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1 All authors: Department of Diagnostic Imaging, Rhode Island Hospital, Brown Medical School, 593 Eddy St., Providence, RI 02903.
Received July 19, 2002;
accepted after revision November 5, 2002.
Address correspondence to W. W. Mayo-Smith.
Abstract
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MATERIALS AND METHODS. Solid renal masses in 32 patients underwent 38 treatment sessions using imaging-guided percutaneous radiofrequency ablation. During 36 sessions, radiofrequency ablation was performed using CT guidance, and two, using sonographic guidance. The average patient age was 76 years (range, 5287 years), and the average renal mass size was 2.6 cm (range, 15 cm). The average number of radiofrequency treatments per solid mass at each session was 2.4 (range, 16 treatments), and the average time per treatment was 9.2 min (range, 314 min). A single electrode was used in 12 sessions, and a cluster electrode was used in 26 sessions. The average follow-up time was 9 months (range, 136 months).
RESULTS. Twenty-six of 32 patients had successful treatment of the solid renal mass using percutaneous imaging-guided radiofrequency ablation after one treatment session. Successful treatment was defined as lack of enhancement of the treated region on follow-up CT. Six of 32 patients had residual enhancing tissue after the first treatment session and returned for a second session. Five of these six retreatments were successful. Masses requiring a second treatment session were significantly larger than masses treated in a single session (3.5 vs 2.4 cm, respectively; p = 0.0013). Two patients had perinephric hematomas (which did not require transfusion), and one patient developed a 5-mm skin metastasis at the electrode insertion site, which was resected without recurrence.
CONCLUSION. Percutaneous imaging-guided radiofrequency ablation shows promise in the treatment of solid renal malignancies.
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Radiofrequency ablation is a new technique that has been used most extensively to treat liver neoplasms [7, 8, 9] and has been described in laboratory animals [10, 11, 12, 13, 14, 15, 16]. It has more recently been described in treating a limited number of patients with solid renal masses [17, 18, 19, 20, 21, 22, 23, 24, 25]. If it can be shown to cause complete tumor eradication, renal radiofrequency ablation may hold promise as a new minimally invasive technique to treat renal malignancies on an outpatient basis without the need for hospital admission or general anesthesia.
Our purpose was to describe our experience in 38 consecutive treatment sessions of solid renal masses using percutaneous imaging-guided radiofrequency ablation and to describe techniques, complications, and results in these patients.
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Tumor Characteristics
Of the 32 patients, 18 had pathologic confirmation of the diagnosis from
imaging-guided biopsy performed either in advance or at the time of the
radiofrequency ablation. The pathologic results from the biopsies were 14
renal cell carcinomas, two oncocytomas, one angiomyolipoma that did not
contain macroscopic fat, and one metastatic angiosarcoma. Fourteen patients
did not have pathologic confirmation of the renal lesion, but the mass was
either solid on renal sonography (with homogeneous internal echoes) or showed
over 15 H of enhancement at dedicated contrast-enhanced renal CT. The average
size of treated renal masses was 2.6 cm (range, 15 cm). Twenty renal
masses were treated in the right kidney, and 12 were treated in the left.
Three tumors were located in the anterior renal cortex; 15, in the lateral
renal cortex; 13, in the posterior cortex; and one lesion, in the superior
cortex.
The location (or macroscopic morphologic location) of renal neoplasms was defined by Gervais et al. [20] as either exophytic, mixed, or central depending on the relationship of the tumor to the perinephric fat, renal parenchyma, and renal sinus fat. Exophytic renal masses were defined as at least 25% of the tumor extending beyond the renal contour and not abutting the renal sinus fat. Central masses extended into the renal sinus fat and were limited to the confines of the renal contour. The mixed category included tumors that were located adjacent to the renal sinus fat and distorted the renal contour. According to this definition, 29 of the treated tumors in our series were exophytic (Figs. 1A, 1B, 2A, 2B, 2C, 3A, 3B, 3C, 3D), and three were mixed.
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Radiofrequency Technique
For the first 2 years of the study, all patients were interviewed
immediately before the treatment by an interventional radiologist. For the
past year, our interventional service has employed a dedicated nurse
practitioner who helps coordinate referrals, gathers relevant outside
radiologic studies, and coordinates the pre- and posttreatment communication
with both the patient and referring physician. Currently, all patients
referred for a renal radiofrequency ablation have a dedicated visit to our
service in advance of the treatment, at which time the procedure is explained
in detail by the nurse practitioner who also obtains a brief history and
performs a physical examination. An interventional radiologist then interviews
the patient to further explain the technique and answer any questions. All
patients had chest, abdominal, and pelvic CT performed before the
radiofrequency ablation to stage the cancer.
The procedure was performed in all patients using conscious sedation (droperidol, midazolam and fentanyl) administered by dedicated nursing personnel. Continuous monitoring of heart rate, ECG tracing, oxygen saturation rate, and respiratory rate was performed, and blood pressure was taken every 35 min according to the conscious sedation protocol at our hospital. In 1998, at the beginning of our study, two patients were admitted for observation after the radiofrequency procedure. Since that time, all patients have been discharged on the day of the procedure after appropriate monitoring because of conscious sedation. No patient received prophylactic antibiotics before or after the procedure.
