. In this situation, the identification of the viable component of the tumor was easy on MR imaging. Signal intensity on MR imaging is not affected by the retention of iodized oil in the tumor, and all necrotic lesions show hypointensity on T2-weighted images [4]. However, it is more difficult to perform contrast-enhanced MR imaging for every patient after transcatheter arterial embolization mixed with Lipiodol than it is to perform contrast-enhanced CT because MR imaging is more time-consuming. Thus, in this study, dynamic CT was used as the gold standard to assess the ability of contrast-enhanced harmonic imaging to evaluate therapeutic effectiveness in patients with hepatocellular carcinoma.
Levovist is a galactose-based microbubble contrast agent that can be administered IV. The microbubbles are echogenic and create back-scattered signals at multiple harmonic frequencies. Harmonic imaging is a new sonography technique that transmits ultrasound pulses at one frequency and selectively receives echoes at double that frequency. The theoretic advantage of the harmonic frequency over the fundamental frequency is that only contrast-agent microbubbles resonate with harmonic frequencies, whereas adjacent tissues either do not resonate or their harmonic resonation is slight. Therefore, harmonic imaging greatly improves the signal-to-noise ratios and reveals flow in moving tissue without a flash artifact [14, 17,18,19]. Gray-scale harmonic imaging is the first method to enable visualization of blood perfusion and capillary blood flow on sonography with the IV administration of a contrast agent. However, to effectively obtain harmonic signals of Levovist with continuous gray-scale harmonic imaging, a dose of Levovist three to five times larger than that clinically used for humans was needed in an animal study [25], because continuously transmitted acoustic power breaks the microbubbles quickly. Intermittent harmonic imaging transmits an ultrasound beam with a flexible interval to destroy most of the bubbles in a region of interest with high acoustic power and to permit refreshment of bubbles on the scanning plane as a result of fresh blood inflow [18, 20, 26]. Digital subtraction harmonic B-mode images are automatically obtained by subtracting the last-frame image from the first-frame image produced by multishot ultrasound propagation with the same trigger when the multishot mode is preset. It can extract only the blood flow echoes created from the destruction of microbubbles, and echoes from tissue are effectively cancelled. This mode makes it possible to clearly depict residual blood flow in tumors after therapy. Furthermore, with the help of a dual-monitor system, tumor perfusion flow on the same sonographic scanning plane could be obtained with different intermittent intervals because the real-time monitor image, transmitting the ultrasound beam at a low acoustic power output, does not destroy microbubbles during the interval [20] (Fig. 1).
As stated previously, microbubbles of Levovist are destroyed quickly when an ultrasound beam is introduced. However, flash echo or intermittent harmonic images showing tumor perfusion flow are considered to be at least equivalent to arterial phase CT images although late-phase images in each technique cannot be compared because of different flow dynamics.
Sonography offers some obvious benefits over other imaging modalities such as low cost, easy repetition, real-time guidance for therapy, and little influence from Lipiodol. Contrast-enhanced color and power Doppler sonography have been used to evaluate the treatment response of hepatocellular carcinoma [27, 28]. Results of previous studies have shown that both color and power Doppler sonography can provide clinically useful information related to tumor vascularity. Nevertheless, although a contrast agent greatly increases slow flow signals, conventional Doppler sonography has some limitations. Lack of perfusion flow and increased motion artifacts are inevitable on conventional color and power Doppler sonography. Fortunately, these limitations can be overcome by digital subtraction of harmonic B-mode imaging. In this study, 14 of 30 hepatocellular carcinoma lesions were revealed after therapy as enhanced on subtraction harmonic B-mode images and were interpreted as viable cancer cells. The sensitivity was 93.3% when compared with that of dynamic CT. Furthermore, subtraction harmonic imaging showed flow signals of residual viable tumor objectively with good spatial resolution (Figs. 2A,2B,2C,2D and 3A,3B,3C,3D). On the other hand, all necrotic nodules on dynamic CT showed no enhancement, resulting in a high specificity (100%). These findings suggest that contrast-enhanced subtraction harmonic B-mode imaging could depict residual viable tumor with high sensitivity and accuracy. Contrast-enhanced subtraction harmonic B-mode imaging may act as an initial posttreatment imaging study, which will reduce unnecessary CT.
In the light of the results of this study, we have adopted the protocol of performing contrast-enhanced harmonic studies in all patients after percutaneous therapy. If enhancement is seen in the treated tumor, additional percutaneous therapy is performed under sonographic guidance without performing CT. Follow-up CT is performed only for patients in whom no enhancement is seen on harmonic imaging. Therefore, although all patients should undergo dynamic CT after completion of therapy, the number of CT scans may be reduced.
There were two false-negative cases on intermittent harmonic imaging although dynamic CT showed enhancement. It is very difficult to depict intratumoral perfusion flow in deeply seated nodules on intermittent harmonic imaging, which is one of the limitations of this technique [20].
Our study has some other limitations. First, dynamic CT was the gold standard to evaluate the treatment response of hepatocellular carcinoma. Dynamic MR imaging was better than dynamic CT in evaluating the outcome of hepatocellular carcinoma treated with Lipiodol transcatheter arterial embolization. However, because of practical difficulties, dynamic MR imaging was not performed on all patients after transcatheter arterial embolization. Second, no patients in our study underwent surgery after treatment; therefore, the lack of pathologic correlation is another limitation of this study. Eleven of 14 enhanced nodules were treated with additional percutaneous therapy, and no enhancement was seen at the end of treatment. These nodules were recognized as complete tumor necrosis, which was confirmed clinically. The other three enhanced nodules, which did not receive complete therapy because of poor liver function, were confirmed as residual tumor during the follow-up period. Further investigations seem to be necessary to establish the full reliability of subtraction harmonic B-mode imaging.
In conclusion, digital subtraction contrast-enhanced harmonic B-mode images revealed tumor vascularity in patients with hepatocellular carcinoma after transcatheter arterial embolization and percutaneous therapy with high sensitivity and accuracy when compared with that of dynamic CT. Because contrast-enhanced harmonic sonography is easy to perform and provides real-time needle-insertion guidance, it may be preferable to perform after localized therapy to monitor treatment response, which may result in the reduction of unnecessary CT. Further studies may be needed to confirm our conclusion.
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