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Original Research |
1 Department of Radiology, Massachusetts General Hospital, 55 Fruit St., White
270, Boston, MA 02114.
2 Department of Urology, Massachusetts General Hospital, Boston, MA 02114.
Received June 29, 2004;
accepted after revision October 6, 2004.
Address correspondence to D. A. Gervais.
Abstract
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MATERIALS AND METHODS. Over a 6-year period, 100 renal tumors in 85 patients underwent radiofrequency ablation at a single institution. The absence of enhancement on CT or MRI after radiofrequency ablation was interpreted as complete coagulation necrosis. Results were analyzed by tumor size and location using multivariate analysis. A p value of 0.05 or less was considered significant.
RESULTS. All 52 small (3 cm) and all 68 exophytic tumors underwent complete necrosis regardless of size, although many large tumors (> 3 cm) required a second ablation session. Using multivariate analysis, we found that both small size (p < 0.0001) and noncentral location (p = 0.0049) proved to be independent predictors of complete necrosis after a single ablation session. Location was a significant predictor (p = 0.015) of complete necrosis after any number of sessions, whereas size showed a strong trend (p = 0.059) toward predicting success after any number of sessions. Complications were either self-limited or readily treated and included hemorrhage (major, n = 2; minor, n = 3), inflammatory track mass (n = 1), transient lumbar plexus pain (n = 2), ureteral injury (n = 2), and skin burns (n =1).
CONCLUSION. Radiofrequency ablation is a promising minimally invasive therapy for renal cell carcinoma in patients who are not good operative candidates. Small size and noncentral location are favorable tumor characteristics, although large tumors can sometimes be successfully treated with multiple ablation sessions.
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As new therapies are introduced, 5-year results are compared with those for conventional open nephrectomy. Although the literature currently contains several series of small renal cell carcinomas treated with percutaneous radiofrequency ablation, all these series report mean low follow-up periods of less than 2 years [8-15]. Thus, 5-year results of substantial cohorts of patients are awaited. Nevertheless, several issues with respect to performance of radiofrequency ablation of renal masses can be addressed on the basis of current experience. We undertook these studies to review our experience with radiofrequency ablation of 100 renal masses. In this article, part 1, we review indications, technique, results based on size and location, clinical and imaging follow-up, and complications. In part 2, we review technical considerations such as patterns of residual disease and approach to ablation of residual disease, effects on the collecting system, considerations for bowel displacement, and angle of approach of the electrode relative to the mass.
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Ninety tumors were biopsy-proven renal cell carcinomas with both fine-needle aspirates and 18-gauge cores obtained at biopsy. Treatment for two patients was based on imaging findings: One patient was treated on the basis of finding an enlarging mass on serial MRI, and another was treated on the basis of finding an enlarging mass on CT after an unrevealing biopsy. A third patient twice underwent biopsy of a complex cystic-solid mass without evidence of malignancy, but subsequent biopsy of an isolated sacral lesion proved to be metastatic renal cell carcinoma. This isolated renal mass was then treated with radiofrequency ablation on the basis of the biopsy findings. An additional seven tumors were treated without biopsy based on imaging findings of both an enhancing mass and biopsy-proven renal cell carcinoma of a separate renal mass in the same patient. Biopsies were generally performed at a separate visit from the radiofrequency ablation except in 19 patients. However, biopsy and radiofrequency ablation were performed during the same visit in 19 patients who either had von Hippel-Lindau disease or required hospitalization for reversal of warfarin therapy.
Initially, radiofrequency ablation was limited to patients without metastatic disease. However, after we were able to achieve local control of renal cell carcinoma in several cases, we performed radiofrequency ablation in suitable tumors in patients with limited metastatic disease and documentation of very slow progression. Among the 85 patients, four had limited nonprogressive metastatic disease treated with immunotherapy, radiation, or surgery. In addition, one patient had two small pancreatic metastases discovered only in retrospect on preablation CT.
