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Vascular and Interventional Radiology |
1 From the Departments of Radiology (T.D.A., M.A.F., M.R.C., J.W.C.) and Urology (B.C.L., D.E.P., G.K.C., M.L.B.), Mayo Clinic, 200 First St SW, Rochester, MN 55905. Received December 28, 2005; revision requested February 22, 2006; revision received April 5; accepted May 10; final version accepted July 21. Address correspondence to T.D.A. (e-mail: atwell.thomas{at}mayo.edu).
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONADVANCES IN KNOWLEDGEReferences |
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Materials and Methods: This study was compliant with the Health Insurance Portability and Accountability Act and had institutional review board approval; informed consent was waived. From March 12, 2003, through August 4, 2005, 23 men and 17 women (mean age, 76 years ± 9.7 [standard deviation]; range, 53–92 years), each with a single renal tumor, underwent one percutaneous cryoablation treatment session that combined ultrasonographic (US) guidance and CT monitoring. Technical success was defined as extension of the visible ice ball 5 mm beyond the tumor margin. Local tumor progression was defined as any tumor with intralesional enhancement or a serial increase in tumor size when compared with that on images obtained immediately after ablation. Tumor characteristics, complications, and follow-up were evaluated.
Results: The maximum diameter of the 40 treated lesions ranged from 1.5 to 7.2 cm (mean, 3.4 cm ± 1.3). Twenty (50%) of 40 tumors were 3 cm or larger in diameter. Nineteen tumors (48%) extended into the renal sinus fat. One complication (2%) conformed to a grade 3 event, as determined with the Common Terminology Criteria for Adverse Events (version 3.0) of the National Cancer Institute; the overall complication rate was 8%. Thirty-eight (95%) of 40 cryoablation procedures were technically successful. Twenty-nine patients underwent follow-up (mean, 8.0 months ± 4.3; range, 1.2–18.4 months); no local tumor recurrence was found.
Conclusion: Percutaneous cryoablation with US guidance and CT monitoring is safe and effective for the treatment of solid renal tumors. Longer follow-up should provide further proof of the effectiveness of this technique.
© RSNA, 2007
With an increasing number of renal tumors discovered incidentally in the general population (1) and the uncertain clinical significance of small renal tumors (2), efforts have been directed toward the use of methods that are less invasive than radical nephrectomy for the treatment of small tumors. Alternatives include nephron-sparing surgical resection, laparoscopic partial nephrectomy, laparoscopic cryoablation, percutaneous radiofrequency (RF) ablation, and percutaneous cryoablation.
Although investigators have reported the successful treatment of solid renal tumors with percutaneous RF ablation (3–6), it has two important limitations. First, tumors larger than 3 cm in diameter require multiple precisely targeted and overlapped RF ablations. Second, the RF ablation zone cannot be monitored effectively with computed tomography (CT) or ultrasonography (US). Accurate monitoring is critical importance for the treatment of tumors in the renal pelvis, ureter, or colon. Cryoablation expands the indications for percutaneous renal ablation because larger tumors can be treated with simultaneous operation of multiple cryoprobes, and the ablation margin can be accurately monitored with CT.
On the basis of cryoablation experiences from other centers and our own intraoperative liver cryoablation experience, we incorporated this procedure into our clinical practice. The purpose of our study was to retrospectively determine the safety and effectiveness of percutaneous cryoablation, monitored with CT, for the treatment of solid renal masses.
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MATERIALS AND METHODS |
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Thirty-six (90%) patients were referred from the Department of Urology, two patients (5%) were referred from the Department of Medical Oncology and had metastatic renal cell carcinoma (RCC), one patient (2%) was referred from the Divisions of Nephrology and Hypertension and Transplantation Surgery and had previously undergone liver transplantation, and one patient (2%) was referred from the Division of Hematology and had lymphoma. Indications for cryoablation included comorbid medical conditions (21 [52%] patients, including three with metastatic RCC), previous renal surgery (10 patients [25%], including seven who had previously undergone total nephrectomy), and informed decisions to pursue ablation as an alternative to surgical resection (nine patients [22%]). Patients with metastatic RCC were treated to prevent tumor growth (and subsequent renal insufficiency or kidney loss) in a solitary kidney or to optimize response to subsequent immunotherapy (7). Cryoablation was chosen instead of RF ablation because of tumor size (22 patients), the proximity of the tumor to the ureter (11 patients) or to the bowel (four patients), or the central location of the tumor (three patients).
Tumor Characteristics
When the tumor was visible after cryoprobe placement and biopsy was deemed to be safe, percutaneous biopsy was performed with cryoablation to obtain tumor specimens for histologic analysis. One 18-gauge core from the renal mass was obtained with US guidance. We used an 18-gauge biopsy device (Bard Monopty Biopsy Instrument; CR Bard, Covington, Ga). Ablations were performed regardless of tissue findings at pathologic examination because percutaneous biopsy can be unreliable for exclusion of RCC (8,9).
