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1
Third Department of Internal Medicine, Yokohama City University School of
Medicine, 3-9 Fukuura, Kanazawa-ku, Yokohama 236-0004, Japan.
2
Clinical Laboratory, Yokohama City University School of Medicine, Kanazawa-ku,
Yokohama 236-0004, Japan.
3
Second Department of Surgery, Yokohama City University School of Medicine,
Kanazawa-ku, Yokohama 236-0004, Japan.
Received August 24, 2000;
accepted after revision October 19, 2000.
Address correspondence to K. Numata.
Abstract
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SUBJECTS AND METHODS. Twenty-nine patients with 39 hepatocellular carcinoma lesions were examined. We scanned lesions before and after therapy using contrast-enhanced wideband harmonic gray-scale sonography after injection of a galactose—palmitic acid contrast agent. All patients held their breath for 20-50 sec after injection while the vascularity of the tumor was observed. We then monitored tumor enhancement between 60 and 180 sec after injection with patients breath-holding for a few seconds. Lesions were considered to exhibit viable tumor residue if hypervascular enhancement was observed in the tumor. We compared this enhancement with helical CT findings.
RESULTS. After therapy, 36 of the 39 lesions showed viable tumor residue on contrast-enhanced wideband harmonic gray-scale sonography, with no artifacts from iodized oil. Helical CT revealed a high-attenuation area in 12 of the 36 lesions, whereas 24 of the 36 lesions could not be evaluated for tumor residue as a result of artifacts from iodized oil accumulation in the tumor. The remaining three lesions showed complete deposition of iodized oil and complete necrosis on contrast-enhanced wideband harmonic gray-scale sonography.
CONCLUSION. Contrast-enhanced wideband harmonic gray-scale sonography is useful in evaluating the therapeutic effects of transcatheter arterial embolization for hepatocellular carcinoma.
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Contrast-enhanced wideband harmonic grayscale sonography is a promising new technique with high sensitivity for microbubble detection [5,6,7] that has recently been introduced for liver imaging, and its sensitivity in revealing tumor blood perfusion has been excellent [7,8,9,10]. Recently, we have been using contrast-enhanced wideband harmonic gray-scale sonography for diagnosing advanced hepatocellular carcinoma. This modality allows clear observation of hepatocellular carcinoma tumor enhancement, even when the tumor is located in the left lobe of the liver. We used this novel contrast-enhanced sonographic technique to evaluate residual tumor in patients with advanced hepatocellular carcinoma who have undergone transcatheter arterial embolization.
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Hepatocellular carcinomas were diagnosed at pathologic examination of biopsy specimens. Aspiration biopsies were performed with a 21-gauge fine needle (Sonopsy; Hakko, Tokyo, Japan) under conventional sonographic guidance. The size of the hepatic lesions was assessed on fundamental sonography. The mean maximal diameter (in millimeters) of the hepatocellular carcinoma lesions was 27 ± 16 mm (± SD). All patients had cirrhosis, and the diagnosis was made histologically, clinically, or both. The cause of the cirrhosis was alcohol in one patient, hepatitis B in three patients, hepatitis C in 24, and non-B, non-C hepatitis in one. According to Child's classification [11], 22 patients had class A cirrhosis and seven had class B.
All patients underwent contrast-enhanced wideband harmonic gray-scale sonography, helical CT, and digital subtraction arteriography. Informed consent was obtained from all patients and their relatives.
Contrast-Enhanced Wideband Harmonic Gray-Scale Sonography
In all patients, contrast-enhanced wideband harmonic gray-scale sonography
was performed before and 1 week after transcatheter arterial embolization.
