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Vascular and Interventional Radiology |
1 From the Department of Radiology, Massachusetts General Hospital, Fruit St, Boston, MA 02114. From the 1999 RSNA scientific assembly. Received February 11, 2000; revision requested March 24; revision received May 1; accepted May 22. Address correspondence to D.A.G. (e-mail: dgervais@partners.org).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Twenty-four percutaneous RF ablation treatments for nine tumors were performed in eight patients with renal cell carcinoma. Indications included coexistent morbidity, previous surgery, or solitary kidney in patients with a life expectancy shorter than 10 years. Smaller (
3-cm) peripheral lesions (n = 3) were treated with single electrodes. All but one of the larger (>3 cm) and/or central lesions (n = 6) were treated with cluster or multiple electrodes. Patients returned for a second treatment when follow-up imaging depicted tumor enhancement. Follow-up imaging was performed at 1 and 3 months and then at 6-month intervals, with a mean follow-up of 10.3 months. Seven patients were alive at least 6 months after their initial treatment.
RESULTS: All five exophytic tumors were free of enhancement. One of three central tumors was free of enhancement. One tumor had both central and exophytic components and was free of enhancement. Three tumors were 3 cm or smaller and free of enhancement. Of the six tumors larger than 3 cm, four were free of enhancement.
CONCLUSION: Percutaneous RF ablation is a promising treatment for select patients with renal cell carcinoma. The ultimate role of this modality will continue to evolve and warrants further study.
Index terms: Kidney, interventional procedures, 81.1269 • Kidney neoplasms, CT, 81.12111, 81.12112, 81.30 • Kidney neoplasms, MR, 81.12141, 81.12143, 81.30 • Radiofrequency (RF) ablation, 81.1269
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The application of thermal energy by means of radio frequency (RF) to destroy benign or malignant tumors has proved to be successful for osteoid osteomas (9) and small primary and metastatic liver lesions (10–12) in humans. The results of recent animal studies (13,14) have demonstrated the feasibility of RF ablation in the kidney. In addition, Zlotta et al (15) reported on a series of renal tumors in humans that were treated with RF ablation and then resected. McGovern et al (16) reported a case of in vivo RF ablation in a patient with renal cell carcinoma (16) but without follow-up. To the best of our knowledge, however, to date, no short- or long-term results from nonexcised, percutaneously treated tumors are available. The purpose of our study was to report our early experience with RF ablation of renal cell carcinoma, with imaging follow-up.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Tumor Characteristics
A total of nine tumors were treated in eight patients. Five tumors were on the left, and four were on the right. All tumors were imaged before RF ablation with contrast material–enhanced CT (with ioxilan 62% [Oxilan-300], 300 mg of iodine per milliliter; Cook, Bloomington, Ind) (n = 8) or magnetic resonance (MR) imaging (with gadopentetate dimeglumine [Magnevist]; Berlex Laboratories, Wayne, NJ) (n = 1). Diagnosis of a tumor as renal cell carcinoma was based on the following criteria: needle biopsy findings positive for renal cell carcinoma (n = 7), enlarged enhancing renal mass at CT with two nondiagnostic biopsies (n = 1), and an enlarged enhancing mass at MR imaging (n = 1). Although biopsy proof was not available for two tumors, their solid nature, enhancement, and enlargement at serial imaging supported their inclusion in this study. Preablation contrast-enhanced and nonenhanced CT scans were obtained in all patients who had a baseline creatinine level of 2 mg/dL (152.5 µmol/L) or lower. Otherwise, contrast-enhanced and nonenhanced MR imaging was performed.
Tumor size ranged from 1.2 to 5.0 cm in largest diameter, with a mean diameter (± SD) of 3.3 cm ± 1.1. The enhancement of all lesions was greater than 15 HU. The tumor assessed with MR imaging was enhancing on the basis of qualitative evaluation of the pre- and postcontrast images. Six tumors were larger than 3 cm, and three were 3 cm or smaller. Five tumors were classified as exophytic, which we defined as at least 25% of the tumor extending beyond the renal contour with no tumor extending into or up to the renal sinus (Fig 1). Three tumors were classified as central, which we defined as tumor limited to the confines of the renal contour and extending into the sinus. One tumor was classified as mixed because it showed both extension into the renal sinus and extension beyond the renal contour.
