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1
Servizio di Radiologia, Ospedale Civile via Cesare, Battisti 25, Vimercate,
Milano, Italy.
2
Department of Radiology, Beth Israel Deaconess Medical Center, 330 Brookline
Ave., Boston, MA 02215.
3
Servizio di Radiologia, Ospedale Maggiore, Largo Donatori Sangue 1, Lodi,
Italy.
4
Istituto di Radiologia, Universita Degli Studi di Roma "La
Sapienza" Roma, Italy.
5
Istituto di Radiologia, Universita di Pavia Piazzale, Golgi 1, Pavia,
Italy.
Received September 18, 2000;
accepted after revision January 30, 2001.
Address correspondence to S. N. Goldberg.
Abstract
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MATERIALS AND METHODS. Thirty-five consecutive patients (24 men and 11 women; mean age, 64 years) with 43 hepatocellular carcinomas (3.6 ± 1.1 cm) were treated using internally cooled radiofrequency ablation therapy. Therapeutic response was evaluated at 4 months with dual-phase contrast-enhanced helical CT, conventional power Doppler Sonography, and pulse inversion harmonic imaging using a sonographic contrast agent (SH-508). CT and sonographic studies were reviewed separately in random order by four radiologists at different consensus conferences. Sensitivity and specificity of the sonographic methods were determined using CT as a gold standard and results were compared using the McNemar test.
RESULTS. CT examinations identified residual tumor in 12 lesions (27.9%). Although conventional contrast-enhanced power Doppler sonography identified residual viable tumor foci in four incompletely treated lesions (9.3%), contrast-enhanced pulse inversion harmonic imaging identified residual tumoral enhancement in 10 lesions (23.3%). Thus, the sensitivity of pulse inversion harmonic imaging (83.3%) was significantly greater (p < 0.05) for detecting residual nonablated tumor compared with conventional contrast-enhanced power Doppler sonography.
CONCLUSION. Our study suggests that contrast-enhanced pulse inversion harmonic imaging may enable the detection of residual nonablated tumor in more cases than contrast-enhanced power Doppler sonography and may ultimately prove to be a useful adjunct for percutaneous ablation therapies. Nevertheless, contrast-enhanced axial imaging (CT or MR imaging) is currently the most sensitive test for managing thermal ablation for patients with hepatocellular carcinoma.
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Investigators have recently gained significant experience using radiofrequency ablation and have achieved complete tumor necrosis in 80-90% of hepatocellular carcinomas measuring less than 3.0 cm in diameter [7, 9, 10]. Additionally, favorable results (65% complete ablation) have been documented for encapsulated lesions measuring 3-5 cm [11]. Furthermore, these encouraging results have been obtained while simultaneously markedly reducing the number of sessions required for appropriate treatment compared with the use of percutaneous ethanol injection (1.2 vs 4.8 sessions) [10].
One key issue concering radiofrequency ablation and other thermal therapies is that of proper evaluation of treatment efficacy [2, 3]. Currently, contrast-enhanced axial imaging (either biphasic CT with iodinated contrast enhancement or dynamic MR imaging) is considered the mainstay for evaluating the therapeutic efficacy of thermal oblation [2,3,4,5,6,7,8,9,10, 18] because gray-scale, color Doppler, and power Doppler sonographic findings cannot adequately differentiate between treated and residual viable tumor [8, 9, 18]. CT (and MR imaging) examinations rely on the identification of residual foci of enhancement for inadequately treated tumors, compared with the absent perfusion noted in coagulated tissues [18]. However, given the spatial resolution of CT and MR imaging and the difficulty of achieving adequate margins of tissue ablation around treated lesions [2], long-term imaging follow-up has been necessary to document the presence or absence of small foci of residual tumor in the treatment zone.
Recently, several investigators advanced the notion of using sonographic contrast agents to permit the identification of residual foci of untreated tumor after radiofrequency ablation [19, 20]. Although Goldberg et al. [19] have shown radiologic-pathologic correlation to 1 mm in 92% of tumors in animals, Solbiati et al. [20] reported the detection of residual tumor in only three (50%) of six patients with hepatic metastases. Thus, improvements in the sensitivity and validation of the sonographic contrast material's usefulness for follow-up after ablation of hepatocellular carcinoma are still required.