Tumor size was defined as the maximum diameter measured with the imaging modality at which the tumor was most conspicuous. In the case of an irregularly shaped tumor, the largest measurement was recorded.
As previously described (3), tumors were classified as exophytic, intraparenchymal, or central, depending on their position relative to the renal parenchyma. Tumors were classified as central if they extended into the renal sinus fat, exophytic if 50% or more of the tumor circumference was outside the renal capsule, and intraparenchymal if less than 50% of the tumor circumference was outside the renal capsule.
The location of the center point of the tumor in the upper, middle, or lower third of the kidney was recorded. Tumors were also classified according to their anterior, lateral, or posterior location in the kidney.
Imaging
Cryoprobe placement was guided with use of US (Acuson Sequoia; Siemens Medical Solutions, Mountain View, Calif). A 4- or 6-MHz US transducer was typically used, although we occasionally used other transducers, depending on the tumor location.
CT monitoring during the procedure was performed with a helical scanner (HiSpeed CT/i; GE Medical Systems, Milwaukee, Wis) or an open 40-section CT system (Somatom Sensation; Siemens, Munich, Germany). Cryoprobe positions were confirmed by using 2.5–5.0-mm-thick sections with a standard CT technique (120 kVp and approximately 240 mA). CT was performed immediately after cryoablation and at 3–6 months, 12 months, 18 months, 24 months, and 36 months after ablation by using one of five multidetector CT scanners (LightSpeed Ultra or LightSpeed 16, GE Healthcare, Waukesha, Wis; Sensation 16, Sensation 40, or Sensation 64, Siemens Medical Solutions, Malvern, Pa). Examinations were performed before and after the intravenous administration of 140 mL of contrast material (Omnipaque 300; Amersham Health, Amersham, England) and included arterial (45 seconds), nephrographic (90 seconds), and excretory (300 seconds) renal phases with 2.0–2.5-mm section thickness and interval, 120 kVp, 195–350 mA, and 0.5-second rotation time.
For patients who were allergic to iodinated contrast material or those with renal insufficiency, contrast material–enhanced magnetic resonance (MR) imaging was performed within 48 hours of ablation by using a 1.5-T unit (Signa Excite with Twin-Speed technolgoy; GE Healthcare, Waukesha, Wis). The renal MR examination consisted of a three-plane localizer image acquired by using a single-shot fast spin-echo or a fast spoiled gradient-echo sequence. This examination was followed by coronal single-shot fast spin-echo imaging (echo time, 80 msec; 83-kHz bandwidth; 110° flip angle; 256 x 256 matrix; 0.5 signal acquired; 44-cm field of view [FOV]; and 5-mm section thickness with a 1-mm gap). Transverse in-phase and opposed-phase spoiled gradient-echo images were obtained and included the adrenal glands and kidneys (repetition time msec/echo time msec, 100–200/2.1, 4.2; 70° flip angle; 32-kHz bandwidth; 256 x 192 matrix; one signal acquired; and 6-mm section thickness with a 1-mm gap). Respiratory-triggered fast spin-echo T2-weighted images were obtained (two R-R intervals/85; echo train length, 12; 32-kHz bandwidth; 256 x 224 matrix; two signals acquired; and 5–6-mm section thickness with a 1-mm gap). Dynamic fat-saturated three-dimensional fast spoiled gradient-echo images were obtained before and after contrast material administration (3.4/1.6, 0.75 signal acquired, 83-kHz bandwidth, 15° flip angle, 256 x 224 matrix, and 3–4-mm section thickness). Fifty to sixty sections were acquired with zero filling to obtain a 512 x 512 in-plane matrix with 50% overlapping sections along the z-axis. Parallel imaging with an acceleration factor of 1.8 in the phase-encoding direction was performed by using a proprietary array spatial sensitivity encoding technique (Asset; GE Healthcare). A transverse low-spatial-resolution fast spoiled gradient-echo calibration image was obtained before the parallel images were acquired. Gadodiamide (Omniscan; Amersham Health) was injected intravenously at a rate of 3 mL/sec (final concentration, 0.1 mmol/kg). A test bolus of contrast material (2 mL) was injected before contrast-enhanced three-dimensional images were recorded to help determine the appropriate image delay for achieving an optimal set of arterial phase images. A second set of contrast-enhanced images was obtained approximately 10 seconds after arterial phase images were obtained. A third set of images was obtained approximately 2 minutes after the second set was complete. Last, a transverse fat-saturated two-dimensional spoiled gradient-echo sequence was performed (100–200/2.6; 70° flip angle; 32-kHz bandwidth; 256 x 192 matrix; 0.75 phase FOV; 32–40-cm FOV; 6-mm section thickness with a 1-mm gap). The FOV for all transverse sequences was adjusted according to patient size and typically ranged from 34 to 44 cm. The phase FOV was 0.70–1.0.