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RF Ablation Procedure
All RF ablation treatments were scheduled as outpatient procedures to be performed early in the day to allow appropriate postprocedural monitoring of patients for possible complications that might necessitate hospital admission or additional treatment before discharge. All procedures were performed with intravenous sedation that consisted of midazolam (2–5 mg), fentanyl (100–300 mg), and droperidol (0.625 mg), as needed. Intravenous sedation was induced by an interventional radiology nurse according to institutional guidelines. Monitoring of vital signs, cardiac rhythm, and pulse oximetry was performed. In addition to intravenous analgesia, local analgesia with 1% lidocaine was administered.
RF ablation was performed with an RF generator (Cosman Coagulator CC-1; Radionics, Burlington, Mass) by using a single (with one 2.0–3.0-cm tip) or cluster (with three 2.5-cm tips) cooled-tip electrode. The type (single or cluster) of electrode and length of the exposed tip were chosen by the operator on the basis of tumor size and location. In general, tumors 3 cm or smaller were treated with a single electrode. Tumors larger than 3 cm were treated with a single electrode when they were exophytic, with the exception of one area of residual disease, which was treated with a cluster electrode. Early in our experience, we treated one central tumor with a single electrode. However, the limited effect of the single electrode on a large central tumor led us to treat subsequent central tumors with a cluster electrode, which has a cluster of three tips. Cooling of the electrode tip was accomplished by using perfusion of iced saline solution or water (17). Once the electrodes were deemed to be in the appropriate location for treatment, a 12-minute treatment session was performed by increasing the current to 1,500–1,800 mA for 1 minute and monitoring the impedance for any rapid increase over baseline.
Pulsing of current (ie, temporarily reducing the RF current for 10–15 seconds) was performed, as necessary, when rapid increases in impedance were measured. Initially, pulsing was performed manually by the operator. During the course of the study, however, a computer chip that allowed pulsing to be automated became available. Pulsing is performed in response to rapid increases in impedance, which are usually related to local tissue charring, which limits further heat diffusion. Reducing the current limits the charring. The current is then increased slowly to a therapeutic level. This RF ablation technique has been previously optimized in liver tumors to maximize treated volumes (18).
Once the 12-minute treatment was complete, the electrode was placed in a different location in the tumor, if needed, to treat the entire volume of the tumor. A treatment was defined as one 12-minute RF application. A session was defined as one visit to the radiology department, where one or more RF applications were performed. During a visit, the need for additional treatments was determined on the basis of tumor size and shape. Small tumors were treated with a single placement of the electrode centrally within the tumor. Larger and/or complex-shaped tumors were treated by placing the electrodes eccentrically in the tumor to create overlapping volumes of ablated tumor. Second and third treatments were performed, as needed, in the same manner. Because neither the US nor nonenhanced CT findings during RF ablation of liver or other tumors reliably predict the treatment results, the imaging findings observed during the procedure were not used to guide therapy (19). However, for tumors treated with US guidance, the changes in lesion echotexture during and after RF ablation were noted.
Postprocedural Monitoring
Physiologic monitoring was continued during the recovery period in the interventional radiology recovery unit, where patient activity was allowed to increase as tolerated after 2 hours of bed rest. All patients were monitored for pain, hypotension, and hematuria after the procedure. Microscopic hematuria was assessed with reagent strips (Multistix; Bayer Diagnostics, Elkhart, Ind). Patients were discharged to the care of another adult 3–4 hours after the procedure when the following criteria were met: stable vital signs, no residual gross hematuria in the most recent urine specimen, no substantial flank pain at rest, and toleration of oral intake of liquids and solids. Otherwise, the patients were admitted to the hospital.
