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Experimental Studies |
1 From the Department of Radiology, Beth Israel Deaconess Medical Center, Harvard Medical School, 330 Brookline Ave, Boston, MA 02215. From the 2002 RSNA scientific assembly. Received December 30, 2002; revision requested March 10, 2003; final revision received July 10; accepted August 18. Supported by National Cancer Institute grant RO1-CA87992–01A1. Address correspondence to S.N.G. (e-mail: sgoldber@caregroup.harvard.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Thirty canine venereal sarcomas were implanted in three tissue sites (subcutaneous, kidney, and lung) in 13 mildly immunosuppressed dogs. Five of 25 tumors, which were 19 mm ± 3 (mean ± SD) in diameter, were allocated to each of five groups: (a) subcutaneous tumors, (b) kidney tumors, (c) lung tumors with blood flow, and (d) subcutaneous and (e) renal tumors without blood flow, which was achieved by sacrificing the animal to eliminate tumor perfusion. A sixth group comprised larger subcutaneous tumors (mean diameter, 46 mm ± 4) that were also treated. RF ablation was performed with a 1-cm tip and 5 minutes of ablation at 90°C ± 1. Impedance, temperature, and resultant coagulation diameter were recorded and compared. Data were analyzed statistically, including one-way analysis of variance to determine the effect of tissue conductivity (ie, systemic impedance) on necrosis size and tissue temperatures. Linear regression analysis was used to compare changes in impedance between the control and experimental groups.
RESULTS: Increasing linear correlation was observed between tumor coagulation diameter and overall baseline system impedance (R2 = 0.65). RF ablation of lung tumors resulted in the greatest coagulation diameter (13.0 mm ± 3.5) compared with that in the other groups (P < .01). The smallest coagulation diameter was observed in kidney tumors in the presence of blood flow (7.3 mm ± 0.6) compared with that in the other groups (P < .01). Elimination of blood flow in kidney tumors increased coagulation diameter to 10.3 mm ± 0.6 (P < .01). After RF ablation, coagulation diameter in the subcutaneous tumor groups was the same (mean, 9.8 mm ± 1.0) (difference not significant), regardless of tumor size or presence of blood flow.
CONCLUSION: The characteristics of tissue that surrounds tumor, including vascularity and electric conductivity, affect ablation outcome. Predominance of tissue-specific characteristics will likely result in site-specific differences in RF-induced coagulation necrosis.
© RSNA, 2004
Index terms: Animals • Experimental study, 60.3255, 81.329, 90.9335 • Hyperthermia, 60.3255, 81.329, 90.9335 • Radiofrequency (RF) ablation, 60.3255, 81.329, 90.9335 • Sarcoma, 40.319, 60.3221, 81.329
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Results in recent animal and agar phantom modeling studies (16,17) suggest that local tissue parameters may play an important role in the determination of overall RF energy deposition and thermal ablation effectiveness. In addition to the now well-established negative effects of perfusion-mediated tissue cooling (18–20), alterations in local electric tissue conductivity immediately around the RF electrode, as outlined in the bioheat equation (21), can influence overall RF-induced tissue coagulation (16,17,22,23). While substantial efforts have been directed toward achieving a greater understanding of the role of local conductivity in improved RF effectiveness, few investigators have explored the effect of surrounding tissues on RF energy deposition. Nevertheless, in one study of RF ablation in patients with hepatocellular carcinoma surrounded by underlying cirrhotic liver tissue, Livraghi et al (24) described an "oven effect," in which RF-induced necrosis conformed to the size and shape of the tumor, and they further hypothesized that the fibrous cirrhotic liver functions as a thermal insulator that concentrates heating in the tumor tissue. Similar insulating properties of cortical bone have also been reported by Dupuy et al (25) in an experimental study performed in bone tumors. In addition, in studies (23,24) in a subcutaneous canine sarcoma model, an edge effect was observed at the tumor margin, particularly in situations of higher current or markedly increased tissue impedance. These results suggest that electric parameters at distances from the electrode may also be important in the determination of RF heating throughout a tumor volume.
