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Experimental Studies |
1 From the Department of Radiology, Massachusetts General Hospital, Boston, Mass (S.N.G., M.T.S., G.S.G.) and the Department of Research and Development, Acusphere, Cambridge, Mass (R.C.W., J.A.S.). Received August 25, 1998; revision requested October 28; final revision received February 18, 1999; accepted April 6. Supported in part by grants from Radionics, Burlington, Mass. S.N.G. supported in part by the RSNA Research and Education Foundation as a 1997 Cesare Gianturco/RSNA Fellow supported by the Cook Group. Address reprint requests to S.N.G., Department of Radiology, Beth Israel Deaconess Medical Center, 330 Brookline Ave, Boston, MA 02215 (e-mail: sgoldber@caregroup .harvard.edu). G.S.G. is a paid consultant to Acusphere. R.C.W. and J.A.S. are employees of Acusphere.
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Abstract |
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MATERIALS AND METHODS: VX2 (adenocarcinoma) tumors (0.8–1.5-cm diameter) were implanted into 12 rabbits. Gray-scale and color Doppler US were performed with or without intravenous injection of a US contrast agent composed of poly-lactide-co-glycolic acid polymeric (PLGA) microspheres (2-µm diameter) filled with perfluorocarbon gas. Radio frequency was applied to each nodule for 6 minutes at 127 mA ± 33 (mean ± SD) (tip temperature, 92°C ± 2). Repeat US with a second dose of the contrast agent was performed immediately after ablation. In four animals, a third dose was administered 30–120 minutes after ablation. Radiologic-histopathologic correlation was performed and included in vivo staining and studies of mitochondrial function.
RESULTS: Intense contrast agent enhancement was seen throughout the tumor prior to ablation. At gray-scale US, ablation produced hyperechoic foci, which were within 1 mm of the foci identified at histopathologic examination in seven of 12 animals (58%). After the administration of contrast material, foci devoid of previously visualized enhancement, which measured 7.3–15.0 mm, were identified. These were within 1 mm of the size of the foci identified at histopathologic examination in 11 of 12 animals (92%, P < .01). In two animals, enhancement depicted viable tumor, which appeared hyperechoic, on nonenhanced images. On delayed images, hyperechoic areas decreased in size, whereas the nonenhanced region remained unchanged.
CONCLUSION: A PLGA microspherical US contrast agent enabled the immediate detection of coagulation necrosis as a region devoid of contrast enhancement after radio-frequency ablation in rabbit hepatic tumors. Therefore, this agent could provide real-time guidance during complex ablative procedures and may provide an efficient technique for postprocedural assessment.
Index terms: Animals • Liver neoplasms, US, 761.321, 761.12988 • Radiofrequency (RF) ablation, 761.1269 • Ultrasound (US), contrast media, 761.12988 • Ultrasound (US), Doppler studies, 761.12983, 761.12988
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Introduction |
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The main goal of percutaneous ablation is complete eradication of the tumor. However, because adequate treatment of a given lesion is not always feasible with a single application of energy, an imaging strategy that can be used to reliably differentiate ablated tissue from residual foci of untreated tumor is necessary. Unfortunately, findings from gray-scale, color, and power Doppler US after ablation do not correlate well with the extent of induced coagulation necrosis (1–5,10). Specifically, it has been observed that either underestimation or overestimation of the zone of radio-frequency–induced coagulation necrosis may occur at US. Furthermore, the US appearance of the treated area changes rapidly after ablation such that the actual size of necrosis is difficult to estimate at US. Most investigators have, therefore, used iodine-enhanced computed tomography (CT) and gadolinium-enhanced magnetic resonance (MR) imaging to determine the extent of induced coagulation. For these imaging strategies, the absence of perfusion (ie, lack of enhancement within the treated focus) has been shown to correspond to regions of coagulation necrosis (1–5,11).
