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Experimental Studies |
1 From the Departments of Radiology of Beth Israel Deaconess Medical Center, 330 Brookline Ave, Boston, MA 02215 (S.N.G., M.A., J.B.K., J.C.H., B.S.O., R.E.L.); and Massachusetts General Hospital, Boston (G.S.G., E.F.H.). Received May 11, 2000; revision requested July 7; revision received August 4; accepted August 30. Supported in part by grants from Radionics, Burlington, Mass. 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 DISCUSSIONSTATISTICAL CONSULTANT...REFERENCES |
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MATERIALS AND METHODS: RF was applied for 12–15 minutes with internally cooled electrodes. For phantom experiments (n = 51), the NaCl concentration in standardized 5% agar was varied (0%–25.0%). A nonlinear simplex optimization strategy was then used in normal porcine liver (n = 44) to determine optimal pre-RF NaCl solution injection parameters (concentration, 0%–38.5%; volume, 0–25 mL). NaCl concentration and tissue conductivity were correlated with RF energy deposition, tissue heating, and induced coagulation.
RESULTS: NaCl concentration had significant but nonlinear effects on electrical conductivity, RF deposition, and heating of agar phantoms (P < .01). Progressively greater heating was observed to 5.0% NaCl, with reduced temperatures at higher concentrations. For in vivo liver, NaCl solution volume and concentration significantly influenced both tissue heating and coagulation (P < .001). Maximum heating 20 mm from the electrode (102.9°C ± 4.3 [SD]) and coagulation (7.1 cm ± 1.1) occurred with injection of 6 mL of 38.5% (saturated) NaCl solution.
CONCLUSION: Injection of NaCl solution before RF ablation can increase energy deposition, tissue heating, and induced coagulation, which will likely benefit clinical RF ablation. In normal well-perfused liver, maximum coagulation (7.0 cm) occurs with injection of small volumes of saturated NaCl solution.
Index terms: Liver, interventional procedures • Liver neoplasms, therapy, 761.1289, 761.30 • Radiofrequency (RF) ablation
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONSTATISTICAL CONSULTANT...REFERENCES |
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One potential strategy to increase the efficacy of RF ablation is to modulate the biologic environment of treated tissues (14). Along these lines, several investigators (15–17) have demonstrated the possibility of increasing RF tissue heating and coagulation during RF ablation by injecting saline or other NaCl solutions into the tissues during RF application. Using this technique, Curley and Hamilton (15) infused up to 10 mL/min of normal saline in ex vivo liver for 4 minutes during RF application to increase the coagulation diameter from 1.4 to 2.6 cm. Livraghi et al (16) also reported increasing coagulation up to 4.1 cm in diameter by using continuous infusion of normal saline at 1 mL/min in experimental animal models and human liver tumors. Miao et al (17) infused 1 mL/min of 5.0% hypertonic NaCl solution in ex vivo liver for 12 minutes during RF application and achieved coagulation 5.5 cm in diameter.
Two mechanisms have been proposed to account for the improved tissue heating and increased RF-induced coagulation with simultaneous saline infusion: (a) that NaCl alters tissue properties such as electrical conductivity to permit greater RF energy deposition, or (b) that the infusion of fluid during RF application improves the thermal conduction within the tissues by more rapidly and effectively convecting heat over a larger tissue volume. However, the exact mechanisms responsible for the increase in coagulation have thus far not been well characterized. Furthermore, to our knowledge, optimization of tissue heating and induced coagulation volume for RF ablation with adjuvant NaCl solution administration has yet to be performed. In addition, as far as we are aware, the effects of NaCl concentration have not been thoroughly explored.
We therefore conducted a series of experiments to better characterize the direct effects of NaCl concentration on local tissue electrical conductivity, RF energy deposition, and heating in an agar phantom model. In subsequent experiments, we sought to optimize the effects of NaCl solution concentration and injection volume on RF ablation (ie, tissue heating and induced coagulation) in an in vivo porcine normal liver model.