Postprocedural CT imaging on the day of the procedure was not routinely performed; it was performed only when the interventional radiologist was concerned about a complication such as hematoma. The clinical parameters that determined the need for immediate postprocedural CT were postprocedural hypotension, higher than expected degree of pain or tenderness, and/or gross hematuria.
Postprocedural Imaging Assessment
All patients were followed up with contrast-enhanced imaging. The imaging study of choice was focused renal CT, with 5-mm sections obtained with and without intravenous contrast material. The patients were monitored by using CT (n = 7), with the exception of one patient, in whom impaired renal function (ie, creatinine level >2 mg/dL [152.5 µmol/L]) precluded the administration of iodinated contrast material. In this patient, gadolinium-enhanced MR imaging was used to monitor treatment. Postablation imaging was performed at 1, 3, and 6 months. Two authors (D.A.G., P.R.M.) evaluated the postprocedural images for tumor size, tumor enhancement, and evidence of metastatic disease by means of consensus. Subsequent imaging was performed at 6-month intervals. Patients with residual enhancing tumor were re-treated with RF ablation targeting the area that showed persistent enhancement. Any lesion that was enhancing more than 10 HU after contrast material administration was considered to be untreated tumor. At MR imaging, any qualitative increase in the signal intensity of the tumor after contrast material administration was considered to be untreated tumor. Our bases for this protocol were data extrapolated from the radiologic-pathologic correlation in liver tumors performed by Goldberg et al (20). Repeat biopsy was not performed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Patient Follow-up
Complete results, by patient and tumor characteristics, are given in the Table. Six-month follow-up imaging data were available in seven of the eight patients. The length of follow-up ranged from 3 to 21 months (mean, 10.3 months). Seven of nine tumors were completely treated. The smaller and exophytic tumors necessitated fewer treatments than did the larger central tumors.
Small Exophytic Tumors
All three small (3-cm) exophytic tumors were completely free of enhancement at 6 months or longer (Fig 2). These lesions necessitated only one treatment, which was performed with a single internally cooled RF electrode and US guidance. Two lesions were treated with a 2-cm active electrode tip, and one was treated with a 3-cm active electrode tip. One of these patients died of leukemia diagnosed 6 months after RF ablation, and two were alive and healthy 13 and 21 months after ablation.
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The third patient with a large central lesion had a 5-cm tumor that demonstrated interval enlargement during 6 months. US-guided RF ablation was performed in two treatments with a cluster electrode. Subsequent CT depicted enlargement of the tumor to 7 cm and very little (<15%) treatment effect. The patient was re-treated in two additional treatments with CT guidance and a 2.5-cm cluster electrode. Imaging within 1 month after the second visit demonstrated that the tumor size had decreased to 6 cm, and approximately 70% of the tumor was enhancing.
Mixed Tumors
We treated one mixed tumor, which was 4.1 cm in diameter with extension beyond the renal parenchyma both into the central sinus fat and beyond the outer renal contour. This patient required two visits and four US-guided RF applications with a cluster electrode. Follow-up MR imaging 1 month after the second visit depicted no residual enhancement and a decrease in tumor size.
Summary of Patient Results
All five exophytic tumors and all three tumors 3 cm or smaller were free of enhancement at 6 months or longer after ablation; only one of the three central tumors was free of enhancement. The two tumors with persistent enhancement were larger (4.4 and 5.0 cm) and necessitated repeat treatments: One patient required treatment during four separate visits, and the other required treatment during two visits. Approximately 80% of one of these tumors was treated. Less than 50% of the other tumor was treated, but RF ablation seemed to have stopped its enlargement. No patients developed metastatic disease during the study period. In addition, renal function remained stable in all patients, as evidenced by their creatinine levels. At the end of the study, all but one patient were alive and none had manifestations of renal cell carcinoma.
Imaging
As described with RF ablation of liver lesions, the US findings during RF ablation of renal cell carcinoma were intense echoes spreading from the active electrode tip. In all cases, these echoes reversed 5–10 minutes following treatment, leaving the lesions of heterogeneous echotexture; there was no correlation between the US appearance and the later findings at contrast-enhanced CT or MR imaging. Early in our experience, one patient underwent contrast-enhanced CT the day of the procedure; this resulted in an underestimation of the residual disease seen at 1-month follow-up. On the basis of this experience, we changed our practice and no longer obtain a routine CT or MR image on the same day of the procedure.