Recently, microbubble and other US contrast agents have been described (12,13). The increased echogenicity of these agents enables improved detection of parenchymal organ blood flow at contrast-enhanced US, as compared with routine color and power Doppler US (14). As a result, previously inapparent differences in vascularity between benign and malignant lesions can be detected (15–18). Given this ability to discriminate between areas of absent or low tissue perfusion, several investigators (10,19) have proposed the use of these US contrast agents to differentiate between ablated and nonablated tumor. In this study, we sought to evaluate this approach by using a synthetic polymeric US contrast agent to differentiate coagulation necrosis from untreated tumor immediately after radio-frequency ablation in an animal tumor model, with appropriate radiologic-histopathologic correlation.
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MATERIALS AND METHODS |
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Overall Study Design
Tumor implantation with VX2 adenocarcinoma was performed in 12 New Zealand White rabbits (body weight, 3.1–3.3 kg). Eight to 14 days after tumor implantation, the tumor-bearing liver was exposed at midline laparotomy. Baseline US was performed without or with administration of a US contrast agent (poly-lactide-co-glycolic acid polymeric [PLGA] microspheres; Acusphere, Cambridge, Mass). This was followed with a single application of radio frequency to induce tumor ablation. Repeat US was then performed immediately after radio-frequency ablation. In four animals (33%), a third contrast-enhanced US examination was performed 30–120 minutes after ablation. These US examinations were immediately followed with histopathologic studies to enable radiologic-histopathologic correlation. Two investigators (S.N.G. and G.S.G.) reviewed the US images by consensus at the time the studies were performed. All histopathologic specimens were reviewed by consensus (including S.N.G.) at the conclusion of the study.
Tumor Model
VX2 carcinoma was harvested from the thigh of a carrier rabbit, as previously described (20). By using aseptic technique and real-time US guidance, a 25-gauge needle was percutaneously inserted into the parenchyma of the left hepatic lobe. Suspensions of VX2 carcinoma (5 x 107 cells in 0.1–0.5 mL of Hanks buffered saline solution [Gibco, West Islip, NY]) were injected slowly over 30 seconds into the hepatic parenchyma. Contrast-enhanced (Omnipaque 350 [iohexol]; Nycomed Amersham, Princeton, NJ; 5-mL bolus administered manually) CT scanning was performed periodically in the 7–21 days after injection to follow up the growth of the hepatic tumor nodules. US examinations and radio-frequency ablation were performed once the tumors had reached a minimum of 8 mm in diameter.
Radio-frequency Technique
Tumor ablation was performed by using a radio-frequency generator (Series 3; Radionics, Burlington, Mass) that was capable of producing 150 W of power. Monitoring capabilities for temperature, tissue impedance, and current were incorporated into the circuitry of the radio-frequency generator. Twenty-one–gauge needle electrodes were used for all experiments. The needles were electrically insulated, except for the distal 1-cm metallic tip, by coating the needle shaft with a thin layer of acrylic resin.
The abdomen of each animal was shaved, and a grounding pad was placed in contact with this area. Positioning of the grounding pad was adjusted to minimize initial circuit impedance. Electrodes were then placed into the tumors with real-time US guidance. Radio frequency was applied through the electrode for 6 minutes, with a tip temperature of 92°C ± 2 (mean ± SD) (127 mA ± 33). A thermistor at the tip of the probe permitted continuous monitoring of probe temperature, which enabled manipulation of the power output of the generator. These parameters were selected based on findings from our previous work (21), which demonstrated maximal tissue coagulation without charring at these settings. Probe-tip temperature, tissue impedance, and wattage required were recorded at baseline and at 60-second intervals throughout the procedure.
