Anesth Analg 2002;94:1416-1420
© 2002 International Anesthesia Research Society
CARDIOVASCULAR ANESTHESIA
An Increase in Body Temperature During Radiofrequency Ablation of Liver Tumors
Maiko Sawada, MD,
Seiji Watanabe, MD,
Hideaki Tsuda, MD, and
Tatsuhiko Kano, MD
Department of Anesthesiology, Kurume University School of Medicine, Fukuoka, Japan
Address correspondence and reprint requests to Maiko Sawada, MD, Department of Anesthesiology, Kurume University School of Medicine, Asahimachi 67, Kurume, Fukuoka 830-0011, Japan. Address e-mail to mmss416{at}hotmail.com
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Abstract
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Radiofrequency ablation (RFA) therapy using an active needle electrode inserted into liver tumors has been used clinically. To avoid hyperthermia, we investigated the relationship between the total output energy of the applied radiofrequency wave and changes in body temperature (BT) in patients receiving RFA. Fifteen patients undergoing RFA of liver tumors with general anesthesia were enrolled. The total output energy of radiofrequency waves was calculated from the power and duration of RFA. Changes in rectal (Trect) and tympanic temperatures were measured throughout the study. The mean number of liver tumors per patient was 1.7 ± 1.3. The mean RFA time was 30.0 ± 26.3 min. The mean total output energy was 125,935 ± 114,506 J. The mean value of Trect increased from 36.3°C ± 0.5°C to 37.0°C ± 1.0°C (P < 0.01). A linear correlation was obtained between the total output energy and the changes in Trect, indicating that Trect increased approximately by 1°C for every 3000 J/kg of total output energy. The increase in BT during RFA of liver tumors under general anesthesia is predictable. Close observation of total output energy delivered and BT are required, and preparation of cooling measures is important, in RFA of liver tumors.
IMPLICATIONS: The increase in body temperature (BT) is predictable during radiofrequency ablation (RFA) of liver tumors under general anesthesia. Close observation of total output energy delivered and BT are required, and preparation of cooling measures is important, in RFA of liver tumors.
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Introduction
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Thermal coagulation therapy has been widely adopted for the treatment of patients with liver tumor(s) (1,2) because the procedure is less invasive and less time consuming than conventional surgical resection. Localized application of thermal energy destroys tumor cells. When tumor cells are heated more than 45°C–50°C, intracellular proteins are denatured and cell membranes are destroyed through dissolution and melding of lipid bilayers (3,4). A needle electrode with expandable tips is introduced into the center of the tumor under ultrasonographic guidance, through which a radiofrequency (RF) electrical current is applied for the thermal coagulation of the tumor and the surrounding tissue. An expandable needle electrode enables the treatment of large lesions.
In the case of multiple liver tumors, prolonged RF ablation (RFA) duration results in an increase in the total output energy, which is calculated by multiplying the time and power of the applied RF wave. Long duration of ablation with such a heated electrode in the liver, where blood flow is abundant, could induce a fever during treatment. Hyperthermia is more harmful than hypothermia, although the incidence of hyperthermia is small during general anesthesia. We investigated the relationship between the applied total output energy of the RF wave and the corresponding changes in body temperature (BT) in patients receiving RFA of liver tumor(s) under general anesthesia.