Sonography was performed with a SONOLINE Elegra (Siemens Medical Systems,
Issaquah, WA) with a 3.5-MHz convex probe. Before IV bolus injection of the
300 mg/mL concentration of the galactose-palmitic acid mixture contrast medium
(Levovist; Schering AG, Berlin, Germany), the liver was scanned using
fundamental gray-scale imaging (transmit, 3.4 MHz; receive, 3.4 MHz). After
the injection, the liver was scanned using contrast-enhanced wideband harmonic
gray-scale sonography (transmit, 2.8 or 2.5 MHz; receive, 5.6 or 5.0 MHz) at
1-5 frames per second. We usually used 2 frames per second. The transmission
power was 100%, and the mechanical index values were between 1.5 and 1.9. The
focus position was just below the bottom of the tumor. Levovist is a
suspension of galactose (99.9%) stabilized with 0.1% palmitic acid. A 7 mL
dose of this agent was injected at 0.5 mL/sec via a 22- to 20-gauge cannula
placed in an antecubital vein. After bolus injection of Levovist, 5% glucose
was continuously infused at 5 mL/min. The patients gently inspired and then
breath-held for about 30 sec (20-50 sec after contrast medium injection) while
the tumor vessels and tumor enhancement were examined (observation of the
arterial phase) (Fig. 1A).
After observation of the arterial phase, we froze the image. We then reviewed
the images frame by frame from cine loop memories and stored them on
magneto-optical disks. This procedure takes approximately 15-35 sec (mean, 25
sec). We used this time for pooling the contrast agent in the hepatic
parenchyma. We scanned the whole tumor and observed tumor enhancement 60-180
sec after injection of the contrast agent while patients breath-held for a few
seconds (observation of the portal phase)
(Fig. 1B). If breath-holding
was poor, we changed the frame rate from 2 to 5 frames per second. We
subsequently froze the image again. We also reviewed these images on a
frame-by-frame basis with a cine loop and stored them on magneto-optical disks
for hard-copy printing. The portal phase was observed at least twice. If the
patient had more than one lesion, the same procedure was repeated after a
second injection of contrast medium. The full examinations were recorded on
S-VHS videotape.
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Before treatment, the intratumoral vascularity was analyzed. We evaluated the images for the presence of intratumoral vessels during the arterial phase. Lesions were judged to exhibit "hypervascular enhancement" if their enhancement was much greater than that of the surrounding liver parenchyma during the arterial phase. Hypervascular enhancement was further subdivided into homogeneous and heterogeneous patterns of enhancement according to findings in both the arterial and portal phases. After transcatheter arterial embolization, we evaluated the presence or absence of a hypervascular area within the tumor in the arterial phase and a hypervascular area within the tumor in the portal phase. When hypervascular areas were observed within the tumor, we considered them to be residual hepatocellular carcinoma lesions. If additional treatment was performed, the same procedure was carried out after therapy.
Helical CT
Helical CT was performed in all patients with a Proceed SE (General
Electric Medical Systems, Milwaukee, WI) before and 2 weeks after
transcatheter arterial embolization. A dual-phase study was obtained in each
patient as follows. First, an unenhanced helical sequence through the liver
was obtained. Next, after IV infusion of 100 mL of iohexol (Omnipaque; Sanofi
Winthrop Pharmaceuticals, New York, NY) into an antecubital vein at a rate of
3 mL/sec, an arterial phase sequence was performed after a delay of 25 sec,
followed by a portal venous phase sequence beginning 80 sec after starting the
contrast medium infusion. All images were obtained in helical mode with 7- or
10-mm collimation and a 7- or 10 mm/sec table-feed speed. Images were
reconstructed at 7- or 10-mm intervals.
Findings were evaluated subjectively by two observers who were unaware of the findings of contrast-enhanced wideband harmonic gray-scale imaging sonography. Lesions were considered hypervascular if they appeared more dense than the surrounding liver during the arterial phase. Before transcatheter arterial embolization, hypervascular lesions were further subdivided into homogeneous and heterogeneous patterns of enhancement. After transcatheter arterial embolization treatment, we evaluated the residual hepatocellular carcinoma represented by the hypervascular area in the arterial phase. We also evaluated the deposition of iodized oil and classified it as complete or incomplete.
Transcatheter Arterial Embolization Treatment
Before therapy, tumor vascularity was shown for all lesions on digital
subtraction arteriography. We performed transcatheter arterial embolization by
selectively introducing a microcatheter into the right or left hepatic artery
or a segmental branch of the hepatic artery and injecting a mixture of iodized
oil (Lipiodol; Andre Guerbet, Aulnay-sous-Bois, France) and styrene maleic
acid neocarzinostatin (1.0-6.0 mg per patient) (SMANCS; Yamanouchi
Pharmaceutical, Tokyo, Japan) or epirubicin hydrochloride (30-60 mg per
patient) (Farmorubicin: Pharmacia & Upjohn, Tokyo, Japan) in all patients.
