DOI: 10.1148/radiol.2441052054
(Radiology 2007;244:151-156.)
© RSNA, 2007
Microwave Ablation with Multiple Simultaneously Powered Small-gauge Triaxial Antennas: Results from an in Vivo Swine Liver Model1
Christopher L. Brace, PhD,
Paul F. Laeseke, BS,
Lisa A. Sampson, CVT,
Tina M. Frey, RT(R),
Daniel W. van der Weide, PhD, and
Fred T. Lee, Jr, MD
1 From the Departments of Radiology (C.L.B., L.A.S., T.M.F., F.T.L.), Biomedical Engineering (P.F.L.), and Electrical and Computer Engineering (D.W.v.d.W.), University of Wisconsin–Madison, 600 Highland Ave, Madison, WI 53792-3252. Received December 16, 2005; revision requested February 10; revision received September 20; accepted November 3; final version accepted November 8. Supported by National Institutes of Health Grant R21 RR018303-01.
Address correspondence to C.L.B. (e-mail: clbrace{at}wisc.edu).
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ABSTRACT
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Purpose: To prospectively investigate the ability of a single generator to power multiple small-diameter antennas and create large zones of ablation in an in vivo swine liver model.
Materials and Methods: Thirteen female domestic swine (mean weight, 70 kg) were used for the study as approved by the animal care and use committee. A single generator was used to simultaneously power three triaxial antennas at 55 W per antenna for 10 minutes in three groups: a control group where antennas were spaced to eliminate ablation zone overlap (n = 6; 18 individual zones of ablation) and experimental groups where antennas were spaced 2.5 cm (n = 7) or 3.0 cm (n = 5) apart. Animals were euthanized after ablation, and ablation zones were sectioned and measured. A mixed linear model was used to test for differences in size and circularity among groups.
Results: Mean (±standard deviation) cross-sectional areas of multiple-antenna zones of ablation at 2.5- and 3.0-cm spacing (26.6 cm2 ± 9.7 and 32.2 cm2 ± 8.1, respectively) were significantly larger than individual ablation zones created with single antennas (6.76 cm2 ± 2.8, P < .001) and were 31% (2.5-cm spacing group: multiple antenna mean area, 26.6 cm2; 3x single antenna mean area, 20.28 cm2) to 59% (3.0-cm spacing group: multiple antenna mean area, 32.2 cm2; 3x single antenna mean area, 20.28 cm2) larger than 3 times the mean area of the single-antenna zones. Zones of ablation were found to be very circular, and vessels as large as 1.1 cm were completely coagulated with multiple antennas.
Conclusion: A single generator may effectively deliver microwave power to multiple antennas. Large volumes of tissue may be ablated and large vessels coagulated with multiple-antenna ablation in the same time as single-antenna ablation.
© RSNA, 2007
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INTRODUCTION
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Microwave (MW) ablation with a single triaxial antenna in an in vivo porcine liver has recently been explored (1). However, all single-applicator thermal ablation modalities are characterized by rapidly decaying temperatures away from the applicator. There are many patients in whom large, multiple, or nonspherical tumors must be treated. In such patients, simultaneous treatment with multiple applicators may be useful. Multiple applicators may be able to rapidly ablate disproportionately larger volumes of tissue in less time and with less complexity than overlapping single ablations due to thermal synergy (2–4) (Fig 1).
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Figure 1: Graph shows relative temperature distribution for single (x = 0 cm) and double (x ± 2 cm) MW sources from a one-dimensional model at 10 minutes. The temperature between two antennas is consistently higher across ablation zone due to thermal synergy.
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Attention has been recently focused on multiple-electrode radiofrequency (RF) and multiple-antenna MW systems (2,3,5–8). One manufacturer (Valleylab, Boulder, Colo) offers a multiple-electrode RF ablation system in the United States, which requires a switching algorithm that reduces the duty cycle, or "on time," of each electrode. This switching algorithm increases the total ablation time because time is spent waiting for tissue to rehydrate without applying power. Another multipolar system available in Europe (Celon ProSurge, Hamburg, Germany) also allows mutlielectrode operation, but only in bipolar mode. It also requires a temporal switching algorithm during ablation, and with 15-gauge applicators, is slightly more invasive than the Valleylab electrodes. Thus, while multiple-electrode RF ablation holds many advantages over single-electrode systems—including thermal synergy, the ability to treat multiple tumors simultaneously, and customized ablation zone shapes—intrinsic limitations in RF energy delivery limit the efficiency of these systems.