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Methods
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The study was approved by the Ethics Committee of Kurume University School of Medicine. Fifteen patients scheduled for RFA of primary liver tumors during surgery were enrolled onto this study. Written informed consent was obtained from all subjects before starting the study. Two of the patients had been receiving insulin injections for diabetes mellitus. Patients were premedicated with IM atropine (0.3–0.5 mg) and hydroxyzine (1 mg/kg) or oral flunitrazepam (1 mg). Acetated Ringer’s solution was infused IV at 5 mL · kg-1 · h-1. Before the induction of anesthesia, an epidural catheter was placed in 6 of 15 patients at the T8-9 or T9-10 spinal level for postoperative pain control. Anesthesia was induced with IV fentanyl (200 µg) and thiopental (5 mg/kg) followed with supplementary inhaled anesthetics (sevoflurane, 11 of 15 patients and isoflurane, 4 of 15 patients). The trachea was intubated after the administration of IV vecuronium (0.1 mg/kg), and the lungs were ventilated to maintain the end-tidal CO2 around 40 mm Hg. Blood pressure was measured by tonometry every 5 min. Subsequent anesthesia was maintained with a 1%–2% end-tidal concentration of the inhaled anesthetic used at the induction. Room temperature (Troom) was adjusted to approximately 24°C throughout the study. The patients were covered with disposable surgical drapes. BT controllers, such as a water blanket or a heating coil for venous catheters, were not used during the study of BT measurements. Rectal (Trect; n = 15) and tympanic temperatures (Ttymp; n = 12) and Troom were monitored each with a thermocouple probe (Mon-a-thermTM, Mallinckrodt Medical, St Louis, MO) throughout the study.
The size, shape, and location of liver tumor(s) were confirmed with ultrasonography directly on the liver surface under an open surgical procedure. Then, a monopolar needle electrode was introduced into the liver tumor under ultrasound guidance. The electrode consisted of a 15-gauge, 12-cm long, insulated cannula containing 10 individual hook-shaped electrode arms. A RF electric current (sinusoidal current of 460 kHz) supplied by an RF 2000® generator (Radio Therapeutics Corp, Mountain View, CA) was delivered through the electrode arms deployed in situ. Two different disposable electrode pads were placed on both sides of the anterior surface of the thigh. RFA was conducted for 15 min at a time and was repeated after a 5-min interval in cases of multiple liver tumors until the completion of thermal ablation. During treatment, the area of tissue ablation was monitored with ultrasonography to measure the zone of increased echogenicity corresponding to coagulation of the tissue. Trect and Ttymp were also obtained after the induction of anesthesia and every 30 min during the period of pre-RFA ultrasound examination of the liver. RFA was started immediately after the completion of the pre-RFA ultrasound examination. The Trect and Ttymp before the start of RFA served as the baseline values. Trect and Ttymp were monitored every 5 min after RFA was started, and they were determined at the maximum temperature after the termination of RFA. If Trect reached 38°C during RFA, the study was terminated, and cooling of the patient’s body was started for safety reasons.
The power and time of the applied RF wave were automatically recorded every 15 s. RFA was performed with the output power between the ranges of 20 and 90 W. Total output energy (J) was calculated by multiplying the output power (W) and time (s) of each ablation procedure. The energy (kcal) required to increase BT by 1°C was estimated by multiplying body weight and the average human specific heat of 0.83 kcal · kg-1 · °C-1. Therefore, the predicted increase in BT (°C) during RFA was calculated as [total output energy · 4.2-1]x[body weight x 0.83 x 1000]-1, in which 4.2 is the exchange coefficient from J to cal.
Analyses were performed using a commercially available statistical package (SPSS version 10.0J, SPSS Inc, Chicago, IL). The difference in changes in each variable was tested with the paired t-test. Regression analysis was performed between the values of total output energy and the maximum changes in each temperature during the observation among the patients. It was also performed between the values of Trect and the integrated output energy of respective ablations in each patient. Three cases were excluded from only later linear regression analysis because of short duration of RFA (Case 5, 6, and 8). Data were expressed as mean ± SD, and P < 0.05 was considered significant.