US Technique
A 2-cm–thick, gelatinous, "stand-off" pad (Aquaflex; Parker Laboratories, Orange, NJ) was placed on the exposed liver to minimize near-field reverberation artifacts. Gray-scale (B-mode) and color Doppler US were performed by using an XP/128 scanner (Acuson, Mountain View, Calif) and a 7-MHz linear-array transducer. Power Doppler US and harmonic imaging were not used in this study. US settings included a depth of 40, power of -9 dB, and a logarithmic compression of 70 dB. The depth gain compensation curve included a near-field gain of 2, a slope of 4.5, a delay of 50, and a far-field gain of 0. Gain settings were maintained at optimized parameters (ie, the highest level of color gain without observed artifacts, as determined during initial preablation color Doppler imaging without contrast enhancement). For each animal, gain settings were not changed from this baseline for any of the pre- or postablation US studies. The pulse repetition frequency was maintained at 1 kHz for all studies.
US contrast agent enhancement was obtained by using 2-µm–diameter PLGA microspheres filled with perfluorocarbon gas at a dose of 4–8 mg/kg. These microspheres can be used for gray-scale enhancement and can induce an increase in signal enhancement of at least 40 dB in vitro. The contrast agent was reconstituted to a volume of 1 mL in aqueous diluent immediately prior to use. An intravenous injection of a bolus of the agent and an injection of 5 mL of a 5% dextrose solution were administered over 10 seconds. During and after the administration of contrast material, monitoring was performed by using a combination of gray-scale and color Doppler US. A minimum of 5 minutes of imaging was recorded after each administration of contrast material. Eight animals received two doses of contrast material (before ablation and 15–20 minutes after ablation), and four received a third dose of contrast material (30–120 minutes after ablation). The minimal interval between administration of contrast doses was 30 minutes.
Histopathologic Assessment of Coagulation Necrosis
Rabbits were sacrificed with an overdose of pentobarbital sodium (Somlethal; Anpro Pharmaceutical, Arcadia, Calif) after the postablation US studies. In seven rabbits, 10 mL of 2% Evans blue, an in vivo dye that is used to detect vascular perfusion and cellular viability, were injected into a dorsal ear vein 30 minutes prior to sacrifice. Pathologic analysis was performed in all rabbits. The visible region of coagulation necrosis was measured with calipers in fresh tissue prior to preservation in 10% formalin. Measurements were based on a consensus of the two observers. Specimens from the five rabbits that did not receive Evans blue were stained separately with hematoxylin-eosin and 2,3,5-triphenyltetrazolium chloride (Sigma Chemical, St Louis, Mo), a marker for mitochondrial enzyme activity (22). These samples were fixed in 2% 2,3,5-triphenyltetrazolium chloride for 30 minutes at room temperature and were sectioned for examination at light microscopy. All specimens were examined and fixed within 1 hour of sacrifice.
Data Analysis
Findings on immediate and delayed gray-scale and color Doppler US images were compared with findings from baseline images and histopathologic studies. The accuracy of contrast-enhanced and conventional color Doppler US in identifying the extent of tumor ablation was determined by using histopathologic findings as the standard. Radiologic-histopathologic correlation was performed. The Student t test was used to compare the accuracy of findings at conventional and contrast-enhanced US.
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RESULTS |
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Histopathologic Findings
Findings at histopathologic analysis confirmed the presence of a solitary focus of induced coagulation necrosis that measured 6–14 mm in diameter (8.9 mm ± 2.2). In 11 animals (92%), a contiguous area of cell death was observed. However, in the animal in which a focus of enhancement was identified on postablation contrast-enhanced images, an island of viable tumor cells surrounded a 1-mm intratumoral vessel that traversed the ablated focus (Fig 3b).
Radiologic-Histopathologic Correlation
The hyperechoic region observed immediately after ablation on nonenhanced images corresponded to an area the size of which was within 1 mm of the size of the ablated focus in only seven of the 12 animals (58%). The hyperechoic focus caused overestimation of the treated area in four animals (33%) and underestimation of the ablated region in one animal. Thus, in four animals in which the extent of induced coagulation was overestimated at US, contrast-enhanced images enabled detection of viable tumor that otherwise would have been missed. At delayed scanning, the hyperechoic area caused underestimation of the ablated focus by more than 5 mm in two of the four animals (50%).