Pulse inversion harmonic imaging is an advanced sonographic technique that is capable of enhancing visualization of microbubble contrast agents because of improved contrast to tissue conspicuity [21,22,23,24]. We hypothesize that this technique may improve the utility of sonographic contrast agents for evaluating the response of primary hepatocellular carcinoma nodules after radiofrequency ablation. Thus, the purpose of this study was to compare the efficacy of contrast-enhanced harmonic imaging with conventional power Doppler sonography and helical CT to determine the incomplete local treatment for a well-defined population of patients with hepatocellular carcinoma.
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In all patients the pretreatment workup included a power Doppler
sonographic examination with and without contrast material, unenhanced and
dual-phase helical CT, and marker levels of 
-fetoprotein and
des-gammacarboxy-prothrombin (DCP). Biopsy confirmation was performed in 17
(48.6%) of these patients because their -fetoprotein levels were less
than 200 ng/mL or their DCP levels were normal, and the sonography and CT
findings were not pathognomonic for the diagnosis of hepatocellular carcinoma.
The remaining 18 patients (51.4%) had hypervascular lesions in the setting of
cirrhosis, with markedly elevated -fetoprotein levels (>200
ng/mL).
Radiofrequency Ablation Technique
Written investigational review board approval was obtained before the
initiation of this study. All patients provided written informed consent to
undergo the treatment. The ablation procedure was performed under real-time
sonographic guidance (AU 5 or ASTRO; Esaote Biomedica, Genoa, Italy). A guide
device incorporated into the sonography probe (Hitachi, Tokyo, Japan) was used
to assist the radiofrequency electrode placement in all cases. In cases in
which treatment required only one electrode insertion (solitary lesions <3
cm, n = 19), the patient was placed under conscious sedation, and the
treatment was performed using an intramuscular injection of 0.5 mg of atropine
sulfate (Atropina; SALF, Bergamo, Italy), 1:3 oral drops/kg of diazepam
(Ansiolin; Doppel, Piacenza, Italy), 2.5 mg of IV droperidol (Sintodian;
Farmitalia, Milan, Italy), 30 mg of IV ketrolac trometamine (Lixidol; Roche,
Milan, Italy), and 200 mg of IV tramadole cloridrate (Fortadol; Bayer, Milan,
Italy) 1 hr before treatment. In the remaining 16 patients, treatment was
performed under general anesthesia, according to protocol.
Patients were continuously monitored before, during, and after the
procedure. After the patient's skin was cleansed with iodized alcohol, the
most appropriate approach to target the lesion was chosen. For lesions located
in the right lobe, an intercostal approach was often preferred, whereas for
lesions located in the left lobe, a subcostal approach was generally used. A
20-cm-long, 18-gauge internally cooled radiofrequency electrode (Radionics,
Burlington, MA) with 2-3 cm of exposed metallic tip was used to deliver the
radiofrequency to the tissue
[25]. Thirty-two lesions were
treated using a single electrode, and 11 larger lesions (
4.0 cm) were
treated with triple-cluster electrodes
[26]. Grounding was achieved
by attaching two to four dispersive pads, each with a 100 cm2
surface area, to the patient's thighs. The electrode was then attached to a
500-kHz, 200-W radiofrequency generator (series CC-1; Radionics). Tissue
impedance was monitored continuously using circuitry incorporated in the
generator. A peristaltic pump (Watson-Marlow, Medford, MA) was used to infuse
0°C normal saline into the cooling lumen of the electrode at a rate
sufficient to maintain a tip temperature of 20-25°C.
For each treatment session, a single radiofrequency electrode was positioned at the center of the tumor. Initially, after the baseline tissue impedance was measured, generator output was slowly increased from 1000 to 2000 mA. Radiofrequency energy was then applied for 10-12 min using a pulsed technique according to a previously described automated algorithm [27]. Only one application of radiofrequency was used for each tumor measuring less than 3 cm, with up to three insertions during a single session for larger tumors. Only one treatment session was performed in every patient before the initial 4-month imaging evaluation. The mean total procedure time was approximately 40 min per session. After the radiofrequency procedure, the patients were observed for 48 hr; and if no complications occurred, they were discharged.