Radiofrequency Ablation
Radiofrequency ablation was performed by one of three radiologists with
experience in radiofrequency ablation as the primary operator in consultation
with the other two radiologists with respect to treatment planning. The choice
of imaging technique and radiofrequency system was at the discretion of the
primary operator. Multiple overlapping ablations were performed as needed to
cover the entire tumor. The systems used and number of ablation sessions by
tumor size are listed in Table
1. If residual disease was detected on imaging after ablation,
repeat ablation sessions were scheduled as needed and as appropriate depending
on the clinical status of the patient. In this fashion, a total of 429
ablations were performed over 126 radiofrequency ablation sessions, 114
sessions with CT guidance and 12 sessions with sonography guidance.
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Two monopolar radiofrequency systems were available. A 200-W generator with internally cooled electrodes (Cool-Tip, Valleylab) and impedance-controlled pulsed current was used in 121 ablation sessions [16-18]. Each overlapping ablation was 12 min in duration. In 15 ablation sessions, tumors were ablated with a 150-W generator using multitined expandable electrodes ([3-5 cm] Starburst XL, RITA Medical Systems) and a target temperature of 105°C. Tract ablation was not routinely performed, but was performed if the risk of hemorrhage was thought to be elevated such as in cases of central tumors, coagulopathy, or evidence of bleeding during the procedure. The electrode used for each tumor was chosen to maximize the volume of tumor that would undergo coagulation necrosis in a session.
For the Radionics system, 40 tumors were initially ablated with single electrodes and 52 with cluster electrodes. The decision as to which electrode to use for the Radionics system was determined by the attending radiologist on the basis of the following guidelines: All tumors except one that were 1.5 cm or less were treated with a single electrode. The exception was the use of a cluster electrode in a patient whose first tumor required a cluster electrode, but who also had a second small tumor for which we used the same electrode. Tumors between 1.5 and 3.5 cm were treated with single or cluster electrodes at the discretion of the attending radiologist involved in the case. Tumors that were 3.5 cm or larger were treated with a cluster electrode. The exceptions—tumors larger than 3.5 cm for which single electrodes were used—included a long but narrow tumor in which the electrode could be advanced along the long axis of the tumor, a tumor near bowel for which there was concern that the greater pressure needed to insert the cluster electrode would push the tumor so that it would be adjacent to bowel, and our first central tumor.
Radiofrequency ablation was performed while patients were sedated. IV sedation consisted of 100-300 mg of fentanyl citrate (Sublimaze, Janssen) and 2-5 mg of midazolam (Versed, Baxter). In addition, 0.625 mg of droperidol (Inapsine, Akorn) was used before 2001 when droperidol became unavailable. Subsequent patients received 25-50 mg of meperidine hydrochloride (Demerol, Abbott Laboratories) if needed. Radiofrequency ablation was performed as an outpatient procedure in most patients. Admission was reserved for patients who required reversal of anticoagulation with warfarin, those with extreme frailty due to severe comorbid conditions, and those with hemorrhagic complications after radiofrequency ablation.
A total of 62 patients underwent radiofrequency ablation as outpatients, and 22 patients were admitted. One patient was in the hospital for other indications at the time of radiofrequency ablation. Five patients had pacemakers, and radiofrequency ablation was performed with the pacemakers on but not in the path of the electrical circuit (i.e., all grounding pads were placed on patients' thighs). These patients with a pacemaker were followed by the cardiology service after the radiofrequency ablation.
Imaging Follow-Up
All patients underwent contrast-enhanced imaging (MRI or CT) before
radiofrequency ablation that served as a baseline comparison for subsequent
imaging after ablation. Patients with a serum creatinine level of 2.0 mg/dL or
less (n = 73) were followed with unenhanced and enhanced CT
(LightSpeed, GE Healthcare): Before 1999, single-detector only was performed;
in 1999, 4-MDCT was available; and in 2003, 16-MDCT was available. Patients
with a serum creatinine level of greater than 2.0 mg/dL (n = 12) were
followed with MRI (Signa, GE Healthcare): T1-weighted, T2-weighted, and fast
spin-echo gradient-echo sequences were performed before and after gadolinium
enhancement (gadopentetate dimeglumine [Magnevist, Berlex]). All five patients
with pacemakers received iodinated contrast material for CT, but two patients
required premedication. One patient required prednisone and diphenhydramine
hydrochloride because of a history of allergy, and another required
N-acetylcysteine because of a creatinine level of 2.5 mg/dL.