This was followed by placement of a gelatin sponge (1 x 1 x 2 mm)
(Spongel; Yamanouchi Pharmaceutical) in 15 of the 29 patients.
Serum 
-Fetoprotein Levels
Serum -fetoprotein levels (normal range, <7 ng/mL) were measured
before and after treatment.
Statistical Analysis
Data are expressed as means ± standard deviations.
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Before therapy, helical CT showed a high-attenuation area in the arterial
phase in 37 of the 39 lesions. The remaining two lesions showed tumor staining
on digital subtraction arteriography. On helical CT, 26 of the 37
high-attenuation lesions had a homogeneous pattern; the other 11 had a
heterogeneous
pattern.
,
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Table 1 summarizes the results of contrast-enhanced wideband harmonic gray-scale sonography of assessment of the therapeutic effectiveness of transcatheter arterial embolization for advanced hepatocellular carcinoma. After therapy, only three of the 39 lesions showed complete necrosis. However, the remaining 36 lesions showed residual hepatocellular carcinoma (Figs. 2D and 3B). A hypervascular area was observed in 23 of the 39 lesions in the arterial phase (Fig. 1A), and a hypervascular area was observed in all 36 residual lesions in the portal phase (Figs. 1B, 2D, and 3B). We performed aspiration biopsy in five of the 36 residual lesions that had apparent hypervascular areas. Biopsies obtained from these hypervascular areas revealed viable hepatocellular carcinoma cells. Conversely, biopsy specimens obtained from areas that had no enhancement showed necrosis.
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Table 2 summarizes the results of contrast-enhanced wideband harmonic gray-scale sonography for assessing the therapeutic effectiveness of transcatheter arterial embolization for advanced hepatocellular carcinoma compared with helical CT findings. On helical CT, a high-attenuation area in the arterial phase was observed in 12 of the 36 lesions (Fig. 3A). The remaining 24 lesions could not be evaluated because of the presence of iodized oil (Fig. 2C). These 36 lesions showed incomplete deposition of oil in the tumor on helical CT, and all lesions had residual hepatocellular carcinoma on contrast-enhanced wideband harmonic gray-scale sonography. Only three lesions in which complete deposition within the tumor was observed on helical CT had complete necrosis on contrast-enhanced wideband harmonic gray-scale sonography. These three lesions in three patients were not additionally treated. These patients did not experience a recurrence for approximately 6-8 months after treatment. The absence of local recurrences in these patients was confirmed on contrast-enhanced harmonic gray-scale sonography.
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Thirty-six lesions that had residual hepatocellular carcinoma on contrast-enhanced wideband harmonic gray-scale sonography received additional treatment. Nineteen of the 36 lesions were treated with percutaneous ethanol injection therapy until the hypervascular areas disappeared on contrast-enhanced wideband harmonic gray-scale sonography (Figs. 2E and 3E). After percutaneous ethanol injection therapy, helical CT revealed no high-attenuation areas in the arterial phase of helical CT. The remaining 17 of the 36 lesions were treated with subsequent transcatheter arterial embolization therapy, and all 17 showed tumor staining on digital subtraction arteriography; however, after retreatment only one lesion showed complete necrosis on contrast-enhanced wideband harmonic gray-scale sonography. Therefore, 23 lesions in 19 patients showed complete necrosis on contrast-enhanced wideband harmonic gray-scale sonography at the end of the initial treatment series.
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During the follow-up periods (mean, 6.1 ± 2.6 months), 16 of the 29 patients experienced tumor recurrence, as assessed on follow-up contrast-enhanced wideband harmonic gray-scale sonography. In the 19 patients in whom complete necrosis was observed on contrast-enhanced wideband harmonic gray-scale sonography at the end of the initial treatment series, one patient experienced a local recurrence, and five patients developed new lesions. In the 10 patients in whom incomplete necrosis was observed on contrast-enhanced wideband harmonic gray-scale sonography after the initial therapy, all patients experienced local recurrences, and new lesions developed in six patients.
