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Original Research |
1 Department of Radiology, Mayo Clinic, 200 1st St. SW, Rochester, MN
55902.
2 Department of Urology, Mayo Clinic, Rochester, MN.
Received August 28, 2006;
accepted after revision October 31, 2006.
Address correspondence to T. D. Atwell
(atwell.thomas{at}mayo.edu).
Abstract
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MATERIALS AND METHODS. We reviewed 40 percutaneous cryoablation procedures performed on 40 patients with renal tumors 3 cm in diameter or larger. All patients underwent cryoablation with CT monitoring. Technical success was defined by extension of the ice ball beyond the tumor margin and postablation imaging findings of no contrast enhancement in the area encompassing the original tumor. Complications meeting grade 3 of the National Cancer Institute Common Terminology Criteria for Adverse Events were recorded.
RESULTS. Mean ± SD tumor diameter was 4.2 ± 1.1 cm (range, 3.0-7.2 cm). Technical success was achieved in 38 (95%) of 40 cryoablation procedures. There was one grade 3 adverse event (3% rate of significant complications). Follow-up images obtained 3 months or longer (mean, 9 ± 6 months; range, 3-22 months) after ablation were available for 26 (65%) of the 40 patients. No local tumor recurrence or tumor progression was found.
CONCLUSION. Percutaneous cryoablation of renal tumors measuring 3 cm or larger is technically feasible and relatively safe. Short-term follow-up results are encouraging, although long-term follow-up is necessary to assess true treatment efficacy.
Keywords: cancer • cryoablation • kidney • oncology • percutaneous ablation • sonography
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A common theme in the radiofrequency ablation literature is difficulty managing larger tumors, typically defined as larger than 3 cm in diameter. Such large tumors often necessitate additional radiofrequency ablation sessions, and technical success rates are lower than those reported for smaller tumors [2, 7, 8]. Although the published findings on percutaneous cryoablation are limited, authors [3, 5, 6] have tended to treat patients with smaller tumors, usually less than 5 cm, even though cryoablation technology allows simultaneous operation of several cryoprobes to generate large confluent ice balls for tumor treatment.
Given that 80% of surgically resected renal tumors are larger than 3 cm [9], it is clear that percutaneous ablation techniques must evolve to allow management of these larger tumors if we are to offer this alternative to a greater number of appropriate patients. Such patients are typically considered at high risk for surgery because of previous renal resection or advanced comorbid medical conditions. For this reason, we reviewed our experience in the percutaneous cryoablative management of renal tumors measuring 3 cm or more in diameter.
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All patients underwent formal consultation in our department of urology. On the basis of results of critical discussion between the urologist and radiologist, patients were considered for cryoablation. Indications for percutaneous ablation included previous renal surgery in seven (17%) of the cases and comorbid medical conditions in 28 (70%). Five (13%) of the patients wanted to avoid major kidney resection and chose ablation as an alternative to surgery. In all 40 cases, cryoablation was chosen over radiofrequency ablation because of tumor size. Eleven patients had additional concerns, including proximity of renal tumors to the colon (3/40, 7%), renal collecting system (5/40, 13%), and adrenal gland (3/40, 7%).
Tumor Characteristics
All patients underwent cross-sectional imaging that showed a solid renal
mass. Maximum tumor size was determined on the basis of the largest
measurement obtained with the technique that best depicted the renal tumor.
Tumors were classified as exophytic, intraparenchymal, or central, depending
on their position relative to the renal parenchyma. Any tumor that extended
into the renal sinus fat was classified as a central tumor. Exophytic tumors
were those in which 50% or more of the circumference was outside the renal
capsule. Intraparenchymal tumors were those in which less than 50% of the
tumor circumference was outside the capsule. The location of the tumor
epicenter was recorded as upper, middle, or lower part of the kidney and as
anterior, lateral, or posterior aspect of the kidney.
In this series, we did not require tissue confirmation of renal cell carcinoma before ablation because findings at percutaneous biopsy can be unreliable in excluding this neoplasm [10, 11]. In addition, we and others [12] believe that the absence of malignant cells in a biopsy specimen cannot be used alone to conclude a renal mass is benign. Ninety percent of renal tumors larger than 3 cm are malignant [9].
Treatment Procedure
Ablation was performed by four experienced interventional radiologists with
5, 6, 5, and 25 years of experience. Oral informed consent was obtained. We
performed cryoablation under general anesthesia. Although others
[3] have had success with
conscious sedation, we find that general anesthesia allows greater control of
respiration during cryoprobe placement and maximizes patient tolerance of the
procedure.