While RF delivery has been optimized to realize potentially higher effectiveness in the setting of hepatic tumors, these paradigms may not be optimal for tumors located in other organs on the basis of inherent differences in local tissue characteristics. However, the extent to which differences in background tissue composition can influence clinical effectiveness has not been fully elucidated. Thus, an improved understanding of the particular differences among various tissue types is required. Therefore, the purpose of our study was to determine the effect of surrounding tissue type on coagulation necrosis after RF ablation in a homogeneous animal tumor model.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Experiment 1: effect of surrounding tissue.—In experiment 1, the role of surrounding tissue environment on RF-induced coagulation diameter and energy deposition was examined. In these experiments, canine venereal sarcomas were implanted into three tissue sites (with five tumors in each group): group A, small subcutaneous tumors with blood flow; group B, kidney tumors with blood flow; and group C, lung tumors with blood flow. Each tumor was treated with a standardized protocol of RF ablation. Tumors of approximately the same size (mean diameter, 19 mm ± 3 [SD]) were used. RF ablation was applied as described later, after which histopathologic assessment was performed.
Experiment 2: effect of blood flow.—In experiment 2, the role of blood flow in normal tissue surrounding the tumor was examined. For this experiment, tumors were implanted into two tissue sites with known differences in normal tissue perfusion rates: kidney (high blood flow) and subcutaneous tissue (low blood flow). Two groups of tumors were treated in this experiment (with five tumors in each group): group D, small subcutaneous tumors without blood flow; and group E, kidney tumors without blood flow. Results were compared with those for tumors treated in either site in the presence of blood flow from experiment 1 (groups A and B). To accomplish this, 10 additional tumors were treated in situ with the same standardized RF ablation protocol immediately after the animals were sacrificed to reflect a situation without perfusion. Absence of a heartbeat was documented in each animal before initiation of RF ablation for all tumors allocated to the groups with no blood flow.
Experiment 3: effect of tumor size.—With the results from earlier experiments, a last experiment was performed to determine if tumor size (ie, the proximity of normal surrounding tissues to the RF electrode) influenced RF coagulation. In this experiment, an additional group (group F, large subcutaneous tumors with mean diameter of 46 mm ± 4) were also treated with the standardized RF protocol. Results in this group were compared with those in experiment 1 (group A), where smaller subcutaneous tumors were treated. Tumor blood flow was not altered in this group.
Animal Model
Approval of the institutional animal care and use committee was obtained before initiation of these studies. Experiments were performed with a well-characterized established canine venereal sarcoma cell line (23,26). Thirteen female Labrador dogs (retired breeders [weight range, 30–40 kg]; Team Associates, Canterbury, Conn) were mildly immunosuppressed (cyclosporin A [25 mg per kilogram of body weight, twice daily], Neoral; Novartis Pharmaceuticals, Cranbary, NJ) for 5 days before tumor transplantation, and immunosuppression was continued until the end of the experiment. Fresh tumor (approximately 2 cm in diameter) was initially harvested from a live carrier. Within 30 minutes of tumor explantation in each animal, the tumor was homogenized with a tissue grinder (model 23; Kontes Glass, Vineland, NJ) and aseptic technique and was suspended in 15 mL of Dulbecco modified Eagle medium (INC Biomedicals, Aurora, Ill). Results of previous unpublished control experiments documented that this procedure resulted in a concentration of approximately 1 x 108 tumor cells per milliliter of tumor suspension.
All animals were anesthetized for 30 minutes with one dose (10 mg/kg administered intramuscularly) of Telazol (Lederle Parenterals, Carolina, PR) before tumor transplantation. Before tumor inoculation, sites of injection were shaved and disinfected with Betadine (Purdue Frederick, Norwalk, Conn) and 70% ethanol. Each animal received subcutaneous tumor implantations, followed by random allocation to receive either direct kidney injection or intravenous injection (to homogeneously implant tumor in the lung) (Table 1). Three phases of implantation were used in two groups of four animals and one group of five. Tumor cell line characteristics were preserved by removing one untreated subcutaneous tumor from one animal in each sequential group to be transplanted into the animals in the next group. Therefore, one index tumor was used as the original source for all transplants. At no point were the tumor cells stored or frozen.
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Intrarenal Tumor Implantation
Tumor and animal preparation before tumor implantation was described earlier. With US guidance, the tip of an 18-gauge spinal needle was placed in the lower pole of each kidney, and 1.5 mL of the tumor suspension was injected slowly. Each animal received one injection per kidney for a total of 10 kidney implantations in five animals (M.A., S.N.G.). To follow tumor growth, each animal underwent contrast material–enhanced computed tomography (CT) of the lungs and kidney every 10–18 days until one or more renal or lung tumors grew to a diameter of 1.5–2.0 cm. After RF ablation, the animals were sacrificed. Specific techniques of RF ablation and histopathologic tissue analysis are described later.