In contrast, with multiple-antenna MW ablation, electromagnetic interaction between MW antennas does not substantially interfere with heating, so multiple antennas may be simultaneously powered. Since MW heating is not substantially hindered by desiccated or charred tissue, each antenna may be operated at a 100% duty cycle. Commercial MW systems currently require that separate generators be used to power each antenna, but it is possible that power may be delivered from a single source, where the only limit to how many antennas may be used is the maximum output power of the generator. Thus, multiple antennas may be used simultaneously to create large zones of ablation or to ablate several tumors without a reduction in duty cycle or power delivery.
While there are many advantages to MW ablation, there are two crucial limitations in commercially available systems: (a) large antenna diameters (14-gauge and larger), and (b) the requirement of multiple generators to power multiple antennas. The triaxial antenna was designed to overcome the limitation of large antenna diameter without compromising antenna performance (1,9,10) (Fig 2). To overcome the expense and complexity of using multiple generators, we propose that a single, controllable, high-power generator and inexpensive power splitter may be used to power multiple antennas. Thus, the purpose of our study was to prospectively investigate the ability of a single generator to power multiple small-diameter antennas and create large zones of ablation in an in vivo swine liver model.
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Figure 2: Triaxial antenna design schematic. The antenna is inserted through the needle to create triaxial structure that reduces reflections from the antenna and improves antenna efficiency. Insertion depth = 3.5 mm, antenna length = 12.3 mm; antenna length and insertion depth were optimized to minimize reflections in liver tissue.
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MATERIALS AND METHODS
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Animals, Anesthesia, and Procedures
Thirteen female domestic swine (mean weight, 70 kg) were used for our study. Preapproval was obtained from the research animal care and use committee of the University of Wisconsin (Madison, Wis), and all husbandry and experimental studies were compliant with the National Research Council's Guide for the Care and Use of Laboratory Animals. Animals were anesthetized and maintained with inhaled isofluorane (L.A.S., 10 years experience with animal anesthesia) while the medial portion of the liver was exposed at laparotomy (L.A.S., T.M.F.). An open approach was necessary to ensure proper antenna positioning for our study. MW ablations were performed as described in the sections below (P.F.L., C.L.B., 2 years experience each). After ablation, animals were euthanized with an intravenous overdose of pentobarbital sodium and phenytoin sodium (Beuthanasia-D; Schering-Plough, Kenilworth, NJ). Zones of ablation were excised and sectioned into approximately 5-mm transverse slices.
Multiple-Antenna Experimental Setup
All MW ablations described in our study were performed by using a 17-gauge triaxial MW ablation system (9,10). Antennas were placed in the large medial lobes of the liver to assure adequate room for ablations using a rigid template to maintain antenna spacing and parallel insertion. MW power for all antennas was produced by a single, 2.45-GHz magnetron generator (Cober-Muegge, Norwalk, Conn) capable of delivering up to 300 W of continuous power. A four-way power splitter (SM Electronics; Fairview, Tex) divided power equally between the three antennas, while the remaining channel was directed to a high-power load and power meter for continuous power monitoring (Fig 3). Generator output and reflected power were also measured continuously. Radio-grade (RG400/U) coaxial cables (Pasternack Enterprises, Irvine, Calif) with sub-minitaure ‘A’ connectors were used to transfer power from the splitter to the antennas. The triaxial antennas were created from low-loss, 1.26-mm, semi-rigid coaxial cable (UT-47-M; Micro-Coax, Pottstown, Pa) and 17-gauge introducer needles (Bard Medical, Covington, Ga). For all ablations, each antenna received 55 W for 10 minutes.
Ablations were performed in three groups: (a) a control group of simultaneously-powered ablations using three single antennas (n = 6, 18 zones of ablation) placed in separate liver lobes to ensure that ablations zones did not overlap; (b) an experimental group (n = 7) consisting of three simultaneously-powered antennas spaced 2.5 cm apart, and (c) an experimental group (n = 5) consisting of three simultaneously-powered antennas spaced 3.0 cm apart. These spacings were chosen based on ablation zone diameters achieved with single antennas (1). Each multiple-antenna ablation was carried out in the central portion of the medial liver lobes while control ablations were carried out in the lateral lobes or peripheral portions of the medial lobes to ensure no overlap between control ablations.