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MATERIALS AND METHODS |
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RF energy deposition.—Experiments were performed by using a high-current 500-kHz monopolar RF generator (CC-1; Radionics, Burlington, Mass) that was capable of 2,000-mA (200-W) output. Phantoms were placed in a room-temperature 0.9% normal saline bath that covered all but the top 0.5 cm of the phantom. The RF electrode was placed directly into the center of the phantom at a depth of 1.5 cm. To complete the electrical circuit, a standardized 12.5 x 8.0-cm metal grounding pad (Radionics) was placed within the normal saline exactly 10 cm from the electrode (Fig 1). RF was applied for 15 minutes by using a 17-gauge 2-cm-tip internally cooled RF electrode as previously described (18). Electrode tip temperatures were maintained at 10°–20°C by perfusing the internal lumina of the electrode with water at 0°C.
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Measurement of tissue electrical conductivity.—Tissue electrical conductivity was interrogated at 5 V root-mean-square by using the impedance monitoring circuitry that was contained within the RF generator, since it has been previously shown that for a given electromagnetic frequency at constant temperature, tissue conductivity is inversely proportional to the impedance (19). This low voltage was selected to enable impedance determination at 20°–37°C (prior to tissue heating), since temperature influences tissue conductivity (19). The system was calibrated to within 10% accuracy by using known noninductive resistances, with validation for impedance values of 25–1,000 
. Measurements were obtained through the central RF electrode and a second 1-cm-tip electrode placed 10 mm into the agar.
Measurement of phantom heating.—Temperatures throughout the phantoms were monitored during RF application by using 21-gauge thermocouple probes (Radionics). These probes are not perturbed by RF interference and do not interfere with uniform RF treatment (20). Correct positioning of temperature sensors at 5, 10, 15, and 20 mm from the electrode was assured by using an acrylic stabilizing device (Fig 1). Temperatures, impedance, and current were recorded at baseline and thereafter at 60-second intervals for the 15-minute RF application.
Statistical analysis.—For both experiments, phantom heating at each NaCl concentration was measured, and results were compared by performing routine statistical analysis. One-way analysis of variance with the Dunnett test (P = .05; two-tailed test) was performed to compare the findings obtained with different NaCl concentrations with those obtained without saline. In addition, electrical conductivity was correlated with phantom heating and energy deposition by using linear and higher order regression analyses to determine the best-fit least squares functions. The extent of coagulation was not measured in this model, since the agar phantoms were relatively heat resistant and did not produce a readily identifiable marker of coagulation.
Animal Studies
Once the phantom studies were completed, the effects of NaCl concentration and injection volume were studied and optimized in tissue in vivo—normal swine liver. Animal experiments were performed by three individuals (S.N.G., B.S.O., and J.C.H.). For these experiments, tissue heating and RF-induced coagulation served as objective end points.
Animal model.—A widely accepted normal swine liver model was selected (17,18,20). Sixteen Yorkshire pigs (Parson’s Farm, Hadley, Mass) of either sex (75.0–100.0 kg) were used. Approval of the Beth Israel Deaconess Medical Center institutional subcommittee on animal research care was obtained prior to the initiation of these studies. Animals were intubated and anesthetized with isoflurane (Isoflo; Abbott Laboratories, North Chicago, Ill). Cardiac and respiratory parameters and arterial blood gases were monitored throughout the procedures. Access to the liver was obtained by means of open laparotomy.