Postablation CT and MR images were examined by several individuals (T.D.A., M.A.F., M.R.C., and J.W.C.) to determine the extent of ablation and evaluate possible complications.
Treatment Procedure
Ablations were performed by four experienced interventional radiologists (T.D.A., M.A.F., M.R.C., and J.W.C., with 4, 5, 4, and 24 years of experience, respectively). After informed consent had been obtained, ablations were performed in the CT suite, and patients received a general anesthetic. The use of general anesthesia enables greater control of respiration during cryoprobe placement and maximizes patient tolerance of the procedure. The cryoablation system (Cryocare; Endocare, Irvine, Calif) that we used enables independent and simultaneous operation of as many as eight cryoprobes. The cryoprobe (Perc-24; Endocare) is a sealed 2.4-mm-diameter (13-gauge or 7.2-F) needle that, according to the manufacturer, generates an ice ball up to 3.7 cm in diameter and up to 5.7 cm in length along the probe shaft. The rapid expansion of argon gas in a sealed cryoprobe with a distal uninsulated portion results in rapid freezing of tissue, and temperatures can reach –100°C within seconds (10). The diameter of the ice ball is controlled by the rate of gas delivery to the probe. Thawing is achieved by replacing the argon gas with helium gas.
We placed cryoprobes into the tumor before we performed biopsy because bleeding after the biopsy procedure may obscure the tumor and make cryoprobe placement difficult or impossible. One or more sterile cryoprobes were introduced through a nick in the skin by one or more of the participating radiologists (T.D.A., M.A.F., M.R.C., and J.W.C.). With US guidance, cryoprobes were advanced into the tumor with the goal of placing the probes 1–2 cm apart for complete tumor coverage. Cryoprobe positions were determined according to tumor geometry and expected ice ball size. CT was used to verify placement of the multiple cryoprobes. After the cryoprobe positions were confirmed to be accurate and before freezing, biopsy of the targeted kidney mass was usually performed. With some patients, a biopsy could not be performed because the tumor was obscured by the cryoprobes.
Each lesion received a single treatment cycle of freezing, thawing (5 minutes), and refreezing. The duration of the freezing time was based on growth of the ice ball relative to the tumor. Limited unenhanced CT scans were obtained approximately every 2 minutes during the freezing portions of the cycle by using body window width and window level settings of 400 HU and 40 HU, respectively, and 2.5–5.0-mm collimation to monitor growth of the ice ball (Fig 1). Coronal reconstructed images were generated according to the proximity of other critical structures (eg, ureter, bowel, adrenal gland). CT was used to accurately monitor ice ball size and location and help predict subsequent cell death (11,12). Because complete cell death occurs approximately 3 mm inside the edge of the ice ball (13,14), the goal was to extend the ice ball 5 mm beyond the tumor margin during both freezing portions of the cycle. After the final freeze of the cycle, cryoprobes were actively warmed with helium gas and withdrawn when the temperature was higher than 20°C.
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Postablation Imaging Assessment
Patients underwent CT or MR imaging (as described earlier) within 48 hours after the ablation procedure, and images were reviewed by the radiologist who performed cryoablation. Initial technical success was defined as an ablation that produced a volume of tissue with no contrast enhancement in the area encompassing the original tumor.
Continued follow-up at our recommended 3–6-month intervals included CT or MR imaging performed before and after the intravenous administration of contrast agent by using the techniques described earlier, and images were reviewed by one of the four radiologists who performed ablation. Local tumor progression was diagnosed when a tumor showed intralesional enhancement or a serial increase in size when compared with that on images from the immediate follow-up examination. A biopsy was not performed as part of routine follow-up.
Complications
Clinically important complications were defined by using the Common Terminology Criteria for Adverse Events (CTCAE) (version 3.0) of the National Cancer Institute (15). Complications with a grade of 3 or higher were recorded.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONADVANCES IN KNOWLEDGEReferences |
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Twenty-nine (72%) of 40 patients underwent percutaneous biopsy immediately before cryoablation. Biopsy was not performed in the remaining 11 (28%) patients because visualization of the targeted tumor was limited owing to cryoprobes, adjacent hemorrhage, or both. Results of biopsy in 29 patients indicated that 17 (59%) had RCC, three (10%) had oncocytic neoplasm, and five (17%) had oncocytoma. Findings were nondiagnostic in four (14%) of 29 patients. Three (7%) patients had undergone biopsy of the kidney mass before the ablation procedure; two biopsy specimens were positive for RCC, and one specimen showed an oncocytic neoplasm. One patient (2%) underwent biopsy of a vertebral body on the day before the ablation procedure; results were positive for metastatic RCC. In seven (18%) of 40 patients, no histologic diagnosis was made; previously, a contrast-enhanced mass was shown at MR imaging or CT and/or a solid mass was shown at US.