The use of PLGA microspheres enabled greater accuracy in differentiating ablated from untreated viable tumor. The diameter of the nonenhanced focus after contrast administration was within 1 mm of the diameter of the histopathologically proved area of ablation in 11 of the 12 animals (92%; P < .01). In one animal, the area of contrast enhancement caused overestimation of the region of treatment by 2.5 mm; and in two animals, enhancement was seen in regions of tumor that were hyperechoic at US but viable at histopathologic examination (Fig 2). Thus, in these two animals, the foci of contrast enhancement allowed the detection of viable tumor that would have been missed by using nonenhanced imaging alone.
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DISCUSSION |
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After the administration of PLGA microspheres, areas of coagulated tumor appeared as foci devoid of previously visualized (ie, preablation) enhancement at color Doppler US. The size of these nonenhanced areas were within 1 mm of the areas of histopathologically proved coagulation in 11 of the 12 animals (92%) and were used to predict the extent of necrosis more accurately than were the induced hyperechoic areas that were visualized on nonenhanced images (58%; P < .01). Furthermore, the nonenhanced focus did not change in size or appearance on follow-up images obtained 30–120 minutes after ablation, whereas echogenicity seen on nonenhanced images gradually decreased.
In one animal, however, a tiny solitary focus of contrast agent enhancement was identified within the ablated zone. At histopathologic analysis, this was found to correspond to an intratumoral vessel that was surrounded by a thin rim of viable tumor cells. This finding has important therapeutic and diagnostic implications. Previously, perfusion-mediated tissue cooling has been reported to limit the overall diameter of coagulation necrosis and to prevent complete ablation of tumors near large (>3-mm) intrahepatic vessels (23). To our knowledge, more central residual perivascular malignancy adjacent to tumor vasculature has not been described. However, because the potential presence of these residual small foci of malignancy has been established, determination of the adequacy of the ablation will require either high-spatial-resolution imaging (possibly requiring resolution better than the current resolution of MR imaging and CT) or long-term follow-up to detect interval tumor growth. Fortunately, findings from the current study demonstrate that US contrast agent enhancement with PLGA microspheres can be used to detect these residual foci within the tumor at the time of initial ablative therapy.
These study findings confirm previous observations concerning the limited utility of gray-scale, nonenhanced US findings in predicting the extent of radio-frequency–induced coagulation necrosis. We have previously noted that hyperechoic areas that surround the electrode immediately after the application of radio frequency were variable in size and contour and often were reduced in size or disappeared over 15–30 minutes of follow-up; they did not correlate with the extent of coagulation necrosis, as measured at CT or histopathologic examination (2,5). Lorentzen et al (24) also previously reported that the induced hyperechoic zone caused underestimation of the diameter of coagulation necrosis in an ex vivo liver.
Refinements in technique will likely increase the usefulness of US contrast agents in the detection of residual foci of untreated tumor. The use of the intravenous infusion technique has been reported to prolong the duration of useful enhancement with other US contrast agents and may prove beneficial for PLGA microspherical contrast agents, as well (25). Comparisons between PLGA microspherical and other US agents to determine which, if any, has greater clinical utility will also need to be performed. Furthermore, studies in humans, with a range in specific tumor types, will need to be performed to confirm the results obtained in this animal model.
The notion of using US contrast agents to direct therapy has been advanced by Hashimoto et al (19), who used carbon dioxide microbubbles to differentiate hypervascular hepatocellular carcinomas, for which transarterial chemoembolization was indicated, from hypovascular tumors, which were treated with percutaneous instillation with ethanol. In addition, Solbiati et al (10) used the microbubble contrast agent SH U 508A (Levovist; Schering, Berlin, Germany) to identify enhanced foci of residual untreated tumor in three of six (50%) intrahepatic colorectal metastases that were identified at contrastenhanced CT.