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Results
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The age of the 15 subjects (9 men and 6 women) was 64.6 ± 6.9 yr and body weight was 60.3 ± 14.1 kg (Table 1). The number of liver tumor(s) counted by direct ultrasonography during RFA was 1.7 ± 1.3 (range, 1–5), and the largest diameter ranged from 7 to 40 mm (long axis 21.6 ± 10.1 mm and short axis 17.7 ± 9.2 mm). The number of RFA procedures performed for the liver tumor(s) was 5.8 ± 3.8. The total output RFA time was 30.0 ± 26.3 min (range, 2.9–89.7 min), and the total output energy applied during RFA was 125,935 ± 114,506 J (range, 5016–314,769 J). Average volume of fluid transfusion during anesthesia was 6.2 ± 2.2 mL · kg-1 · h-1. Systolic or diastolic arterial blood pressure did not change during RFA (107 ± 13 mm Hg and 60 ± 13 mm Hg at the beginning of RFA and 113 ± 13 mm Hg and 64 ± 11 mm Hg at the end of RFA, respectively). Heart rate did not change during RFA (69 ± 8 bpm at the beginning of RFA and 68 ± 9 bpm at the end of RFA). A small dose of dopamine (3 µg · kg-1 · min-1 in one patient and 5 µg · kg-1 · min-1 in three patients) was infused before the beginning of RFA in 4 of 15 patients. Adjustment of the dopamine dose was not required during the RFA procedure.
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Figure 1. The relationship between measured changes in rectal temperature (Trect) and total output energy during the radiofrequency ablation (RFA) of liver tumors. Trect significantly increased along with increases in total output energy applied during RFA (n = 15, P < 0.001, r = 0.985).
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The baseline value of Trect was 36.3°C ± 0.5°C and that of Ttymp was 35.8°C ± 0.7°C immediately before RFA. Trect was 37.0°C ± 1.0°C (P < 0.01 versus before RFA; the maximum temperature was 38.8°C in one patient) and Ttymp was 36.6°C ± 1.1°C (P < 0.01 versus before RFA) at the maximum value of each temperature after the termination of RFA. All the patients’ BTs gradually increased along with repetition of the RFA procedure. In 4 of 15 patients, both the Trect and Ttymp reached 38°C during RFA, and active cooling was instituted, with the return of BT to near baseline. No patient experienced a BT above 39°C. The change in Trect after the start of RFA (1.33°C/h ± 0.70°C/h) was significantly larger than that before RFA (-0.09°C/h ± 0.11°C/h) (P < 0.01). There was a positive correlation between the total output energy applied during RFA and the measured increase in Trect (r = 0.985, P < 0.001; Fig. 1). An application of approximately 3000 J/kg of total output energy corresponded to a 1°C increase in Trect. The mean value of slope of the linear regression line of Trect performed in each patient was [3.41 ± 1.14] x 10-4°C · J-1 · kg-1, and r value was 0.981 ± 0.017. The increase in Ttymp showed a similar tendency to that of Trect (r = 0.945, P < 0.001). Each measured value of the increase in Trect or Ttymp was 23% or 26% greater than each predicted value, which was calculated from human specific heat and the total output energy applied during RFA.
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Discussion
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The increase in Trect was well correlated with that calculated from the total electrical output energy during RFA. Delivery of approximately 3000 J/kg total output energy matched a 1°C increase in Trect. Ttymp moved in parallel with changes in the Trect. This suggests that RFA causes not only local heating of intrahepatic tissues but also systemic heating through the intrahepatic blood stream. The former is a conductive heat that reduces rapidly with increasing distance from the intrahepatic needle electrode. The latter is a circulatory heat that conveys the warmed, abundant intrahepatic blood to the whole body like a heat exchanger in cardiopulmonary bypass. During RFA of liver tumors, the temperature increase of a given area and the local blood flow are inversely related. In this study, the longest total duration of RFA was approximately 90 minutes, which produced approximately 300,000 J of total output energy. Therefore, this large amount of energy could increase BT, especially in the path of the electric current. If liver tumors are large, hypervascular, or near the blood vessels, systemic heating during RFA is facilitated. To minimize the systemic radiation of RFA heat and enhance coagulative necrosis, temporary occlusion of hepatic blood inflow during the intraoperative RFA procedure is one option (2).