In six animals, both single- and multiple-antenna ablations could be completed; however, the other seven animals had insufficient liver volume to support both experimental and control ablations. In these animals, only experimental ablations were performed. Because large zones of ablation in the proximal area of the medial lobes reduced perfusion to the distal areas, single control ablations were performed before experimental multiple-antenna ablations so that perfusion in the tissue surrounding the control ablations would not be affected. Performing the control ablations first should not have affected ablations in the experimental group since blood flow is reduced distal to ablations. The power delivery schedule remained identical in control and experimental groups because the same generator, output power, power splitter, supporting hardware, and ablation time were used throughout our study.
Measurement of Ablation Zone Size and Shape
Ablation zone lengths were measured by using calipers prior to slicing. Slices were optically scanned (Perfection 2450 Photograph model G860A; Epson, Long Beach, Calif) and saved as electronic images. Representative slices from the middle of the ablation zone were then selected (P.F.L., C.L.B.) and stained with triphenyltetrazolium chloride (TTC, a marker for mitochondrial enzyme activity) to test for cell viability. Staining was complete when uncoagulated areas of viable tissue stained dark blue. More accurate measurements can be made on coagulated tissue when specimens are stained with TTC because the contrast between necrotic and viable tissue is better demarcated. Standard ablation zone measurements such as diameter, isoperimetric ratio, cross-sectional area, and number and size of vessels were measured and analyzed for each representative slice (P.F.L., C.L.B.) by using the freeware ImageJ (National Institutes of Health, Bethesda, Md). We used only the unstained, white zone of complete necrosis for measurement.
Ablation zone diameters were defined by transverse lines running through the center of the triangle array or the insertion path. Cross-sectional area was used to compare the conglomerate effect of multiple-antenna ablation with that of single-antenna ablations. Estimated ablation volumes were obtained by multiplying each cross-sectional area by the approximate slice thickness and summing all slices in a zone of ablation. Isoperimetric ratio measures the roundness of an ablation (11,12). In this case, isoperimetric ratio values near 1.0 indicate nearly circular zones of ablation and minimal heat sinking by nearby vessels. We also measured the largest circle that could fit completely inside the zone of ablation. This measurement is used to account for the discrepancy that can occur with multiple-antenna ablations between the minimum diameter and the maximum treatable area (Fig 4). This measurement is beneficial because it is not biased by the severely clefted zones of ablation that can yield very small minimum diameters.
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Figure 4: Sample multiple-antenna ablation in swine liver specimens demonstrates utility of a maximum circle size measurement. For multiple-antenna ablations, minimum diameter should not be relied on to describe potential efficacy of the zone of coagulation.
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Statistical Analysis
The statistical means ± standard deviations of each ablation measurement, (minimum and maximum diameter, cross-sectional area, isoperimetric ratio, and maximum circle diameter) were calculated. Because not all control ablations could be paired with experimental ablations, a mixed linear model, with animals modeled as random effects, was used to detect differences in ablation zone size or shape between single- and multiple-antenna groups and between 2.5- and 3.0-cm spacing groups. Volume measurements were not used for comparison because of inherent errors in summing slice areas with an assumed slice width, but are included for completeness. Only measurements that could be directly observed were included for comparison. SAS v9.1 (SAS Institute; Cary, NC) was used for statistical analysis with a P value below .05 indicating a significant difference.
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RESULTS
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Two animals expired prematurely during our study: one during a 3.0-cm-spacing multiple-antenna ablation, the other after ablations were completed. Only data from the animal that expired after ablation was included in the statistical analysis. Therefore, the statistical analysis contained data from groups of single-antenna controls (n = 6) and experimental multiple-antenna groups of seven (2.5-cm spacing) and five (3.0-cm spacing).
Ablation Measurements
Mean minimum and maximum diameters in both multiple-antenna experimental groups were significantly larger than those in single-antenna controls (P < .001 for all comparisons). No significant differences in minimum diameter, maximum diameter, cross-sectional area, or maximum circle diameter were observed between the 2.5- and 3.0-cm spacing groups (P > .05 for all comparisons).
Cross-sectional areas in the multiple-antenna groups were significantly larger than single-antenna controls (P < .001). Furthermore, the mean cross-sectional area of all multiple-antenna ablations was significantly larger than three times the mean area of all single-antenna ablations (P < .02). Mean cross-sectional areas of multiple-antenna zones of ablation with 2.5- and 3.0-cm spacings were 31.2% and 59.3% larger, respectively, than three times the mean volume of a single ablation (26.6/20.3 and 32.3/20.3, Table 1). Thus, simultaneous activation of multiple antennas resulted in more tissue destruction than did three single-antenna ablations. In addition, simultaneously powering three antennas decreased the total ablation time by 67% when compared with sequential ablations performed with a single antenna (10 minutes vs 30 minutes).