Assessment of Therapeutic Efficacy
To evaluate response to radiofrequency therapy, we performed
contrast-enhanced CT scanning, and both power Doppler and pulse inversion
harmonic imaging using a sonographic contrast agent (SH-508, Levovist;
Schering, Berlin, Germany) on all patients
[28,
29]. Comparison examinations
were performed 4 months after the procedure. These examinations were performed
within 1 week of each other (median, 3 days). This time was selected because
of the concern for potential errors in interpretation at earlier follow-up
from confounding, false-positive enhancement caused by the transitory
peripheral rim of reactive hyperemia that has been observed in many cases when
imaging is performed within 3 months of the ablation procedure
[3]. Tumor necrosis was
considered complete when no foci of enhancement were seen within the lesion on
CT scans, or if no enhancement was detected during the pulse inversion study
[18]. In cases in which
residual tumor was identified, a second radiofrequency treatment session was
performed within 2 weeks of diagnosis. The efficacy of all treatments was
reassessed on CT follow-up 4-6 months later (i.e., at 8-10 months). Biopsies
were not performed.
Sonographic Contrast-Enhanced Technique
Patients were scanned using an HDI 5000 scanner (Advanced Technology
Laboratories. Bothell, WA) with a C5-2 probe. For each session, sonography
consisted of conventional gray-scale imaging to identify anatomic landmarks;
Power Doppler sonography was performed before and after the injection of
SH-508; and pulse inversion harmonic scanning was performed after the
administration of a second dose of SH-508. For both injections, the SH-508
sonographic contrast agent was administered as an IV hand-injected bolus of 11
mL (at a flow rate of approximately 2 mL/sec) at a concentration of 300
mg/mL.
For this study, power Doppler settings included midvelocity scale (pulse repetition frequency, 1-1.5 kHz); persistence, medium; frame rate, high; two-dimensional optimization, high resolution. Pulse inversion harmonic settings included persistence, 0; frame rate, high; two-dimensional optimization, color sensitivity index = 3. Pulse inversion harmonic scanning (mechanical index, 1.1-1.3) was performed at 4- to 6-sec intervals from 20 sec after a second injection of SH-508 (during the hepatic arterial phase) for 60-80 sec using a single-frame acquisition mode, rather than continuous imaging. This type of intermittent imaging was considered optimal because it facilitates the sonication (perturbation by the ultrasound beam) of the contrast microbubbles, thereby increasing the contrast signal [22]. Additionally, the relatively long interval between scans permits the constant refilling of the region of interest with new contrast microbubbles, thus enabling improved visualization and differentiation of the sonographic contrast enhancement patterns of focal liver lesions and normal tissues [23, 24]. A complete scan of the entire liver was obtained during the late phase (2 min after injection) using a single sweep through the entire lesion. For all sonographic studies, the focal zone was set to the lower third of the sonographic field. VHS recordings were obtained for the entire examination, with still images recorded on optical disk. These images were subsequently reviewed on a frame-by-frame basis.
CT Technique
CT (Twin Flash; Elscint, Haifa, Israel) was performed using a helical
technique (5-mm-thick sections, 7-mm collimation, 1:1.4 pitch, 120-140 kVp
280-300 mA). Unenhanced images were acquired first and were followed by
dual-phase contrast enhancement during the power injection of 150 mL of 60%
iopamidol (Iopamiro; Bracco, Milan, Italy) at the rate of 3-4 mL/sec. The
entire liver was scanned twice: first at 25-30 sec (arterial phase), and then
at 60 sec (portal phase) after the initiation of contrast injection.
Image Analysis
The criteria used to determine the residual, inadequately treated tumor
were based on the presence or absence of hypervascular enhancement as reported
by several previous investigators
[7,8,9,10,
18]. All lesions were viewed
as one large study group as a result of our rigidly defined study entrance
criteria that provided a homogenous population of small hypervascular lesions.