After radiofrequency ablation, CT or MRI without and with contrast material was performed at 1 month, 3 months, and 6 months. Subsequent imaging follow-up depended on the clinical condition of the patient and comorbid conditions, but was generally at 6- to 12-month intervals.
Images obtained after ablation were interpreted by consensus of two experienced radiologists using the criteria established by Gervais et al. [15]. Enhancement of any portion of the tumor was considered residual viable tumor, and the absence of enhancement was considered complete necrosis and thus completely ablated tumor. Images were also reviewed for the presence of any new metastatic disease or new renal tumors. Recurrence was defined as new enhancement developing after CT or MR images had been interpreted to show complete necrosis. Patients were also monitored for complications and the need for dialysis.
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Multivariate analyses (Cochran-Mantel-Haenszel) were performed to assess the effect of size and location on results of ablation (SAS software [version 6], SAS Institute). Results were assessed for the achievement of complete necrosis by 6 months regardless of the number of ablation sessions and also by the achievement of complete necrosis after a single ablation session. A p value of 0.05 or less was considered significant. Because some centers limit their use of radiofrequency ablation to small tumors and the definition of a small tumor with respect to consideration for radiofrequency ablation ranges from 2.5 to 4.0 cm in the literature, we sought to determine what tumor size would present acceptable sensitivity and specificity levels for the prediction of successful ablation using receiver operating characteristic (ROC) curve analysis.
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Tumor Location
With respect to location, all 67 exophytic tumors that have been evaluated
by the standard imaging criteria underwent complete ablation. One other
exophytic tumor is the tumor followed by size because of absence of
enhancement before ablation. Seven (78%) of nine central tumors were
completely ablated. Eleven (61%) of 18 tumors of the mixed type with both
exophytic and central components underwent complete ablation. Five (100%) of
five parenchymal tumors with neither exophytic nor central components
underwent complete ablation.
Size Versus Location
Multivariate analysis assessing the effect of tumor size and location with
respect to the likelihood of complete necrosis after the first ablation
session showed that both small size (p < 0.0001; odds ratio,
12.5:1) and noncentral location (p = 0.0049; odds ratio, 5.6:1) were
independent predictors of success. Multivariate analysis assessing the same
variables as predictors of complete necrosis after any number of ablation
sessions showed that noncentral location (p = 0.015; odds ratio,
10.5:1) was a predictor of treatment success and that small size showed a
strong trend toward predicting success but did not quite reach statistical
significance (p = 0.059). This latter result is likely related to the
fact that several tumors from 3.1 to 5.5 cm were completely ablated. Of note,
no tumors larger than 5.5 cm were completely ablated.
Sensitivity and Specificity of Size as a Predictor of Complete Necrosis
Assessment of sensitivity and specificity for tumor size as a determinant
of achievement of complete necrosis regardless of the number of ablation
sessions resulted in an ROC curve with an area under the curve of 95%
(Fig. 4). The ROC analysis
yields a critical test result value of less than 4 cm for a specificity of
90%, meaning that the use of this size cutoff by those who limit ablation to
small tumors would achieve complete necrosis in 90% of cases. However, the
corresponding sensitivity would be only 85%, which indicates that 15% of
patients for whom complete necrosis could be achieved would be excluded from
radiofrequency ablation. At the other end of the size range, the ROC curve
predicts a critical test result value for sensitivity of 90% for tumors less
than 4.2 cm and 99% for tumors less than 5.8 cm. This analysis indicates that
use of 4.2 cm or 5.8 cm as the exclusion criterion would include 90% and 99%,
respectively, of all tumors for which complete necrosis can be achieved.
Likewise, tumors larger than 5.8 cm are not likely to be completely treated
with radiofrequency ablation alone. Corresponding specificities at these
levels drop to 87% and 63%, respectively.
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A single case of local progression was detected at 1 year 2 months after radiofrequency ablation in a patient with a 3.2-cm tumor. In retrospect, viable tumor was present on earlier imaging but was impossible to differentiate from volume-averaging artifact on CT. This recurrence was treated with radiofrequency ablation with achievement of complete necrosis stable over 1.5 years.