Serum -fetoprotein levels were evaluated before and after therapy in
the 26 patients in whom pretreatment serum levels were elevated. Serum
-fetoprotein levels decreased in all 16 patients who showed complete
necrosis of the tumor on contrast-enhanced wideband harmonic gray-scale
sonography after the initial therapy; levels returned to normal in two
patients (<7 ng/mL) and decreased to a slightly elevated level in 14
patients (between 10 and 50 ng/mL) after treatment. In 10 patients whose
lesions showed incomplete necrosis on contrast-enhanced wideband harmonic
gray-scale sonography, the serum -fetoprotein levels also decreased but
did not return to normal. The levels decreased to a slightly elevated level in
four patients (between 13 and 50 ng/mL) and decreased to levels greater than
50 ng/mL in six patients.
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In general, transcatheter arterial embolization was performed with iodized oil to improve the survival rate of patients with hepatocellular carcinoma as compared with the rate obtained without iodized oil [12]. However, when iodized oil is used, it becomes more difficult to assess the efficacy of transcatheter arterial embolization on helical CT because iodized oil accumulation in a tumor can mask residual tumor enhancement [2]. Dynamic MR imaging is reportedly useful in the evaluation of the effectiveness of transcatheter arterial embolization, because iodized oil has little influence on the signal intensity of MR imaging [13]. However, after treatment with transcatheter arterial embolization, the signal intensity of some hepatocellular carcinoma lesions changes from hypointense to hyperintense, which may make it difficult to evaluate tumor enhancement even on dynamic MR imaging [14]. In 1999, Catalano et al. [15] reported that contrast-enhanced color or power Doppler sonography is a simple and fast procedure and a sensitive technique for assessing the viability of hepatocellular carcinoma treated with transcatheter arterial embolization. Other investigators have also reported that contrast-enhanced harmonic power Doppler sonography can be effective in evaluating the vascularity of hepatocellular carcinomas because of the advantage of fewer power Doppler artifacts than contrast-enhanced conventional power Doppler sonography [16, 17]. However, using these methods, color flow is sometimes seen outside the lesions, which may result in an overestimation of viable lesions.
In this study, all advanced hepatocellular carcinoma lesions showed intratumoral vessels or hypervascular enhancement, or both, in the arterial phase of contrast-enhanced wideband harmonic gray-scale sonography before therapy. In the portal phase, hepatocellular carcinoma lesions were continuously enhanced until the arterial blood flow in the tumor began to wash out, and the liver parenchyma was also enhanced because of hepatic arterial and portal blood flow. Therefore, in the portal phase, there was no difference between enhancement of hepatocellular carcinoma lesions and that of the liver parenchyma. The necrotic area was not enhanced in either the arterial or the portal phase. In patients in whom tumoral blood flow disappeared completely after transcatheter arterial embolization therapy, arterial inflow was not recognized in the arterial phase, and the hepatocellular carcinoma lesions showed no enhancement in the portal phase. Therefore, these hepatocellular carcinoma lesions that were not viable were recognized as perfusion defects with an oval or round shape and distinct margins in the portal phase. On the contrary, residual hepatocellular carcinoma lesions were visualized as hypervascular areas within the tumor in the portal phase.
Using contrast-enhanced wideband harmonic gray-scale sonography after transcatheter arterial embolization treatment, we found that only three of the 39 lesions showed complete necrosis, whereas the remaining 36 lesions showed residual hepatocellular carcinoma. On helical CT, three lesions showed complete deposition of oil in the tumor, and high-attenuation areas in the arterial phase were observed in only 12 lesions. The remaining 24 lesions could not be evaluated as a result of the accumulation of iodized oil. These 24 lesions showed incomplete deposition in the tumor on helical CT and had residual hepatocellular carcinoma on contrast-enhanced harmonic gray-scale sonography. Contrast-enhanced wideband harmonic gray-scale sonography has no limitations attributable to the iodized oil; therefore, contrast-enhanced wideband harmonic gray-scale sonography is superior to helical CT in revealing viable portions of a hepatocellular carcinoma treated with transcatheter arterial embolization. Furthermore, it is possible to make an earlier diagnosis than with helical CT because there are no iodized oil artifacts, which makes possible subsequent treatment of such lesions using sonographically guided methods [18, 19]. In this study, we also performed percutaneous ethanol injection for the viable hepatocellular carcinoma areas recognized on contrast-enhanced wideband harmonic gray-scale sonography until these areas disappeared.