Mean isoperimetric ratios in the 2.5 and 3.0 cm multiple-antenna groups were nearly identical: 0.83 ± 0.09 and 0.84 ± 0.11, respectively (P = .79). The difference in isoperimetric ratio between the single- and multiple-antenna groups was found to be not significant (P > .05). Very little clefting was observed between antennas in the experimental groups; in fact, the high isoperimetric ratios observed indicate nearly circular ablations, despite the triangular antenna configuration (Fig 5).
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Figure 5a: Representative slices for ablations using (a) a single antenna, or (b, c) multiple antennas with (b) 2.5- and (c) 3.0-cm antenna spacing. Multiple-antenna ablations were significantly larger than three single-antenna ablations, but not significantly different from each other. Despite the triangular configuration, multiple-antenna ablations were nearly as circular as single-antenna ablations.
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Figure 5b: Representative slices for ablations using (a) a single antenna, or (b, c) multiple antennas with (b) 2.5- and (c) 3.0-cm antenna spacing. Multiple-antenna ablations were significantly larger than three single-antenna ablations, but not significantly different from each other. Despite the triangular configuration, multiple-antenna ablations were nearly as circular as single-antenna ablations.
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Figure 5c: Representative slices for ablations using (a) a single antenna, or (b, c) multiple antennas with (b) 2.5- and (c) 3.0-cm antenna spacing. Multiple-antenna ablations were significantly larger than three single-antenna ablations, but not significantly different from each other. Despite the triangular configuration, multiple-antenna ablations were nearly as circular as single-antenna ablations.
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Other Findings
Zones of ablation created with multiple antennas were not substantially affected by perivascular cooling. All vessels inside each zone of ablation were completely coagulated using multiple antennas. We also observed preferential heating, rather than evidence of heat sinking, in the perivascular space of each coagulated vessel (mean coagulated vessel size, 6.7 mm ± 3.7; range, 3.6 mm–11 mm) (Fig 6). Measures of vessel deflection or heat sinking did not apply in our study since the vessels and perivascular regions appeared to be preferentially heated by the multiple-antenna MW device. We made no distinction between arteries and veins in the vessel analysis.
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Figure 6: Swine liver specimen shows 1.1-cm vessel that was completely coagulated during multiple-antenna MW ablation. Note the perivascular space (arrows) is preferentially ablated.
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DISCUSSION
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To our knowledge, our study is the first using multiple-antenna ablation with the triaxial MW ablation system. The zones of ablation created are the largest of any reported that included three applicators small enough for percutaneous use. We also believe ours is the first report of a system using only one generator to simultaneously power multiple MW antennas in an animal model.
The ablation volumes measured in our study with three antennas originating from a single generator are 2.0–3.9 times larger than those reported previously in the literature for RF and MW ablation with the same number of antennas (Table 2). This is most likely due to the increased power capacity of the triaxial antenna compared with other MW antenna designs. Wright et al (2) showed that thermal synergy provided by three simultaneously-powered antennas allows the zone of ablation to be larger than the sum of its parts (ie, the ablation volume with the use of three antennas was larger than that from three single-antenna ablations). However, they noted that substantial clefting of the ablation zone occurred for antenna spacings greater than 1.7 cm. We believe that we were able to achieve larger zones of ablation by increasing the input power and efficiency of each antenna, which allowed conglomerate ablations with 3.0-cm spacing. Thus, it is reasonable to assume that even larger zones of ablation may be possible with higher input powers.
The slightly larger maximum diameters were expected for the 3.0-cm group, simply because of the increased probe spacing, but the differences were not statistically significant. The lack of significant differences between the 2.5- and 3.0-cm spacing groups indicates that 3.0 cm may not be the upper limit of useful spacing for three antennas at the power level and time tested. The relatively high isoperimetric ratio (0.85) at 3.0-cm spacing may indicate that this system is capable of producing conglomerate zones of ablation with 3.5-cm spacing. However, the porcine livers used in our study were not large enough to contain zones of ablation larger than those created. In addition, it has been shown that ablation zones tend to be much larger in tumors than in a normal liver (13), making the creation of larger zones of ablation of dubious clinical value and potentially unsafe if applied to human tumors.