All studies were reviewed in a blinded fashion at consensus conferences in
which four of the authors participated. Comparison studies (the initial
preprocedural or intraprocedural scans) were not provided for this
retrospective analysis. The 35 CT and sonographic examinations were reviewed
during three separate sessions separated by 1 week each. In addition, the
studies (CT, power Doppler sonography, and pulse inversion harmonic images)
were viewed in three different random orders to further eliminate the
possibility of reviewer bias. Results were tabulated, and positive findings
were compared at the fourth consensus conference. The CT findings 8-10 months
after the initial ablation were also reviewed at this time. Sensitivity and
specificity of conventional and pulse inversion harmonic sonography were
determined using the CT findings as a gold standard. Results were compared
using a one-tailed paired McNemar test ( = 0.05).
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All patients tolerated the sonographic contrast agent as administered without signs of adverse reactions or side effects. Conventional power Doppler sonography identified the presence of residual viable tumor foci in four (9.3%) of 43 lesions, and no sign of viable residual tumor was detected in the remaining 39 lesions. Thus, power Doppler contrast-enhanced sonography identified only four (33.3%) of the 12 incompletely treated lesions. Hence, the specificity of the conventional contrast-enhanced power Doppler sonographic examination was 100%, but the sensitivity was only 33.3%. The positive predictive value was 100%, and the negative predictive value was 76.9%.
Studies using pulse inversion harmonic imaging with sonographic contrast material identified residual tumor enhancement in 10 (23.3%) of 43 lesions, including all lesions identified by conventional contrast-enhanced power Doppler sonography (Figs. 1A,1B,1C,1D and 2A,2B,2C). The greatest conspicuity of these enhancing foci was seen in the early hepatic arterial phase (approximately 25-40 sec after the sonographic contrast bolus) (Fig. 3A,3B). The morphology and dimensions of these persistent foci of enhancement were identical to the appearance on CT imaging in nine cases (90%) (Figs. 1A,1B,1C,1D,2A,2B,2C,3A,3B). However, the pulse inversion harmonic study underestimated the extent of enhancement and viable tumor in one case (10%). Pulse inversion harmonic imaging did not identify enhancement in any of the remaining 33 lesions. Hence, the sensitivity of the pulse inversion study was 83.3%, with a specificity of 100%. The positive predictive value was 100%, and the negative predictive value was 93.9%. Thus, the sensitivity of the pulse inversion technique and the negative predictive value were significantly greater (p < 0.05, McNemar test) for detecting residual nonablated tumor compared with conventional contrast-enhanced power Doppler sonography. However, the specificity and positive predictive values were not significantly different.
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Clinical success for the treatment of focal liver tumors has been generally thought to require complete destruction of the entire tumor. If this goal is to be accomplished using radiofrequency ablation techniques, robust diagnostic imaging techniques will be required for precise lesion targeting and for determining the extent of induced coagulation necrosis. In the past, gray-scale and power Doppler sonography have been used primarily to guide electrode placement [7,8,9,10,11]. However, most authors have relied on contrast-enhanced CT and MR imaging after treatment to help differentiate between avascular, nonenhancing coagulated tumor and residual nonablated foci that display tumoral enhancement. Although this approach enables efficacious therapy, the multiple imaging modalities required for ensuring tumor eradication are cumbersome and expensive.
Although conventional gray-scale sonography has been extremely useful for directing real-time placement of radiofrequency electrodes, sonographic findings after ablation (hyperechogenicity surrounding the electrode) are variable and do not correlate well with overall necrosis shape and volume [18, 19]. Previous studies describe the possibility of increasing the sensitivity rate of conventional power Doppler sonography by enhancing the scan using IV-administered sonographic contrast agents [20, 30]. However, our results, in which conventional contrast-enhanced power Doppler sonography detected only 25% of residual viable tumor foci, confirm the findings of Solbiati et al. [20] and Bartolozzi et al. [30] that this strategy alone is insufficient for detecting all residual tumor in every case. Our study further underscores the importance of detecting these foci at the earliest time possible, because almost all foci of progressive tumor growth identified 4 months after initial treatment were sufficiently small when identified to permit additional, definitive treatment.