After transcatheter arterial embolization treatment, a hypervascular area was observed in 23 of the 36 lesions in the arterial phase, and a hypervascular area was observed in all 36 lesions in the portal phase of contrast-enhanced wideband harmonic gray-scale sonography. In regard to the diagnosis of the viability of hepatocellular carcinoma treated with transcatheter arterial embolization, the portal phase is more sensitive than the arterial phase in revealing residual hepatocellular carcinoma. We speculate that in the arterial phase, observation of tumoral blood flow became difficult because arterial flow had been decreased by embolization of the feeding arteries.
Using power Doppler or contrast-enhanced harmonic power Doppler sonography, other investigators have evaluated vascularity or the therapeutic effects of transcatheter arterial embolization for hepatocellular carcinoma lesions 20-25 mm or larger in diameter [4, 16]. Hosoki et al. [2] reported that for lesions located deeper than 7 cm, power Doppler sonography could not precisely reveal persistent tumor after treatment, resulting in many falsenegative findings. In this study, we evaluated hepatocellular carcinoma lesions 9 mm or greater in diameter located 10 cm or less from the skin surface. In this regard, contrast-enhanced wideband harmonic gray-scale sonography may be more sensitive than power Doppler or contrast-enhanced power Doppler examinations.
To obtain a good image of the portal phase, bubbles of contrast agent must be destroyed. Therefore, we used a high mechanical index to destroy all Levovist bubbles simultaneously. However, for lesions located deeper than 10 cm from the skin surface, destruction of Levovist bubbles was difficult because of the decreasing power of the ultrasound beam. If we were to use another contrast medium, one that could be destroyed more easily than Levovist, we might be able to evaluate lesions located deeper than 10 cm from the skin surface.
With power Doppler sonography, Solbiati et al. [19] used the microbubble contrast agent Levovist to reveal enhanced foci of residual untreated tumor in three (50%) of six intrahepatic colorectal metastases that had been identified on contrast-enhanced CT. Using color Doppler sonography, Goldberg et al. [20] reported that a synthetic microsphere sonographic contrast medium permitted the differentiation of radiofrequency-induced coagulation necrosis from inadequately treated tumor immediately after radiofrequency ablation in an animal tumor model. In this study, we compared viable lesions on contrast-enhanced wideband harmonic gray-scale sonography with pathologic findings after transcatheter arterial embolization treatment in only five patients because most hypervascular areas on contrast-enhanced wideband harmonic gray-scale sonography were not large enough to obtain exact specimens by aspiration biopsy under sonographic guidance.
However, all high-attenuation areas revealed on helical CT corresponded to
lesions showing hypervascular enhancement on contrast-enhanced wideband
harmonic gray-scale sonography. All lesions that were interpreted as showing
persistent viability on contrast-enhanced wideband harmonic gray-scale
sonography for which additional transcatheter arterial embolization was
performed showed tumor staining on digital subtraction arteriography. In all
patients who showed complete necrosis on contrast-enhanced wideband harmonic
gray-scale sonography, the serum -fetoprotein levels decreased to a
normal or slightly elevated level. During the follow-up periods, only one of
the 19 patients in whom complete necrosis was observed on contrast-enhanced
wideband harmonic gray-scale sonography experienced a local recurrence 6
months after treatment. Therefore, we believe that contrast-enhanced wideband
harmonic gray-scale sonography can distinguish viable from necrotic portions
of hepatocellular carcinoma lesions and that this method may be useful for
guiding additional treatments such as percutaneous ethanol injection or
radiofrequency ablation therapy.
Perfusion imaging techniques, such as contrast-enhanced wideband harmonic gray-scale sonography are useful for assessing the vascularity of advanced hepatocellular carcinoma lesions and residual tumor after transcatheter arterial embolization treatment. In addition, this method can be used to evaluate the effectiveness of percutaneous ethanol injection treatment for hepatocellular carcinoma. Contrast-enhanced wideband harmonic gray-scale sonography reduces the need for helical CT in evaluating the therapeutic effect of percutaneous ethanol injection during the course of treatment.
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