Experimental design.—Both saline concentration (0%–38.5%) and injection volume (0–25.0 mL) were studied by using a nonlinear simplex optimization strategy (21). Initially, three combinations of saline concentration and volume were selected to form an isosceles triangle on a graphic representation of the surface domain. Results were analyzed to determine which combinations provided the greatest tissue heating and coagulation. Subsequently, saline parameters for the next iteration were selected by using triangulation and reflecting away from the set of parameters that provided the least favorable results. The process was continued until the saline volume and concentration that provided maximum heating and coagulation were identified (ie, after two successive iterations yielded results with reduced temperatures and coagulation). In total, 11 points of the surface-response domain were interrogated, including a control of no NaCl injection. Four trials each were performed for each set of variables for a total of 44 RF applications. For these experiments, tissue conductivity was altered, RF applied, and temperatures and sizes of coagulation measured and compared.
Alteration of tissue electrical conductivity.—Tissue electrical conductivity was altered by the direct injection of NaCl solutions into the tissues. Prior to the application of RF energy, 0–25 mL of NaCl solution (0%–38.5% concentration by weight) was injected into the liver tissue surrounding the electrode by using a 25-gauge needle. To ensure uniform local distribution of the NaCl solution, injections were performed with the injection needle touching the previously inserted RF electrode and with the needle being slowly withdrawn along the electrode axis during injection.
RF application.—RF was applied by using the 500-kHz RF generator that was used in the phantom study. To complete the electrical circuit, four foil grounding pads (400-cm2 total surface area) were affixed to the lower back and thighs of the pig. By using ultrasonographic (US) guidance, a 3-cm-tip internally cooled RF electrode was inserted into the exteriorized liver parenchyma. Three to four ablation trials were performed in each pig liver. No more than two ablations were performed in each liver lobe. Electrodes were placed to minimize the potential effect of prior ablations.
RF was applied for 12 minutes at an initial generator output of 2,000 mA (200 W). If impedance increases were observed, the current output was automatically reduced in accordance with a previously designed pulsing algorithm that optimizes energy deposition and tissue coagulation (20). Parameters of the RF ablation were recorded at baseline and thereafter at 60-second intervals for the duration of RF application.
Tissue electrical conductivity measurements.—Alterations in tissue electrical conductivity were assessed by measuring direct local impedance at 500 kHz between the 3-cm-tip RF electrode and a second 2-cm-tip 21-gauge electrode placed 2 cm from the initial electrode. Local impedance over this short distance by using these well-defined parameters was measured to minimize the possible confounding effects of measuring the global system impedance, which can vary because of extraneous variables such as grounding pad contact and distance between the nonuniform grounding pad and electrode (22). Local tissue impedance was measured at baseline and after every 3–6 mL of NaCl solution injection.
Temperature measurements.—Tissue temperatures were measured during RF application at the electrode surface and 10 and 20 mm from the electrode by using the thermocouple probes that were described for the agar phantoms. An acrylic guide and US guidance ensured proper spacing of these temperature sensors. In addition, the position of the temperature sensors within the tissue was adjusted along the z axis parallel to the electrode during the initial 3 minutes of RF application to determine and permit monitoring at the maximum temperature.
Assessment of coagulation necrosis (pathologic studies).—Animals were sacrificed with an overdose of pentobarbital (0.2 mL per kilogram of body weight of Nembutal; Abbott Laboratories, North Chicago, Ill) within 30 minutes following ablation treatments. Fifteen minutes prior to sacrifice, 2 mL/kg of 2% Evans Blue dye (Fisher Scientific, Fairlawn, NJ) was administered intravenously. The use of this agent permitted the confirmation of intact or absent perfusion within the liver vessels and sinusoidal capillaries (23). RF lesions were excised and sectioned, and the extent of coagulation that was visible at pathologic examination was measured with calipers as previously described (18,20). Specimens were sectioned along the longitudinal and transverse axes of each lesion. Measurement of the coagulation diameter perpendicular to the electrode axis was based on the consensus of two observers (S.N.G. and J.C.H.). Histopathologic studies included cross-sectional mounting with hematoxylin-eosin staining and staining for mitochondrial enzyme activity by incubating thin representative tissue sections for 30 minutes in 2% 2,3,5-triphenyl tetrazolium chloride, or TTC (Sigma, St Louis, Mo), at 20°–25°C. The latter test can be used to determine irreversible cellular injury during the early stages of RF-induced necrosis (24,25).