Pulmonary Tumor Implantation
An 18-gauge catheter was placed into a distal superficial forearm vein in each animal. Five milliliters of tumor suspension, which contained several small solid tumor pieces (to facilitate tumor seeding and entrapment in the lung capillary bed), was slowly injected intravenously through the catheter in five animals, for a total of five tumor implantation procedures (M.A., S.N.G.). Thus, unlike previous models, this model represents tumor embolus implantation. Animals were followed for tumor growth with biweekly contrast-enhanced CT until one tumor reached a diameter of 1.5–2.0 cm. After RF ablation, the animals were sacrificed. Specific techniques of RF ablation and histopathologic tissue analysis are described later.
RF application.—For the ablation experiments, animals were intubated and anesthesia was maintained with isoflourane (Forane; Baxter Healthcare, Deerfield, Ill). Cardiac and respiratory parameters and arterial blood gas levels were monitored throughout the procedures. RF energy was applied with a 500-kHz RF generator (CC-1; Radionics, Burlington, Mass) (M.A., Z.L., S.N.G.). To complete the electric circuit, two foil grounding pads (400-cm2 total surface area) were affixed to the lower back and thighs of the dog. A 1-cm-tip 22-gauge RF electrode (SMK; Radionics) was inserted into the center of the tumor. RF energy was applied for 5 minutes and titrated to a tip temperature of 90°C ± 1. A similar method was used to induce 0.8–1.2-cm coagulation diameter in a rabbit adenocarcinoma model (27,28). Parameters of the RF ablation were recorded at baseline and thereafter at 60-second intervals for the duration of RF application. These parameters included measurements of baseline systemic impedance as an indirect determinant of differences in tissue electric conductivity (16). RF electrode placement and ablation therapy of subcutaneous tumors were performed with direct visualization. Animals with kidney tumors underwent open laparotomy before RF application, and tumor localization and electrode placement were performed with US guidance. Tumor localization, electrode placement, and RF ablation of lung tumors was performed with fluoroscopic CT guidance.
Tissue cooling measurements.—A measurement of the time (seconds) required for the central RF electrode temperature to decrease from 90° to 60°C immediately after RF ablation ceased (t60) was recorded (M.A., K.S.A.) as a representative measurement of tissue cooling and heat retention after RF ablation has ceased for all three tissue sites (27).
Assessment of coagulation necrosis and histopathologic findings.—Animals were sacrificed within 30 minutes after ablation treatments by means of pentobarbital overdose (Nembutal [0.2 mL/kg]; Abbot Laboratories, North Chicago, Ill). In five animals, 2 mL/kg of 2% Evans blue dye was administered intravenously 15 minutes before sacrifice (Table 1). Use of this agent permitted confirmation of the absence of perfusion in the tumor (23). RF lesions were excised and sectioned (M.A., Z.L.), and the extent of visible coagulation at gross pathologic examination was measured with calipers. Specimens were sectioned along the longitudinal and transverse axes of each lesion. The coagulation diameter perpendicular to the electrode axis was measured with consensus of two observers (K.S.A., M.A.). Findings in previous studies in the same model (23,29) document the accuracy of this technique. Histopathologic studies included cross-sectional mounting with hematoxylin-eosin staining, as well as staining for mitochondrial enzyme activity by incubating thin representative tissue sections for 30 minutes in 2% 2,3,5-triphenyl tetrazolium chloride at 20°–25°C. This latter test is capable of determining irreversible cellular injury during early stages of RF-induced necrosis (28,30,31).