The cryoablation system (Endocare) used allows independent and simultaneous operation of up to eight cryoprobes. The cryoprobe (Perc-24, Endocare) is a sealed 2.4-mm diameter (13-gauge) needle that, according to the manufacturer, generates an ice ball up to 3.7 cm in diameter and up to 5.7 cm along the probe shaft. Rapid expansion of argon gas in a sealed cryoprobe with a distal uninsulated portion results in rapid freezing of tissue, and the temperature can reach -100°C within seconds [13]. The diameter of the ice ball is controlled by the rate of gas delivery to the probe and the duration of freezing. Thawing is achieved by replacing the argon gas with helium gas.
Before the cryoablation procedure, images were critically reviewed for anticipated probe placement. Allowing for a 3-cm effective short-axis diameter of the ice ball, we planned 1.0- to 1.5-cm probe-shaft spacing within the tumor, overall probe positioning being defined by the geometric features of the tumor and expected ice ball size.
Cryoprobes were placed into the tumor before biopsy because bleeding after biopsy can obscure the tumor and make cryoprobe placement difficult or impossible. In the group of patients selected, two or more sterile cryoprobes were introduced through a skin nick by one or more of the participating radiologists. Sonography was used to guide cryoprobe placement. We used an Acuson Sequoia sonography system (Siemens Medical Solutions), typically with a 4- or 6-MHz transducer, although we occasionally used other transducers, depending on tumor location and conspicuity. CT was used to verify placement of the cryoprobes. Additional probes were placed if CT findings suggested the tumor might not have been completely covered with initial probe placement. After confirmation of the accuracy of the cryoprobe positions and before freezing, biopsy of the targeted renal mass usually was performed. We used an 18-gauge biopsy device (Bard Monopty, CR Bard) to obtain one or two cores of tissue. Biopsy was not performed on some patients because the tumor was obscured by the cryoprobes.
CT monitoring during ablation was performed with one of two systems (GE HiSpeed CT/i system, GE Healthcare; Somatom Sensation Open 40-MDCT system, Siemens Medical Solutions). CT has been shown accurate in monitoring of ice ball size and location and for prediction of cell death [14, 15]. Cryoprobe positions were confirmed with 2.5- to 5.0-mm slice thickness with standard CT technique (120 kV peak and approximately 240 mA). Each lesion was subjected to a single treatment cycle of freezing, thawing, and freezing again.
During the freezing portions of the cycle, limited unenhanced CT images were obtained approximately every 2 minutes at body window and level settings (width, 400; level, 40 H) and 2.5- to 5.0-mm collimation for monitoring of the growth of the ice ball. Duration of freezing was based on growth of the ice ball relative to the tumor. Reconstructed images were generated depending on the proximity of critical structures (e.g., ureter, bowel, and adrenal gland). Because complete cell death occurs approximately 3 mm inside the edge of the ice ball [16, 17], the goal was to extend the ice ball 5 mm beyond the tumor margin during both freezing portions of the cycle. The procedure was complete when the ice ball extended beyond the tumor margin during the second freeze. After the second freeze cycle, cryoprobes were actively warmed with helium gas and withdrawn when the temperature was greater than 20°C.
Technical success was defined as extension of the ice ball beyond the tumor margin and acquisition of postablation images showing no contrast enhancement in the area encompassing the original tumor. Lesion location and size, number of cryoprobes, duration of freeze and thaw periods of each cycle, maximum and minimum ice ball diameters, and serum creatinine levels before and after cryoablation were recorded for each patient.
Follow-up Imaging
Immediately after treatment and 3-6 months, 12 months, 18 months, 24
months, and 36 months after cryoablation, CT examinations were performed with
one of five MDCT scanners (LightSpeed Ultra or LightSpeed 16, GE Healthcare;
Sensation 16, Sensation 40, or Sensation 64, Siemens Medical Solutions).
Examinations were performed without and with 140 mL of IV iohexol (Omnipaque
300, Amersham Health) and included arterial (45 seconds), nephrographic (90
seconds), and excretory (300 seconds) renal phases with 2.0- to 2.5-mm slice
thickness and interval, 120 kVp, 195-350 mA, and 0.5-second rotation time.