Statistical analysis.—The tissue temperatures generated and the diameter of coagulation necrosis induced with each set of parameters were compared. Coagulation diameter was chosen as our primary measure of treatment effect, since it indicates the size of tumor that is potentially treatable with RF. Results were subjected to statistical analysis as described for the phantom experiments. In addition, multiple regression analysis with interactions was performed to determine the effect of NaCl solution volume and concentration on necrosis size, and the Dunnett test was performed to compare changes in impedance between the control and experimental groups.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONSTATISTICAL CONSULTANT...REFERENCES |
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± 1.5 vs 343.0 ± 12.5) and increased RF current (1,533.3 mA ± 76.4 vs 483.3 mA ± 5.8) within the phantoms (P < .001, both comparisons).
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Our analysis of the surface domain of the NaCl solution volume and concentration data plot further suggested elliptic boundary conditions, with a trend toward maximizing coagulation by increasing tissue electrical conductivity with increased NaCl concentration rather than with increased solution volume (Fig 7). Overall correlation between tissue heating 20 mm from the electrode or coagulation and impedance was poor (r2 = 0.2 for linear and higher order models). However, as expected, a linear correlation between tissue temperatures and coagulation was observed (r2 = 0.57).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONSTATISTICAL CONSULTANT...REFERENCES |
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The "bio-heat" equation governing RF-induced heat transfer through tissue has been previously described by Pennes (35), with this equation simplified to a first approximation by Goldberg and colleagues (14) as "coagulation necrosis = energy deposited x local tissue interactions - heat lost". Originally, most investigators devoted their attention to strategies that increase the energy deposited into the tissues. One common method has been to simultaneously apply energy by using arrays; this process has been made technically easier by the development of umbrella RF electrodes with multiple hooks (2,13). Other strategies have relied on the preferential cooling of the tissues nearest the probe by using single or clustered internally cooled electrodes (3–5,18,36) and/or pulsed RF energy (20) to increase overall energy deposition. With the use of these methods, coagulation diameters of 3.5–5.5 cm have been reported (20,36). However, even these advances do not permit reproducible ablation of larger (>5-cm-diameter) lesions in vivo. Less-than-ideal coagulation volume, limitations in RF generator technology (ie, maximum generator output), and the increased risk of grounding-pad burns with high-current ablation (22) have led investigators to study the modulation of other aspects of the thermal ablation process, which include tissue electrical conductivity and heat transfer during ablation.
In our study, the results confirmed that adjuvant NaCl solution injection prior to ablation substantially increases RF-induced tissue heating and coagulation, as compared with that with RF alone (15–17). More important, we demonstrated that much of this increase can be attributed to changes in electrical conductivity, which influences overall RF heating in a nonlinear fashion. Our data reveal that NaCl concentration influences both the current density that can be deposited in a tissue phantom and heat distribution throughout the phantom. These findings are in accord with those of prior studies (18,37) in which investigators have demonstrated that RF heating is directly proportional to the current density that is applied to a tissue. They also support the recent findings by Merkle et al (38) that increased ferric ions in the form of high doses of magnetic resonance imaging contrast agents that are composed of superparamagnetic iron oxide can elevate the temperature of polyacrylamide phantoms during RF ablation.
Our experimental findings demonstrate that ablative temperatures can be generated farther from an RF electrode by increasing tissue electrical conductivity with NaCl solution injection. This method permits greater energy deposition without inducing tissue boiling, which, in effect, flattens the heat distribution curve. As a result, we overcame a key practical constraint of conventional monopolar RF, namely the rapid falloff of tissue heating that occurs with increased distance from the electrode (39).