Three patients eventually underwent dialysis. The first two patients both had abnormal renal function at the time of ablation despite the fact that both kidneys were functioning. The rate of the rise in the blood creatinine levels after ablation remained the same as the rate of rise before ablation, which suggests that radiofrequency ablation had little to do with the patients' progressive renal insufficiency and likely temporarily deferred them from dialysis that a more aggressive surgical procedure could have accelerated. One patient with a solitary kidney required dialysis 3 months after ablation for renal failure of unknown cause.
New Tumors
Three patients developed new renal tumors. Of these three, one patient with
von Hippel-Lindau disease is awaiting radiofrequency ablation of new tumors.
The other two patients both had undergone contralateral nephrectomy for renal
cell carcinoma before radiofrequency ablation, and both underwent
radiofrequency ablation of additional tumors remote from the initial ablation
site.
Three patients developed new metastatic disease during the follow-up period. Two of these patients had preexisting metastatic disease before radiofrequency ablation; both developed new metastases to the pancreas, one diagnosed by imaging and resected and the other diagnosed at pathology after resection of a primary pancreatic adenocarcinoma. The third patient had had a contralateral nephrectomy, and we were unsuccessful in completely treating the tumor despite two radiofrequency ablation sessions. A small lung metastasis was resected at 3 years. At 4.5 years, because of very slow growth of the renal mass, radiofrequency ablation was attempted again and was successful.
Complications
The most common complication was hemorrhage, which was seen in five
patients. Two patients experienced major hemorrhage requiring RBC transfusion
and stent placement for ureteral obstruction in one and RBC transfusion for a
subcapsular hematoma in the other. Three patients experienced minor hemorrhage
not requiring transfusion that was managed with bladder catheter placement for
bladder outlet obstruction (n = 2) and conservative management for
mild transient ureteral obstruction (n = 1). Three of these five
patients had central tumors. In all five cases, hemorrhage was diagnosed at
the end of the ablation session. There were no delayed cases of
hemorrhage.
One patient developed an asymptomatic posterior abdominal wall enhancing mass with inflammatory changes initially diagnosed as tumor tract seeding on the basis of imaging findings at 6 months. At surgical excision of this abdominal wall mass, pathology revealed acute and chronic inflammation with histiocytes predominating and no malignancy. Less common major complications included ureteral stricture (n = 1), treated with nephrostomy and ureteral stent placement, and urinoma and ureteral injury (n =1), treated with percutaneous drainage and nephroureteral catheter placement. Less common minor complications included first- and second-degree burns at a grounding pad site for the multitined expandable electrode device (n = 1), which were successfully treated in consultation with our burn service. Transient neuropathic pain along the distribution of the lumbar plexus (n = 2) was treated conservatively. Except the inflammatory mass, all complications were detected at the time of ablation or within 24 hr of ablation. There were no cases of bowel perforation or tumor seeding.
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We are the first, to our knowledge, to use multivariate analysis to assess tumor size and location as independent predictors of the results of radiofrequency ablation. Prior series have been too small for a multivariate analysis, and these variables were evaluated using univariate analysis in the past. With our large series, we have shown that both small size and a noncentral location are independent significant predictors of complete necrosis after a single ablation session. Likewise, location is a significant predictor of the ability to achieve complete necrosis after any number of ablation sessions, a reflection of the insulating effect of perirenal fat and the cooling effects of larger central blood vessels [19, 20]. Small size showed a strong trend as a predictor of complete necrosis after any number of sessions.
The importance of performing these analyses in this fashion is more than academic. Patients and referring physicians need to know that radiofrequency ablation may require multiple ablation sessions to achieve complete necrosis and that tumor characteristics such as size and location will influence the likelihood of requiring more than one session. For example, 44% (16 of 36) of the tumors between 3 and 5 cm required more than one ablation session to achieve complete necrosis in our series. This information may be useful in the future if radiofrequency ablation proves to be equivalent to surgical alternatives—for example, if a patient needs to decide between radiofrequency ablation and a laparoscopic partial nephrectomy. Although surgical removal is a single procedure that generally succeeds in complete tumor removal, radiofrequency ablation may require two or more ablation sessions to achieve complete necrosis for tumors between 3 and 5 cm. These considerations may prove vital in decision making for patient management depending on individual patient preferences.