It has been reported that volatile anesthetics inhibited tonic thermoregulatory vasoconstriction (5), and core temperature decreased 1.6°C ± 0.3°C after one hour of anesthesia and 1.1°C ± 0.3°C during the next two hours of anesthesia (6). The decrease in the core temperature under general anesthesia is a core-to-peripheral tissue redistribution of body heat (6). However, the decrease in the core temperature before RFA in this present study (-0.09°C in one hour) was much smaller than mentioned above (-1.6°C or -1.1°C). Although the abdomen was opened in our study instead of closed like in their study (6), this difference may have been caused by the lower ambient temperature of 22°C in their study compared with 24°C in our study, or it may be because of the use of a single cotton blanket instead of our water proof surgical drape, which can reduce heat loss by radiation (7). This higher Troom might more readily allow the display of the effects of RFA on the BT because core temperatures were almost constant in this study. Lower Troom could chill the patient’s abdomen and might inhibit the increase of core temperature during RFA.
Conversely, the measured value of temperatures in this study was approximately 25% greater than the predicted value calculated from total output energy of RFA and body weight. It is possible that breakdown products of proteins produced by RFA act as pyrogens (8). In addition, RFA could stimulate production of cytokines, including tumor necrosis factor 
, interleukin (IL)-1, IL-6, and other proinflammatory mediators from Kupffer cells in the liver (9). The cytokines IL-1, IL-6, and tumor necrosis factor could induce increases in BT via direct and indirect actions on hypothalamic thermoregulatory centers and act as endogenous pyrogens (10,11). However, inhaled anesthetics could also inhibit the expression of fever induced with IL-2 (12). Because inhaled anesthetics were used during the RFA procedure, this might lessen the effects of RFA on the thermoregulation in the present study.
Another possible reason for our findings is that local tissue temperature is not homogeneous in the human body. We measured only the core temperatures in this study. Although the difference between core and peripheral tissue temperatures becomes small because of a core-to-peripheral redistribution of body heat under general anesthesia, a core temperature was still higher than a peripheral tissue temperature (6). We used the average human specific heat of 0.83 kcal · kg-1 · °C-1 in the equation to predict the increase in BT during RFA. In this equation, local tissue temperature is assumed to be equal anywhere in the body. Therefore, the measured core temperatures were possibly higher than the predicted values of temperature calculated based on the average human specific heat used in this study.
Twelve patients were premedicated with IM atropine (0.3–0.5 mg) in this study. The muscarinic receptors on eccrine sweat glands are innervated by sympathetic cholinergic fibers and readily accessible to antimuscarinic drugs. Atropine could suppress thermoregulatory sweating and might affect the temperatures measured in this study. Although atropine fever could be caused in infants and children, even with ordinary doses of atropine (13), we could not find any fever at the start of this study. Therefore, a small dose of atropine in this study was probably insufficient to induce atropine fever in adults.
Hyperthermia is deleterious because it can lead to acidosis, hyperkalemia, increase of permeability, and hypoxia caused by the increased oxygen demands, which worsens the functional neurological outcome in a model of complete cerebral ischemia (14). Tachycardia and arrhythmias also occur during hyperthermia followed by hypotension, decreased cardiac output, and eventual cardiovascular collapse (15). The expanded tips from the top of the needle possibly locate in the large vessel or the high-density area of microvasculature in the tumors. The RF procedure significantly induces blood cell damage, platelet activation, and clotting if the tip of the catheter is positioned in the blood stream (16). The thermal ablation procedure could be responsible for the production of micro-emboli, which were micro-air bubbles, small thrombi, or were caused by tissue breakdown. The patent foramen ovale between the right and left atrium is still persistent in approximately 20% of healthy adults with no clinical symptoms (17) and may allow micro-emboli to pass into the left atrium when right-sided pressures exceed those of the left (18). Edmonds et al. (19) showed cerebral micro-emboli during total hip arthroplasty, probably because of a patent foramen ovale or transpulmonary circulation. In the present study, there were no postoperative neurologic problems, such as confusion or cognitive deterioration, in any of the patients. However, the possibility of micro-embolism in the pulmonary artery and also in the cerebral artery during RFA remains.
In conclusion, close monitoring of BT and preparations for body cooling are important for RFA of liver tumor(s). A well-controlled RFA procedure with an appropriate output time, power, and intervals should be performed to ensure patient safety.
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Accepted for publication January 23, 2002.
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Abstract
Introduction