We have also demonstrated that further increasing tissue electrical conductivity is not always beneficial, since it can decrease the extent of tissue heating at extremely high NaCl concentrations, especially when generator current output is held constant. We hypothesize that increased conductivity has two competing effects on RF ablation efficacy. In many circumstances, increased electrical conductivity enables increased energy deposition and greater tissue heating. However, increased conductivity (ie, less intrinsic electrical resistance) also increases the energy required to heat a given volume of tissue. If this amount of energy is not delivered (ie, is beyond the maximum generator output), less actual tissue heating (and thus less coagulation) will result. Extreme alteration of tissue conductivity may therefore be counterproductive when coupled with strategies that already increase RF generator output, such as internal electrode cooling or pulsing.
Results of our in vivo animal experiments demonstrate the feasibility of increasing coagulation in normal tissue by injecting an NaCl solution prior to RF application. The magnitude of the increase in coagulation to 7 cm in diameter (ie, an increase in coagulation diameter of more than 3 cm), if reproducible in tumors, would be of significant benefit for clinical applications of RF tumor ablation therapy, especially for the treatment of larger lesions.
Statistical analysis of our data shows that both the volume and concentration of the NaCl solution injected are important. Our results further suggest elliptic boundary conditions for the surface domain of this data plot. However, further experimentation and modeling will be required to conclusively confirm this hypothesis and define the mathematic equations that govern this process. For the apparatus chosen, maximum coagulation occurs with the injection of a small volume (6 mL) of the highest possible concentration of NaCl solution (38.5%). These parameters appear to provide the best match between alteration of tissue electrical conductivity and the maximum output capabilities of our generator (ie, a point at which generator pulsing was rarely observed). Limited energy pulsing suggests that the tissue impedance was altered sufficiently to achieve maximum generator output without creating an ionic environment with energy requirements that would overwhelm the generator. However, it is likely that each combination of electrode configuration and generator, because of differing maximum output, will require individual optimization to achieve maximal coagulation.
Our results suggest that much of the increase in RF-induced coagulation reported by prior investigators (17) who used simultaneous saline infusion can be attributed to alteration in tissue electrical conductivity and that increases in coagulation are not solely due to improved tissue heat conduction from liquids that flow through the heated ablation volume. This fact has important implications for simultaneous saline infusion RF techniques (ie, the use of a "virtual wet electrode"). Initially, prior to substantial saline infusion, it is likely that there is less-than-optimal alteration of the tissue electrical conductivity. However, with continued saline infusion, it is possible that sufficient alteration in electrical conductivity will result in reduced tissue heating as changes in the local electrical environment create current requirements that exceed maximum generator output. Hence, methods of simultaneous saline infusion may require further optimization along these lines. For example, better results might be achieved by slowing or stopping saline infusion during the latter portion of RF ablation.
The results of several studies (40–42) suggest that tissue blood flow, which has a cooling effect in vivo, limits the efficacy of thermally mediated tumor ablation. In the current study, patent vessels were identified in the coagulation zone by using Evan’s Blue dye; results demonstrated that tissue perfusion remains intact even with NaCl solution pretreatment. Whereas the higher temperatures generated with NaCl solution pretreatment in the current study will undoubtedly reduce the number of patent vessels in a given zone of coagulation, our results suggest that it is unlikely that this method will enable eradication of all malignant cells in every case, especially when the lesion is near larger vessels.
Effects of vascular flow are likely also responsible for the weaker correlation between remote temperature data and NaCl concentration observed in vivo, as compared with those observed in the phantoms (r2 = 0.57 vs 0.94, respectively). To overcome the effects of perfusion-mediated tissue cooling, it may therefore be necessary to use NaCl solution pretreatment in conjunction with methods that reduce local tissue blood flow, which include angiographic vessel occlusion, pharmacologic blood flow modulation, or direct intratumoral injection of ethanol (25,40–42).