The use of US contrast agents at the time of initial treatment may improve therapy by reducing (or eliminating) the need for CT or MR imaging studies to be performed during the course of therapy, which are currently required to ascertain complete treatment of a given tumor. Contrast-enhanced US performed immediately after ablation clearly would be more convenient and likely would be less expensive than the current combined approach. This strategy may also reduce the number of sessions required for treatment, as residual enhanced regions of tumor potentially could be treated at the time of initial therapy. In addition, US contrast agent enhancement ultimately may be used to direct electrode placement to enhanced, and thus viable, foci of residual tumor at the initial or subsequent treatment sessions. Furthermore, the use of intravascular US contrast agents also may be beneficial, compared with the use iodinated CT contrast media, as the US agents do not distribute into the extracellular space and, therefore, should permit more accurate demonstration of persistent blood flow to untreated tumors.
One potential limitation of our study is the possibility that blooming artifact within enhanced untreated tumors could have altered our results. Yet, this artifact, if present, detracted little from the ability of the PLGA contrast agent to accurately discriminate between coagulation and residual viable tumor. The presence of increased signal from blooming would tend to result in the underestimation of the volume of radio frequency–induced necrosis by producing signal where no flow was present. However, findings at histopathologic analysis, which included the use of the perfusion agent Evans blue, revealed that the nonenhanced areas were within 1 mm of the zone of coagulation in 92% of the animals.
The PLGA agent used in our study provided intense changes in signal within the untreated tumor and liver for extended periods. A mosaic enhancement pattern was identified within discrete visible vessels and also in the parenchymal tissue. The biophysical mechanisms that account for these observations stem from the fact that these synthetic microspheres are not physically destroyed at routine US and that they exhibit a low rate of degassing during imaging (R.C.W., unpublished data, 1996). This effect changes the acoustic response of sufficient numbers of the microspheres to provide signal enhancement during the cross-correlational analysis performed with the machine as a part of the Doppler imaging process. The enhancement with the contrast agent at Doppler US indicates the location of functional capillary beds (including liver sinusoids and VX2 carcinoma) into which the contrast agent has entered. Enhancement lasts for several minutes, which is the duration necessary for complete degassing of the agent. Mosaic enhancement can be attributed to the changes in microbubble size, as they are affected by the interrogating acoustic wave. These changes are of sufficient strength to be detected above the wall filter but are too low to allow sufficient signal strength to generate blooming artifacts outside the viable tissues at the doses and machine settings used in this study.Practical applications: A synthetic PLGA-based, perfluorocarbon-filled, microspherical US contrast agent enables the immediate detection of coagulation necrosis after radio-frequency ablation in rabbit VX2 tumors as a region devoid of contrast agent enhancement. The use of this agent after initial ablative therapy in the clinical setting could potentially lead to fewer intervening diagnostic imaging studies, such as contrast-enhanced CT or MR imaging, which are currently required to adequately assess the complete treatment of a given tumor. An agent such as this, if shown to be effective in human hepatic tumors, could provide an efficient technique for postprocedural follow-up imaging. In addition, such an agent may, therefore, ultimately prove useful in the real-time guidance of therapy during complex ablative procedures that require a staged approach to treatment, with multiple electrode insertions.
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Acknowledgments |
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Footnotes |
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Author contributions: Guarantors of integrity of entire study, S.N.G., G.S.G.; study concepts and design, S.N.G., G.S.G.; definition of intellectual content, S.N.G., R.C.W., G.S.G.; literature research, S.N.G., R.C.W., G.S.G.; experimental studies, all authors; data acquisition, S.N.G., R.C.W., M.T.S.; data analysis, S.N.G., G.S.G.; statistical analysis, S.N.G., G.S.G.; manuscript preparation, S.N.G., G.S.G.; manuscript editing, S.N.G., J.A.S., R.C.W., G.S.G.; manuscript review, all authors.
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