Perivascular heating of coagulated vessels has been noted in prior work (14) with MW ablation but appears to be more pronounced when multiple antennas are used. This may be because MW energy can more effectively heat flowing blood, which then conducts heat into the perivascular space through the vessel wall. The appreciable heating of the perivascular space and thrombosis of vessels up to 1.1 cm in diameter in our study imply that tumors near major vessels may be more effectively treated with MW ablation, particularly with multiple antennas. In the past, inadequate treatment of perivascular tumors has been an important source of failure for virtually all ablation modalities. This limitation may be overcome with multiple-antenna MW devices.
Both premature deaths were animals treated early in the study timeline. The exact cause of death in both cases is unknown, but possible causes include anesthesia complications and low blood pressure coupled with complete or partial large hepatic vein thrombosis. Similar complications have also been observed during large-volume RF ablations on swine in our lab. After these deaths, we began introducing additional intravenous fluid (at least 1 L) before commencing ablation and have observed no animal deaths since. However, the clinical implications and safety of heating such large volumes of tissue and thrombosing large vessels need more study.
An RF ablation system with multiple-electrode capability has recently become commercially available (Cool-tip Switching Controller; Valleylab, Boulder, Colo). This system, while demonstrating that percutaneous multiple-applicator ablation is both feasible and effective, requires that power be applied in a temporally sequential fashion so that only one electrode is active at a given time. The active electrode is switched when the impedance rises beyond a baseline level caused by the inability of RF current to pass through desiccated or charred tissue (ie, tissue heated to 100°C). However, this algorithm results in duty cycles of less than 100% (<1/n, where n is the number of electrodes) for each electrode (3). While the multiple-electrode system offers substantial time and procedure complexity savings over sequential single-electrode RF ablation, the system is currently limited to three electrodes and requires grounding pads and additional peripheral hardware (cooling pumps, tubing, etc) unique to RF ablation. The MW ablation system presented here is capable of powering any number of antennas and does not require grounding pads.
The power splitter used in our study may be cascaded or arranged to provide any number of output channels from a single input. Using more applicators would allow a physician to adapt the zone of ablation to best treat each tumor. Single-applicator ablation is limited in its ability to treat both large tumors and tumors with noncircular cross sections. With this MW ablation system, the number of antennas available for use is theoretically limited only by the power source. Since magnetron power sources are inexpensive, efficient, and simple and can create high power levels, this limitation is not thought to be critical. The power splitter used in our study works best under ideal conditions (ie, when all antennas exhibit a near-zero reflection coefficient). This assumption is generally true for the triaxial antenna. However, if an antenna fails to achieve a low reflection coefficient, power may no longer be equally distributed among all antennas. This mismatch effect may have caused a few relatively small zones of ablation in our study.
Limitations in our study included the lack of a large-animal tumor model and the use of an open surgical approach. As previously mentioned, zones of ablation tend to be larger in tumors than in normal tissue. All ablations in our study were performed in normal porcine liver. Thus, we expect that the zones of ablation may be somewhat underestimated when compared with what may be clinically possible. In addition, multiple-antenna ablations were performed in the medial liver lobes. These lobes contain the highest density and largest vessels, and hence, the highest perfusion rate in the porcine model. Despite these limitations, the larger zones of ablation achieved with multiple antennas seem promising. More study is needed on this system by using a percutaneous approach.
Practical application: The zones of ablation presented in our study suggest the capability of ablating all but the largest human liver tumors with one application. The system created larger zones of ablation in less time than the current clinical standard, RF ablation. The preferential heating around vascular structures and ability to adapt the zone of ablation to the tumor may allow this system to treat tumors at high risk for recurrence, particularly in perivascular areas. Development of a clinical prototype and extension into other organ systems appears warranted.
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ADVANCES IN KNOWLEDGE
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- We demonstrated preclinical experience with multiple small-gauge antennas powered simultaneously from a single generator.
- We noted a relationship between antenna spacing and ablation diameter and shape.
- Large volumes of tissue may be ablated and large vessels coagulated with multiple antennas.
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FOOTNOTES
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Abbreviations: MW = microwave • RF = radiofrequency
Author contributions: Guarantor of integrity of entire study, C.L.B.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, all authors; experimental studies, all authors; statistical analysis, C.L.B., P.F.L.; and manuscript editing, C.L.B., P.F.L., F.T.L.
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References
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ABSTRACT
INTRODUCTION