Statistical analysis.—Tissue temperatures and the diameter of coagulation necrosis were compared in each group. Coagulation diameter was chosen as our primary measure of treatment effect because it indicates the size of a tumor that is potentially treatable with RF. Each of the potential variables (tissue type, blood flow, and coagulation diameter) was analyzed independently in separate statistical tests for each of the three experiments. One-way analysis of variance was used for experiment 1 (SAS; SAS Institute, Cary, NC), and Student t tests were used for experiments 2 and 3. Linear regression analysis was used to compare changes in impedance between the control and experimental groups.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Kidney and subcutaneous tumors treated with RF ablation in the absence of blood flow demonstrated significantly greater heating, as manifested by higher t60 values compared with those in corresponding groups with blood flow present (P < .02) (Table 3). No significant difference was observed between kidney and subcutaneous tumors with or without normal blood flow for any other RF parameter (current, power, start or end impedance).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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cm in diameter (1,5,24,33). To overcome obstacles to RF ablation, particularly for larger tumors, studies have been directed toward improvement of our understanding of the biophysiologic factors that influence RF tissue heating by using the "bioheat equation" (34). This equation was first described by Pennes (21) and then simplified by Goldberg et al (34) to the following: coagulation necrosis equals energy deposited multiplied by local tissue interactions minus heat loss. Based on this equation, several studies document the potentiating effect of increased tissue electric conductivity around the RF electrode in phantom agar, ex vivo and in vivo porcine liver, and clinical models (16,17,22). Goldberg et al (16) demonstrated in phantom agar and in vivo porcine liver models that gains in coagulation are related to volume and concentration of NaCl, with greatest effect for small volumes (approximately 6 mL) of highly concentrated (38%) NaCl solutions. Lobo et al (17) mathematically correlated local electric conductivity to increases in both local temperature and total RF energy deposition when NaCl ionicity was changed around an RF electrode. While investigators have made advances in the understanding of RF interactions with local tissue electric conductivity, anecdotal reports (23,24,35) document irregularities in heating at the margins of tumors treated with RF ablation. These reports suggest that the composition of tissue surrounding the tumor may also influence ablation outcome. Livraghi et al (24) and Boehm et al (35) described altered thermal parameters with RF energy applied in hepatocellular carcinoma surrounded by fibrous cirrhotic liver and in adenocarcinomas implanted in rabbit breast tissue, respectively. They suggest that these effects may be a result of either reduced thermal or electric conductivity, with the cirrhotic tissue behaving as an insulator to retain heat in the tumor and to increase completeness of necrosis. Similarly, Dupuy et al (25) observed that the characteristics of heat deposition and thermal transmission differed significantly when RF energy was applied to vertebrae in comparison to those with either liver or ex vivo agar phantoms. This observation demonstrates an insulating effect of cortical bone, which prevented thermal damage to nerve tissue in the spinal canal. The finding is consistent with results in earlier studies to document the varied conductive properties of different tissues (15). Clearly, investigation of these properties is essential for further understanding of how best to apply RF energy in other tissues.
We believe that our study represents the necessary next step in the characterization of RF and tissue interactions. Our study findings show that the surrounding tissue environment can significantly influence ablation outcomes. These site-based differences can be a result of several environmental characteristics. Our results strongly suggest both that these changes are not caused by one factor alone and that the influence of a given environmental characteristic (ie, blood flow or electric conductivity) in the determination of the ultimate coagulation diameter varies from tissue site to tissue site. Specifically, RF ablation of canine sarcoma tumors implanted in the lung resulted in significantly larger coagulation diameters than were seen in tumors implanted elsewhere. The high starting impedance values (ie, low electric conductivity) and the significant difference in necrosis between the lung tumors and the kidney and subcutaneous tumors with or without blood flow correspond to earlier findings by Goldberg et al (36). They found that the presence of air in the alveoli surrounding tumors increases electric impedance at the outer tumor margins, which results in greater resistive heating in the tumor.
The correlation demonstrated between increased coagulation diameter and increasing global system impedance, given equivalent tumor composition and energy deposition for each of the three sites, suggests that electric conductivity of outer surrounding tissue influences RF ablation outcome. Of note, this correlation is the inverse of previously documented effects of local electric conductivity immediately surrounding the electrode, where greater conductivity (lower impedance) resulted in deeper tissue heating (16,22). We therefore postulate a twofold effect of tissue electric conductivity on the basis of tissue proximity to the RF electrode. First, in local tissue immediately adjacent to the electrode, lower impedance, such as that achieved with the adjuvant injection of highly concentrated NaCl solution, enables increased RF energy deposition, which in turn induces deeper tissue heating. In tissues that surround and are beyond the desired ablation zone (ie, farther from the electrode), however, increased impedance retards RF energy flow, which results in increased local heat generation and functions to keep heat in the lesion.
The role of changing electric impedance that parallels changes in tissue electric conductivity has important implications with respect to clinical application of RF energy for tumor destruction. The use of RF energy for tumors surrounded by poorly conductive tissues can result in increased heating at the margins of the ablation zone, which may result in more complete treatment. In addition to results reported for hepatomas surrounded by less conductive fibrous cirrhotic liver, this finding may in part account for better results reported for RF ablation in exophytic kidney tumors (37). Alternatively, focused heating at tumor boundaries with reduced RF energy transmission into surrounding normal tissue may ultimately hinder the ability to achieve the 0.5–1.0-cm "ablative" margin of treated normal tissue that is desired to minimize local tumor recurrence from microscopic malignant invasion that may be present in this rim of normal tissue (38). Indeed, in earlier reports (23,35,39) of RF ablation in normal breast tissue and canine sarcomas implanted in subcutaneous tissue, irregular margins of coagulation were a result of heat-induced liquefaction of fat immediately adjacent to the RF zone; these findings suggest that increases in electric impedance across tumor boundaries can restrict current flow into peripheral tissue and can concentrate RF heating in this transition zone. The irregular heating that results from rapid increases in electric impedance across tumor boundaries can restrict current flow into peripheral tissue and therefore potentially hinder complete tumor destruction (23,35).