We defined a session as a visit to the radiology department when a renal
mass was treated with radiofrequency ablation. A radiofrequency treatment
referred to the placement of a radiofrequency probe into the lesion and
application of radiofrequency energy. Thus, a patient could undergo more than
one radiofrequency treatment in a single session. All radiofrequency ablations
were performed with an internally cooled radiofrequency system. The
radiofrequency generator (Cosman coagulator-1, Radionics, Burlington, MA)
produces a maximal output of 200 W, and internal cooling of the electrode is
performed with a peristaltic pump that recirculates ice water (80 mL/min)
keeping the electrode tip temperature below 20°. A cluster electrode
(three 2.5-cm active-tip electrodes) was used in 26 sessions, and a single
electrode (2- to 3-cm active tip) in 12 sessions. When the cluster electrode
was used, four grounding pads were placed on the patient's thighs; with the
single electrode, two grounding pads were used. The average number of
radiofrequency treatments per renal mass was 2.4 (range, 16 treatments)
at each session, and the average treatment time was 9.2 min (range, 314
min). The time of treatment was determined by posttreatment intratumoral
temperature. As has been described by Goldberg et al.
[26], a temperature of greater
than 50° was considered adequate to induce tissue necrosis. The average
tumor baseline impedance was 64
(range, 5091
), power
deposition was 141 W (range, 96164 W), and current was 1.5 A (range,
0.82.0 A). The average maximum intratumoral temperature achieved
immediately after radiofrequency treatment was 78.1° (range,
5996°). The radiofrequency electrode tract was not coagulated at
the time of radiofrequency electrode withdrawal.
Follow-Up
After the ablation session, patients were followed up on contrast-enhanced
CT, usually performed at 1-, 3-, and 6-month intervals after the original
session. We obtained follow-up information by direct interview of the patient,
contact with the referring urologist, examination of the radiology reports,
or, if necessary, follow-up in the patient's medical chart.
Statistical comparison of patients treated with one versus two sessions for lesion size, number of radiofrequency treatments, radiofrequency treatment time, and posttreatment temperature was performed using the unpaired Student's t test. Comparison of the type of electrode used (single vs cluster electrode) between the patients treated in one versus two sessions was performed using the chi-square test. Statistical analysis was performed using the software program Statview version. 5.0.1 (SAS Institute, Cary, NC). A p value of less than 0.05 was considered statistically significant.
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All patients tolerated the procedure with no major complications. Two patients had a transient episode of hypertension during the procedure (mean blood pressure, 215/100 mm Hg), which resolved spontaneously after the procedure. Two patients had small perinephric hematomas after the procedure, which resolved and did not require transfusion. One patient with a biopsy-proven renal cell carcinoma had a dilated upper pole calyx on follow-up CT, presumably from a stricture induced by the treatment (Figs. 1A, 1B). One patient had a single 5-mm metastasis in the skin at the electrode insertion site, which was resected, and no recurrent tumor has been identified during the follow-up period of 16 months. Several patients had pain or paresthesias in the periumbilical region for several weeks after the procedure, which resolved spontaneously. This presumably was due to transient damage to the intercostal or lumbar nerves in the affected dermatome. All patients received a prescription for oral pain medications (acetaminophen and hydrocodone bitartrate) at the time of discharge from the hospital, but fewer than 50% of the patients had the prescription filled, and few required analgesia for more than several days after the procedure. No patient experienced the postablative pain syndrome (pain, fevers, malaise, elevated WBC) described after hepatic radiofrequency ablation [27], and no patient required readmission to the hospital after the original treatment session. No patient received antibiotics before, during, or after the procedure.
Patients were imaged with contrast-enhanced CT at approximately 1, 3, and 6 months after the original treatment session. If there was no residual enhancement at the 6-month follow-up, patients were then imaged at 6-month intervals. The average follow-up interval for all patients was 9 months (range, 136 months). Twenty-six patients have shown no residual enhancing tumor on follow-up CT (Figs. 1A, 1B and 2A, 2B, 2C). Six patients did show residual enhancing tumor at follow-up and were treated a second time (Figs. 3A, 3B, 3C, 3D). On average, the second session occurred 4 months after the first session (range, <111 months). After the second treatment, five of these six patients showed no residual enhancement. One showed a small amount of residual enhancement, but the patient refused a third treatment. The small (<1 cm) area of enhancement in this patient has been stable for 18 months and is being followed up. Renal masses requiring a second treatment session (3.5 cm, range 25 cm) were significantly larger than masses that did not require a second session (2.4 cm, range 14 cm; p = 0.0031). There was not a significant difference in type of electrode used, number of treatments per session, posttreatment temperature, or treatment time between tumors treated in one session and those treated in two sessions.