For patients with allergies to iodinated contrast medium or with renal insufficiency, contrast-enhanced MRI examinations were performed within 48 hours of ablation with a twin-speed 1.5-T system (Signa Excite, GE Healthcare). The renal MRI examination consisted of a three-plane localizer sequence performed with single-shot fast spin-echo or a fast spoiled gradient-echo technique. This sequence was followed by a coronal single-shot fast spin-echo sequence (TE, 80; bandwidth, 83 kHz; flip angle, 110°; matrix size, 256 x 256; number of excitations, 0.5; field of view, 44 cm; slice thickness, 5 mm; interslice gap, 1 mm).
Axial in-phase and out-of-phase spoiled gradient-echo images were obtained and included the adrenal glands and kidneys (TR/TE, 100-200/2.1 and 4.2; flip angle, 70°; bandwidth, 32 kHz; matrix size, 256 x 192; number of excitations, 1; slice thickness, 6 mm; interslice gap, 1 mm). Respiration-triggered fast spin-echo T2-weighted images were obtained (TR equal to two R-R intervals; TE, 85; echo-train length, 12; bandwidth, 32 kHz; matrix size, 256 x 224; number of excitations, 2; slice thickness, 5-6; interslice gap, 1 mm). Dynamic fat-saturated 3D fast spoiled gradient-echo images were obtained before and after contrast administration (3.4/1.6; number of excitations, 0.75; bandwidth, 83 kHz; flip angle, 15°; matrix size, 256 x 224; section thickness, 3-4 mm; number of sections acquired, 50-60 with zero filling; in-plane matrix size, 512 x 512; 50% overlapping sections along z-axis).
Parallel imaging with an acceleration factor of 1.8 in the phase-encoding direction was performed with a proprietary array spatial sensitivity-encoding technique (Asset, GE Healthcare). An axial low-resolution fast spoiled gradient-echo calibration scan preceded the parallel image acquisitions. Gadodiamide (Omniscan, Amersham Health) was injected IV at a rate of 3 mL/s (final concentration, 0.1 mmol/kg). A 2-mL test bolus of contrast material was injected before acquisition of contrast-enhanced 3D images to determine the appropriate scan delay to achieve an optimal set of arterial phase images.
A second set of contrast-enhanced images was acquired approximately 10 seconds after the arterial phase images. A third set of images was acquired approximately 2 minutes after the second set was complete. Last, an axial fat-saturated 2D spoiled gradient-echo sequence (100-200/2.6; flip angle, 70°; bandwidth, 32 kHz; matrix, 256 x 192; phase, 0.75; field of view, 32-40 cm; slice thickness, 6 mm; interslice gap, 1 mm) was acquired. Field of view for all axial sequences was adjusted according to patient size and typically ranged from 34 to 44 cm and had a phase field of view of 0.70-1.0.
Follow-up CT and MRI images were examined by three reviewers to determine the extent of ablation, technical success, and presence of complications. Local tumor progression was defined as any tumor that showed intralesional enhancement or serial increase in size compared with images from the follow-up examination immediately after ablation. Biopsy was not performed as part of routine follow-up.
Complications
Clinically important complications were defined according to the National
Cancer Institute Common Terminology Criteria for Adverse Events, version 3.0
[18]. These criteria are
supported by the Cancer Therapy Evaluation Program of the National Cancer
Institute. Grade 3 (severe adverse event) or greater complications were
recorded.
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Biopsy was performed on 31 (77%) of the 40 patients. In four (13%) of the 31 cases, the findings did not yield enough information for diagnosis. Among the other 27 biopsies, tissue showed renal cell carcinoma in 18 (67%) of the patients, oncocytic tumor in three (11%), and oncocytoma in six (25%). Biopsy was not performed on nine (23%) of the 40 patients. Five of these patients had a history of renal cell carcinoma, and the other four patients had a solid enhancing renal mass.
Imaging after the cryoablation procedure showed technical success in 38 (95%) of 40 cases (Figs. 1A, 1B, 1C, 1D and 2A, 2B, 2C, 2D, 2E). One of the failures occurred in the fifth patient in the series. At the end of ablation of a 4.0-cm-diameter tumor, a small amount of residual tumor remained near the hilum of the kidney (Fig. 3A, 3B). Because the patient had only one kidney, we elected not to continue treatment for fear of complications resulting in kidney loss. The second failure occurred in a patient with a 3.6-cm central mass who did not undergo immediate imaging but did undergo contrast-enhanced CT 6 months after ablation. This scan showed residual neoplasm along the central parenchymal margin of the tumor.
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Follow-up images obtained 3 months or more (mean, 9 ± 6 months; range, 3-22 months) after ablation were available in 26 (65%) of the 40 cases. The mean size of the 26 tumors was 4.2 ± 1.1 cm (range, 3.0-7.2 cm). There was no local tumor recurrence or tumor progression.