Several limitations of this study must be addressed. First, the large volumes of coagulation created may not always be beneficial or desired. Overtreatment in some cases could be detrimental if surrounding structures were damaged or too little normal tissue was preserved. Hence, it will be important to determine whether the strategy of injecting NaCl solutions can alter tissue coagulation in a predictable and reproducible fashion so that the volume of coagulation induced can be appropriately matched to tumor size and location. In addition, given that we were unable to measure coagulation in all three dimensions, it is difficult to assess the true volume and ultimate shape of lesions that will be created in thicker tissues. Thus, it is conceivable that the zone of necrosis will approximate an ellipsoid rather than a spheric lesion. Results may further vary in neoplastic tissue because of differences in tissue composition. This idea is further emphasized by the fact that a higher concentration of NaCl (38.5%) was needed to achieve maximum generator output in liver tissue, as compared with that (5.0%) in the phantoms.
An additional concern for the feasibility of adjuvant percutaneous injection strategies is the possibility of nonuniform alteration of tissue electrical conductivity, especially over large volumes, because of the difficulty of achieving uniform fluid diffusion and distribution. Irregularly shaped areas of coagulation have been observed previously with RF during simultaneous saline injection and attributed to nonuniform saline distribution (16,17). We, too, have observed this phenomenon in tissue samples in which 25 mL of saline was injected. However, our data demonstrate that it is possible to obtain maximal tissue heating and coagulation by using only 6–9 mL of NaCl solution. This requirement of only relatively small volumes of fluid may potentially minimize the issue of NaCl solution diffusion over larger volumes. In addition, given that the large volume of ablation will likely encompass the small volume of injected liquid, the possibility of distant tumor seeding by cells spreading with large volumes of injected liquid will likely be minimized. Nevertheless, the variable results seen with 3-mL injections suggest that injection of an inadequate fluid volume may not permit optimal alteration of tissue electrical conductivity.
Practical application: Optimization of NaCl solution treatment prior to RF application can be used to markedly alter local tissue electrical conductivity and energy deposition and thereby increase tissue heating and coagulation. For the apparatus chosen, maximum coagulation in liver in vivo occurs with the injection of a small volume (6 mL) of saturated saline. The magnitude of this increase (ie, coagulation up to 7 cm in diameter) will likely be of benefit for clinical applications of RF tumor ablation therapy. However, to achieve maximal clinical benefit, optimal parameters for NaCl injection will need to be determined for each type of RF apparatus used and for the different tumor types and tissues to be treated.
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STATISTICAL CONSULTANT COMMENTARY |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONSTATISTICAL CONSULTANT...REFERENCES |
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The collection of statistical procedures known as response surface methods was developed to aid in the solution of problems that are similar to the one described in this article. These methods are useful in approximating an unknown relationship between one or more outcome variables and a set of independent variables. Once such an approximation has been verified, various methods are available for determining the values of the independent variables that are associated with the optimal level of the outcome variables. An excellent reference to these methods is provided by Myers and Montgomery (Response surface methodology: process and product optimization using designed experiments. New York, NY: Wiley, 1995).
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, S.N.G.; study concepts, S.N.G., G.S.G., J.B.K.; study design, S.N.G., J.B.K., R.E.L.; literature research, S.N.G., J.B.K.; experimental studies, S.N.G., M.A., J.B.K., J.C.H., B.S.O.; data acquisition, S.N.G., M.A., J.B.K., J.C.H., B.S.O.; data analysis/interpretation, S.N.G., M.A., J.B.K., E.F.H., B.S.O., G.S.G., R.E.L.; statistical analysis, S.N.G., G.S.G., E.F.H., R.E.L.; manuscript preparation, S.N.G., J.B.K., G.S.G.; manuscript definition of intellectual content, S.N.G., J.B.K., G.S.G., R.E.L.; manuscript editing, S.N.G., J.B.K., G.S.G., R.E.L.; manuscript revision/review and final version approval, all authors.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONSTATISTICAL CONSULTANT...REFERENCES |
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