Five tumors (in four patients) showed no enhancement after one visit (Fig 2). Imaging within 1 month after the procedure demonstrated residual enhancement in four tumors, which were all re-treated (Figs 3, 4). Two of these four patients had no residual enhancing tumor at imaging after the second session. The seven tumors that no longer show enhancement showed a decrease in at least one axial dimension over time.
Complications
Two complications were noted during 14 visits. One patient experienced a 5–10-minute dystonic reaction to fentanyl. His extremities and chest wall became rigid, but he maintained spontaneous respiration despite being unresponsive to commands and painful stimuli. He recovered rapidly, and afterward we were able to complete the procedure. During the same visit, further therapy for a second tumor in this patient was without incident. Because he had no family at home, he was admitted for overnight observation and discharged in good condition the next morning.
The patient with the largest central lesion and a solitary kidney experienced transient hypotension accompanied by flank tenderness within 1 hour after RF ablation. CT depicted a large paranephric space hematoma and blood within the renal pelvis. The patient was anuric from clot obstructing the collecting system and experienced a transient increased creatinine level—from 1.7 (129.6 µmol/L) to 2.9 mg/dL (221.1 µmol/L). Treatment consisted of cystoscopic ureteral stent placement and blood transfusion. The patient was discharged 3 days later, and his creatinine level returned to baseline. He recovered completely and continued with RF ablation of residual tumor.
Although gross hematuria was seen only in the patient with the major hemorrhage, microscopic hematuria was common. The first urine specimen from five (62%) of the eight patients showed microscopic hematuria. In all cases, the microscopic hematuria resolved prior to discharge.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Our early results with RF ablation of renal cell carcinoma are encouraging for lesions 3 cm or smaller and exophytic lesions, all of which were successfully treated, as proved by the imaging criteria. Treatment of large central lesions proved to be more challenging: More treatments and patient visits were required for these tumors compared with those for their small or exophytic counterparts.
A key limitation of RF ablation is the size of the lesion that can be successfully treated. Despite advances in electrode design that permit large volume coagulation in ex vivo tissue, complete ablation of tumors larger than 3–4 cm has been challenging (10,17,23,24). One reason is that blood flow through and around tumor has a cooling or "heat sink" effect by constantly replacing heated blood with cooler blood at body temperature. Thus, coagulation in in vivo liver, with its dual blood supply from the portal vein and hepatic artery, yields smaller ablated tissue volumes than does coagulation in muscle (17,24). Renal parenchyma is highly vascular because kidneys are perfused by 20% of the circulating blood volume. Thus, central tumors surrounded by renal parenchyma, with its high blood flow and large central vessels, are expected to be more difficult to treat than exophytic tumors surrounded by perirenal fat, which is relatively avascular.
On the other hand, with exophytic lesions, the location may be beneficial. Fat has an insulating effect and thus increases the temperatures that can be reached in the tumor. This is analogous to the so-called "oven effect," which has been described in hepatomas and results from the insulation provided by the hepatoma capsule and the cirrhotic liver (25). These considerations led us to adopt the classification scheme shown in Figure 1 to allow assessment of RF treatment results on the basis of tumor location.
As was expected because of their small size and favorable location, all three of the small (3-cm) exophytic lesions in our study were treated during one visit and with one treatment each. One of the large (>3-cm) exophytic tumors was treated with a single placement of a 3-cm single electrode. This tumor was 3.5 cm and nearly completely surrounded by fat. However, more aggressive treatment—that is, with cluster electrodes and multiple treatments—was required for the second large exophytic tumor, which was treated completely but necessitated a second visit.