A complication meeting the criteria for grade 3 adverse event according the National Cancer Institute common terminology criteria occurred in one (3%) of the patients. A large hemorrhage occurred immediately after seven-cryoprobe ablation of a 7.2-cm mass in the right kidney, the largest tumor in the group. The patient underwent emergency angiography, which showed no active hemorrhage. This patient was the one in whom transient renal failure necessitated temporary dialysis.
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Other authors also have had difficulty with radiofrequency ablation in the management of large renal tumors. Varkarakis et al. [19] found three tumor recurrences after radiofrequency ablation of 56 tumors. The three tumors that recurred measured 3 cm or larger. On follow-up imaging in the management of 24 tumors, Zagoria et al. [8] found four cases of residual tumor, and all of the tumors were larger than 3 cm. Mayo-Smith et al. [7] found that six of 32 patients had residual tumor after initial renal radiofrequency ablation. Tumors necessitating repeated treatment were significantly larger (3.5 cm) than those successfully managed with a single radiofrequency ablation session (2.4 cm) (p = 0.0031).
The relatively poor performance of radiofrequency ablation in the management of large renal masses reflects treatment before multiple-electrode radiofrequency ablation systems became available. Use of newer systems should lead to more effective management of such tumors. Evolving microwave ablation technology also may allow management of large renal tumors.
Published reports of percutaneous cryoablation experience are limited. Gupta et al. [3] reported results of CT-guided cryoablation of 27 tumors. Those authors restricted the size of tumors to 5 cm or less, the mean tumor size being 2.5 cm. An average of two cryoprobes were used, and mean ice ball diameter was 4.6 cm. Among the 16 tumors for which follow-up images were available, only one tumor had persistent enhancement suggesting the presence of residual tumor; this tumor measured 4.6 cm. There was one case of major hemorrhage, for a complication rate of 4%. The patient needed transfusion of two units of packed RBCs. Silverman et al. [6] used MRI-guided cryoablation to manage 26 tumors. Tumor size ranged from 1.0 to 4.6 cm (mean, 2.6 cm). Three tumors were ineffectively managed during the initial treatment session; two of these tumors measured 2.0 cm (the measurement of the third tumor was not provided). Repeated ablation of one of the three tumors was successful. There were two major complications, for a complication rate of 7% for the 26 initial procedures plus the one repeated procedure.
Using MRI guidance and monitoring, Shingleton and Sewell [5] were successful in single treatment sessions in the management of 21 (95%) of 22 renal tumors with a mean diameter of 3.2 cm (range, 2.8-7.0 cm). Those authors were unsuccessful in the initial treatment of a 5-cm tumor, which was successfully managed with a second cryoablation session.
Our experience with cryoablation has had an important influence on our overall tumor ablation practice. We routinely restrict renal radiofrequency ablation to tumors 3 cm or less in diameter and use cryoablation in the management of larger tumors. In addition, visualization of the ice ball with CT allows precise monitoring of ablation, which is particularly well suited to the management of central, medial, and anterior tumors. Monitoring minimizes the risk of cryoinjury to adjacent organs such as bowel and adrenal gland.
We have safely managed central tumors by cryoablation and have not seen collecting system injury. To our knowledge, no collecting system injury directly related to cryoablation has been reported in humans. In a multicenter review [20] of the complications of cryoablation, no collecting system injury was reported for 139 cryoablation procedures. Other authors [21] have found no adverse sequelae after documented cryoinjury to the collecting system during renal cryoablation. Animal studies also have not shown significant collecting system injury after direct cryoablation [22, 23].
Limitations of this study included controversy regarding tissue confirmation of renal tumor before percutaneous treatment. We know that core kidney biopsies have a 20% rate of insufficient findings for diagnosis [10] and a 20% false-negative rate [11]. In addition, as stated earlier [9], 90% of renal tumors larger than 3 cm are renal cell carcinoma. For this reason, we do not use biopsy findings to guide treatment. Other authors [12] believe that advances in cytologic technique allow accurate differentiation of benign and malignant renal tumors. Those same authors [12, 24] reiterate that negative results should be viewed with caution in the treatment of patients with a radiologically suspicious mass.
Percutaneous cryoablation of select renal masses 3 cm or larger is technically feasible, is relatively safe, and, on the basis of shortterm follow-up findings, appears to be effective in local tumor control. Although the reference standard is surgical resection, percutaneous management of these large renal masses will likely evolve into a reasonable alternative in the treatment of patients for whom the risk of surgery is too great.
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