The results of our experiments also underscore the influence of perfusion-mediated vascular cooling on RF-induced tissue heat generation, because increases in coagulation diameter were achieved with the elimination of blood flow in intrarenal tumors treated with RF ablation. These findings are consistent with those in other published reports (19,40) that document in both animal models and preliminary clinical studies that increased tumor coagulation diameter can be achieved with RF ablation when blood flow is simultaneously reduced. Lu et al (19) documented the negative influence of hepatic blood vessels larger than 3 mm on the completeness of RF-induced coagulation in normal in vivo porcine liver. In addition, in 14 patients with hepatocellular carcinoma (mean tumor diameter, 5.2 cm), Buscarini et al (40) performed RF ablation after hepatic segmental transcatheter arterial embolization and achieved disease-free survival in 79% at 13 months. However, while the negative influence of intratumoral perfusion-mediated vascular cooling is well documented for tissues that are primarily immediately adjacent to the electrode, few studies have been performed to differentiate the effects of intra- and extratumoral vascular perfusion. The results of our study suggest that even in hypovascular tumors, the vascular cooling of normal tissue that encompasses the tumor can also significantly reduce RF tissue heating. Indeed, once blood flow was eliminated, the coagulation diameter of intrarenal tumors was equivalent to that in tumors implanted subcutaneously.
In contrast to intrarenal tumors, subcutaneous tumors showed increased tissue heat retention (as evidenced by increases in t60) with reduced blood flow, but this did not produce a corresponding increase in necrosis. This finding suggests that heat retention is less relevant in the subcutaneous tissue site as a result of either the predominance of other tissue factors or a potential "threshold effect" after which increases in tissue heat retention do not translate into further gains in coagulation. As such, these results underscore the need for direct comparison of coagulation diameter as the primary and most clinically relevant measure of RF outcome rather than indirect temperature end points alone.
While our results highlight the role of changing tissue environments in RF ablation outcome, several limitations in the current study must be noted. Although the use of a consistent tumor type in our experimental design helped us isolate differences in site-specific tissue characteristics, the results in this model may not be applicable to other types of tumors. Several factors, such as conductivity and blood flow, have well-described influences on focal RF heat generation, and the relative importance of each factor will differ on a tumor- and tissue-specific basis. Furthermore, substantially greater amounts of RF power and current are routinely applied in a clinical setting compared with that used in the current study. Tumors of the size included in this study can be consistently and completely treated with RF ablation alone in all three sites (ie, kidney, subcutaneous, and lung). Therefore, outcomes in more clinically relevant tumor models may differ, and extrapolation to other tumor types should be performed with caution. Nevertheless, our results underscore the importance of tissue environment on RF effectiveness, and a better understanding of RF and tissue interactions will ultimately result in improved RF delivery. Further site- and tumor-specific preliminary work will allow development of RF delivery devices, as well as characterization of the most appropriate adjuvant therapies, tailored to generate optimal RF outcomes with minimal adverse effects on a tumor-to-tumor basis.
Practical application: The characteristics of normal tissue that surrounds tumor, including blood flow and conductivity, significantly influence RF ablation outcome and will achieve greater importance as RF therapy is increasingly applied to sites beyond the liver. We observed significant changes in RF-induced coagulation on the basis of differences in the composition of normal tissue types surrounding treated tumor. These findings suggest that surrounding tissue characteristics (ie, vascularity and electric conductivity) clearly affect RF ablation outcome and energy deposition. Our results suggest that further tailoring of RF ablation protocols is warranted because focal tumor ablation is being applied throughout the body with increasing frequency, and this presents an exciting opportunity for better optimization of RF ablation in each organ site.
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, S.N.G.; study concepts, M.A., S.M.L., J.B.K., R.E.L., S.N.G.; study design, M.A., Z.L., K.S.A., S.M.L., S.N.G.; literature research, M.A., S.N.G.; experimental studies, M.A., Z.L., K.S.A., D.W.; data acquisition, M.A., Z.L., K.S.A., D.W.; data analysis/interpretation, M.A., S.N.G.; statistical analysis, M.A., S.M.L., R.E.L., S.N.G.; manuscript preparation, M.A., S.N.G.; manuscript definition of intellectual content, editing, revision/review, and final version approval, all authors
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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