The question of upper size limits for consideration of renal tumors for radiofrequency ablation remains open in the literature. Various investigators have set this limit from 2.5 to 4.0 cm [6, 8-15]. Fitting our data to an ROC curve allows assessment of the sensitivity and specificity of various tumor sizes that might be considered as the exclusion criterion for radiofrequency ablation. Simply stated, what this tool allows us to determine are the answers to two questions. First, what size cutoff allows us to include only those patients who are highly likely to experience complete necrosis after radiofrequency ablation despite excluding some patients who could undergo complete necrosis? Second, what size cutoff will include all those patients who would experience complete necrosis with radiofrequency ablation despite the inclusion of others who will not? Stated this way, the parallels with sensitivity and specificity become clear. Those interventional radiologists who choose to limit their practice to small tumors to ensure a high likelihood of complete necrosis can achieve 90% complete necrosis limiting radiofrequency ablation to tumors less than 4.0 cm, but will exclude 15% of patients who might benefit from this therapy. On the other hand, those striving to include all patients who could possibly be completely treated regardless of the fact that some might not be completely treated could increase the size cutoff to 5.8 cm to include 99% of patients who could achieve complete necrosis while incurring a decrease in the rate of complete necrosis to 63%.
These considerations will be of even greater importance in the future if radiofrequency ablation proves to be a viable alternative in patients who are surgical candidates. For patients who are surgical candidates, a higher likelihood of complete necrosis would be favored because these patients are eligible for curative surgery and should consider radiofrequency ablation only if the likelihood of complete necrosis is high. However, patients for whom no surgical options exist would favor a more inclusive value regardless of a lower likelihood of success because they should not be excluded from a potentially curative therapy in the absence of surgical options. Moreover, as tumor size approaches 6 cm, consideration of combination therapy with embolization and radiofrequency ablation in patients without surgical options may, in part, overcome the limitations of radiofrequency ablation alone [21]. The complexities involved in these considerations underscore the importance of a collaborative approach to each patient with evaluation by both the urologist and the interventional radiologist.
Our inclusion of four patients with isolated metastatic disease brings forth another patient population in whom radiofrequency ablation has not previously been evaluated. Although most series have restricted the use of radiofrequency ablation to patients without metastases, isolated slow-growing metastases are currently being treated by surgical resection, immunotherapy, or both and, in some cases, radiofrequency ablation [22, 23]. Thus, in such patients, if the characteristics of the renal mass are favorable, radiofrequency ablation may become one of multiple therapies aimed at controlling the tumor burden. Given the limited number of patients with metastatic disease in our series, further study will be necessary to determine the optimal candidates for this therapy, especially because patients with extensive or multifocal disease will not likely benefit from treatment of the primary tumor.
Another small population that can be problematic for imaging follow-up is the rare renal cell carcinoma that does not enhance at all before ablation. In our series, one patient presented with an isolated metastasis despite two negative biopsies of the renal mass. Thus, in the setting of extrarenal disease, radiofrequency ablation with close imaging observation for size changes proved to be clinically acceptable. However, for similar tumors in patients without metastatic disease, radiofrequency ablation may not be the optimal treatment.
The issue of local progression after complete treatment as documented by imaging will merit close attention with longer follow-up periods. Thus far, we have a single "recurrence" at 14 months that, in retrospect, was present even at 1-month imaging but could not be differentiated from volume-averaging artifact. This case illustrates the limitations of imaging with respect to the detection of residual tumor. Given the new developments in MDCT technology of the past few years, evaluation of postablation imaging with 16-MDCT scanners or scanners with even more detectors and multiplanar reconstructions will warrant future investigation as a possible means of decreasing false-negative studies [24].
Although our series represents the longest follow-up period at 2.3 years, we still fall short of the 5-year results required to compare radiofrequency ablation with surgical removal. These results will be awaited for some time, and, in the meantime, radiofrequency ablation will be indicated for selected patients as delineated herein. Outcomes thus far are acceptable with the few deaths from other causes expected in a population with preexisting morbid conditions. The absence of new metastases and the low recurrence rate in 80 patients without preexisting metastatic disease will ensure continued evaluation of radiofrequency ablation as a treatment for selected cases of renal cell carcinoma. The complication rates are acceptable, with hemorrhage being the most common complication and seen most commonly, although not exclusively, in central tumors.
Acknowledgments
We wish to thank Elkan F. Halpern for his assistance with the statistical
analysis in preparation of this manuscript.
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