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We have found that CT is the preferred imaging modality for performing renal radiofrequency ablations because both the renal mass and electrode location are reliably seen. In addition, the production of air bubbles at the electrode tip during radiofrequency treatment actually aids in determining the area treated using CT and can obscure both the lesion and localization of the electrode tip using sonography. On the basis of our experience in this small cohort of patients, we recommend using a cluster electrode for treatment of all renal masses because the area of tumor kill is greater than that using a single electrode and fewer treatments should be needed per session. To the best of our knowledge, the duration of each radiofrequency treatment has not been studied in treating renal masses. A treatment time of 12 min with the cooled-tip electrode system in both experimental and human models has been advocated for hepatic lesions [6, 26, 27]. This treatment time in the liver is based on the dual blood supply of the liver, which can dissipate heat generated by the radiofrequency electrode, also known as the "heat sink" effect. We have found that treatment times of 6 min can reliably induce temperatures after treatment of 50° in the lesion, which has been shown to induce tumor necrosis [26]. Depending on the lesion location, treatment times as short as 3 min (in small lesions surrounded by perinephric fat) caused tumor necrosis and lack of enhancement on follow-up imaging. For larger renal lesions, imaging-guided overlapping treatments and measurement of temperature at the electrode tip before retreatment provided reliable guidance for complete tumor ablation, as has been described in a study of radiofrequency ablation of the liver [27].
Eighteen of our patients had pathologic proof of diagnosis, whereas 14 were treated on the basis of imaging characteristics of enhancement of greater than 15 H on contrast-enhanced CT or of a solid renal mass shown on sonography. Sonographic findings and tumor enhancement patterns on CT have been shown to be reliable indicators of a solid renal mass [3, 28]. The role of biopsy before ablation is to document either a benign lesion that does not need treatment or a malignant lesion that does require treatment. The need for biopsy before renal radiofrequency ablation is controversial because renal biopsies can result in indeterminate or false-negative results.
Minimal complications were associated with renal radiofrequency ablation in our study. Two patients had a perinephric hematoma, which did not require a transfusion, and two patients had a transient episode of hypertension during the procedure, which resolved spontaneously. No patient had an episode of macroscopic hematuria. One patient had a 5-mm skin metastasis at the electrode insertion site, which was subsequently resected. These findings underscore the importance of both clinical and radiologic follow-up. One patient had dilatation of an upper pole calyx after the procedure, which may have been due to heat-induced stricture to the collecting system (Figs. 1A, 1B). We know of no other reports of collecting-system stricture caused by this technique. Renal radiofrequency ablation was generally well tolerated by our patients, who required only minimal oral pain medication after treatment.
Although the optimal time for imaging follow-up has not been determined, we currently schedule the patient for dedicated renal contrast-enhanced CT (using 5-mm collimation) at 1-, 3-, and 6-month intervals after the original treatment session. If there is no evidence of enhancement at 6 months, we then follow up at 6-month intervals. The optimal time intervals for follow-up should be investigated in future studies.
Analysis of tumor location showed that most lesions (29/32) were exophytic (> 25% of the tumor margin adjacent to the perinephric fat) (Figs. 1A, 1B, 2A, 2B, 2C, 3A, 3B, 3C, 3D). Three lesions were mixed (margins adjacent to the renal sinus and perinephric fat), and none of the lesions in our patients were purely central (tumor abutting the renal sinus fat and limited to the confines of the renal contour). We treated 32 of 33 patients referred for renal radiofrequency ablation and did not view location of the tumor within the cortex as a contraindication to treatment. One patient referred for renal radiofrequency ablation could not be treated because the exophytic lateral left renal mass was adjacent to the descending colon, but all other referred patients were treated. Thus, we found that most patients with solid renal masses are candidates for this procedure. That most lesions were exophytic and relatively small probably reflects the fact that most were discovered incidentally on imaging, although we did not study this feature specifically. Most lesions treated were either lateral (n = 15) or posterior (n = 13). These locations are optimal for treatment because the lesion is easily accessible using a posterior approach with the patient in the prone position.
Small renal masses have been shown to grow slowly, and a case can be made to follow up elderly debilitated patients because they may die of other causes before death from the renal cell carcinoma [29, 30, 31]. Indeed, nephrectomy may have a higher morbidity and mortality rate than watchful waiting in this patient cohort. The purpose of this study was not to decide whether patients should be observed or treated with radiofrequency ablation but to evaluate the technique of radiofrequency ablation and document its effectiveness. If renal radiofrequency ablation is shown to be comparable to surgical resection, then the appropriate patients for treatment should be investigated in future randomized trials.
In summary, we have found that imaging-guided percutaneous radiofrequency ablation shows great promise in treating solid renal malignancies. The procedure can be performed on an outpatient basis with minimal morbidity. Long-term follow-up should be maintained, and appropriate patient selection criteria should be determined by future studies.
Acknowledgments
We thank the urologists, John Maynard, John Marcaccio, Joeseph Callaghan,
and Bradley Miller, who referred patients for radiofrequency treatment; Glenn
A. Tung for his timely statistical analysis; and Steve Hopkins for his
tireless assistance in image restoration.
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