One recent advance in sonographic techniques has been the development of pulse inversion harmonic imaging [21, 25]. Pulse inversion harmonic imaging is a new contrast material—specific method in which two pulses are transmitted down each ray line, instead of only a single pulse found with conventional and harmonic B-mode sonographic imaging. The first is a normal pulse, whereas the second is an identical copy of the first with its phase inverted. Hence, whenever there is a positive pressure from the first pulse, there is an equal negative pressure from the second. For normal static tissues that respond linearly to a sonographic field, this method of dual sonographic interrogation will reflect back to the transducer equal but opposite waveforms. Because these sound waves are summed at the beam former, all linear targets cancel and no signal is generated. However, microbubbles, which produce nonlinear backscatter, respond differently to phase inverted pulses and do not reflect identical inverted waveforms. The irregular vibration and sonication of contrast microbubbles dephase both interrogating ultrasound beams and amplify the echo signals in tissues containing this material. Thus, the harmonic component is greatly enhanced, with improved signal recorded.
On a clinical level, Wilson et al. [23] showed improved characterization of liver lesions, particularly their vascularity, using pulse inversion harmonic imaging compared with conventional color Doppler sonography. Additionally, Dalla Palma et al. [24] reported improved intrahepatic lesion characterization over conventional power Doppler sonography and an increase in the number of lesions detected in 22% of patients when compared with contrast-enhanced CT. Our study shows that the use of pulse inversion harmonic imaging increases the sensitivity of sonographic contrast techniques for the detection of residual viable tumor in hepatocellular carcinoma nodules after treatment with radiofrequency. Specifically, pulse inversion harmonic imaging identified the presence of additional viable tumor in six cases, and increased the sensitivity of sonographic detection by 50%, from 33.3% to 83.3%.
In this study, contrast-enhanced CT was more sensitive for detecting residual vascular enhancement in radiofrequency-ablated hepatocellular carcinoma nodules than either sonographic method. One possible explanation that may, in part, account for this difference is that our sonographic protocol permitted the analysis of only a single representative slice through the lesion, whereas multislice CT permitted systematic evaluation of the entire lesion. Hence, further advances or improvements in technique will be necessary if sonographic contrast methods are to replace axial imaging as the method of choice. Much research is being conducted on the formulation of new contrast agents that are reported to show greater lesion conspicuity than SH-508 [19, 28, 31, 32]. Additionally, improved methods of SH-508 administration, including a constant drip technique, have been reported [33]. Further refinement to harmonic imaging can also be anticipated.
The use of sonographic contrast agents may offer potential benefits over other imaging strategies. For example, it is possible that sonographic contrast enhancement will permit the guidance of therapy in real time by enabling the direction of the radiofrequency electrodes to foci of residual enhancement. Furthermore, with CT, contrast enhancement is less than ideal because of errors in timing of the contrast bolus that cannot always be corrected immediately with repeated scanning because of toxicity; however, real-time scanning and the ability to administer repeated doses of sonographic contrast material may afford an advantage in some cases for detecting residual tumor. Additionally, it is possible that fewer enhancement artifacts, such as the peripheral rim of enhancement acutely after ablation, will be seen with pulse inversion sonography compared with CT. This, in turn, could lead to earlier detection of residual disease because interpretation of CT scans obtained before 3 months after ablation is difficult given the persistent uniform hyperemia present. Clearly, the answer to these questions will require further study. Given the relative limitations of our study, including the short-term follow-up and the small number of patients studied, further research will be required to validate the results of our initial findings.
In conclusion, the results of our study suggest that contrast-enhanced pulse inversion harmonic imaging may enable the detection of residual nonablated tumor in more patients than contrast-enhanced power Doppler sonography alone. As a result, the use of sonographic contrast agents may ultimately prove to be a useful adjunct for percutaneous ablation. Nevertheless, contrast-enhanced CT remains the most sensitive test for appropriately managing thermal ablation for patients with hepatocellular carcinoma.
Acknowledgments
We thank our nurses, Marisa Brambilla and Manuela Granata, for their
assistance in performing the radiofrequency ablation procedures and in helping
to administer the sonographic contrast media.
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