Tumor enhancement was eradicated with a single treatment in one of three patients with a large central lesion. This tumor was a recurrent renal cell carcinoma in a partial nephrectomy bed that was treated with a single treatment with a cluster probe. There probably was substantial scarring and fibrosis associated with this tumor, as indicated by the resistance felt when the biopsy needle and RF electrodes were advanced. Surrounding fibrosis is expected to reduce thermal conduction and thus improve tumor treatment. The other two tumors of this type were larger and necessitated more aggressive treatment. Although complete treatment may have been elusive in the largest tumor, RF ablation probably played a palliative role in slowing tumor growth.
Treatment of mixed lesions is expected to yield intermediate results. In the current study, our experience with these types of lesions was limited to a single tumor, with 3 months of follow-up and no residual enhancement after four treatments.
We have found that the preprocedural visit is indispensable in planning the procedure and facilitating a timely start on the day of the procedure. Coagulation studies and the appropriate choice of imaging guidance are all addressed before the day of the procedure. In addition, the education and consent processes for therapeutic procedures directed to tumor therapy can be time consuming. Patients and families need many questions answered and their fears addressed. The opportunity to return home and discuss the procedure with family and consider all the options rather than rushing into the procedure served our patients well. Attention to these details during the preprocedural visit reduced the procedure time.
The two complications encountered in our series were managed without long-term adverse effects on the patients. The reaction to fentanyl was not directly related to the procedure. Even major complications, such as the hemorrhage requiring transfusion and ureteral stent placement, can be managed without an operative procedure in most cases. However, the operator and patient should be prepared for hospital admission if necessary. Furthermore, patients with solitary kidneys should be informed of the possibility of renal injury leading to loss of function and the need for dialysis.
To our knowledge, little is known about the imaging appearance of renal cell carcinoma after RF ablation. As with those during RF ablation of liver lesions, findings during US-guided RF ablation do not accurately reflect the ultimate treatment result (19). During RF ablation, the tumor surrounding the electrodes becomes intensely echogenic, but the tissue volume treated does not correlate with the distribution of these echoes (26). These echoes usually resolve within minutes after RF ablation and are thought to be secondary to microbubbles generated during tissue ablation. Immediate contrast-enhanced CT has resulted in an underestimation of residual disease in many of our patients who have undergone RF ablation of liver lesions. On the basis of these experiences, we consider immediate contrast-enhanced CT to be unreliable for assessing the adequacy of ablation.
We assessed our follow-up posttreatment images with the same criteria that are used for primary and secondary liver tumors treated with RF ablation. In liver lesions, residual or new areas of enhancement have been shown to correlate with active tumor at pathologic analysis (19,20). We assessed the treated renal cell carcinomas for lesion size and enhancement. Residual areas of enhancement were considered to represent active disease and thus re-treated. On the basis of our preliminary experience, this approach appears to be justified. However, our mean follow-up time of 10.3 months was short with respect to the expected growth rate of small renal cell carcinomas (21,22). Long-term results are needed to assess the possible small regions of residual tumor that are below the resolution of our imaging capabilities.
The appropriate role of RF ablation of small tumors probably will evolve. Tumors smaller than 3 cm are known to have a slow growth rate, and some investigators (18,19) have advocated serial imaging of these tumors in older or debilitated patients because these individuals may never have substantial clinical problems related to these small renal cell carcinomas. Given that, according to extensive experience with liver tumors and the results of our more limited series of renal tumors, the general success rate of RF ablation decreases with increasing tumor size, serial imaging may be appropriate until a lesion reaches 2.5–3.0 cm in maximum dimension or shows rapid growth not related to hemorrhage. Percutaneous RF ablation would then be a minimally invasive alternative to surgery.
In conclusion, percutaneous RF ablation is a promising minimally invasive therapeutic modality with an evolving role in the management of select cases of renal cell carcinoma. Treatment is more likely to be successful with smaller (3-cm) and exophytic tumors. Although longer-term patient follow-up is needed, our preliminary results are encouraging.
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, all authors; study concepts and design, all authors; definition of intellectual content, all authors; literature research, S.N.G., D.A.G.; clinical studies, all authors; data acquisition, P.R.M., D.A.G.; data analysis, all authors; manuscript preparation, all authors; manuscript editing, D.A.G.; manuscript review, all authors.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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