Complications
With use of the CTCAE (15), only one (2%) complication occurred in the 40 procedures that corresponded to a grade 3 or higher complication; it was a grade 3 adverse event. The patient had a 7.2-cm-diameter tumor in the right kidney that required treatment with seven cryoprobes. A large perinephric hemorrhage with hypotension occurred immediately after the cryoablation procedure. Subsequent emergent angiography failed to show a source of bleeding. The patient was hospitalized for 10 days and required multiple blood transfusions. During hospitalization, the patient had a myocardial infarction and transient acute renal failure, with a peak serum creatinine level of 4.3 mg/dL (380 µmol/L). At discharge from the hospital, the serum creatinine level was 2.0 mg/dL (177 µmol/L); the creatinine level before ablation was 2.3 mg/dL (203 µmol/L).
Two patients had complications that did not meet or exceed a grade 3 event according to the CTCAE. One patient had a large perinephric hemorrhage after percutaneous cryoablation of a 6.7-cm mass in the right kidney that required treatment with six cryoprobes. The patient's hemoglobin level decreased from 14.0 g/dL (140 g/L) before ablation to 11.1 g/dL (111 g/L) 24 hours after the procedure. The patient was hospitalized for an additional day but did not require transfusion, embolization, or other intervention. The third complication occurred in a patient with preexisting labile hypertension that required treatment with four medications. During the cryoablation procedure, the patient had a hypertensive crisis (blood pressure was as high as 264/94 mm Hg). Pulmonary edema also developed, and oxygen supplementation, but not intubation, was required. The patient was hospitalized for another 3 days and discharged in good condition. Thus, our overall complication rate was 8% (three of 40 patients).
Serum Creatinine Level
Serum creatinine levels before and after cryoablation were known for 33 (82%) patients. The mean change in serum creatinine levels after ablation ranged from –0.2 to 2.0 mg/dL (–18 to 177 µmol/L)(mean, 0.1 mg/dL [9 µmol/L]). No patient required dialysis after ablation.
Follow-up
Twenty-nine (76%) of 38 patients in whom ablation was technically successful underwent contrast-enhanced CT or MR imaging during follow-up. The mean follow-up was 8.0 months ± 4.4 (range, 1.2–18.4 months). No local recurrences were identified. Follow-up data for these 29 patients included 15 central tumors imaged at a mean follow-up of 6.9 months ± 4.0 (range, 1.2–15.8 months) and 13 tumors with a diameter of 3 cm or larger, imaged at a mean follow-up of 8.9 months ± 4.5 (range, 2.8–17.5 months). Two of 29 patients died; one died of metastatic RCC (7 months after ablation), and another died of small-bowel obstruction 12 months after ablation. Neither patient had evidence of a locally recurrent tumor at the time of death. Thus, the tumor control rate for the 29 patients was 100%.
No appropriate follow-up images were available for 10 (26%) of 38 patients in whom ablation was technically successful. Three patients underwent unenhanced CT because of renal failure or allergy to contrast material or both; these examinations showed a decrease in the size of the treated tumor, and such a decrease is suggestive of successful tumor control. Three patients were lost to follow-up. One patient died of pulmonary fibrosis before follow-up images could be obtained. Three patients recently underwent ablation, and follow-up is pending.
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONADVANCES IN KNOWLEDGEReferences |
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Our 95% technical success rate and 100% tumor control rate for patients who underwent follow-up CT or MR imaging compare favorably with rates from other percutaneous cryoablation studies. Silverman et al (18) were technically successful in the MR imaging–guided cryoablation of 24 (92%) of 26 renal tumors and noted a single recurrence of tumor at 6 months (4.2%). Shingleton and Sewell (19) treated 22 tumors (20 patients) with MR imaging–guided cryoablation. With a mean follow-up of 9 months, there was one recurrence (4.5%) 3 months after cryoablation; repeat treatment was successful.
Gill and colleagues (17) recently reported 3 years of follow-up data for 56 patients who underwent laparoscopic renal cryoablation. Locally recurrent and/or persistent cancer was documented in two (3.6%) patients. Investigators in two studies (16,20) of intraoperative cryoablation of small solid renal tumors reported successful treatment of 53 patients (success rate, 100%).
Percutaneous cryoablation, compared with RF ablation, has three important advantages in the treatment of certain renal tumors. First and probably most important, CT can help accurately monitor the cryoablation procedure and supplies three-dimensional views of the ice ball as it develops (11,21). The size of the ice ball, as visualized with CT, allows the extent of cell death to be determined because uniform cell necrosis occurs 3 mm inside the edge of the ice ball (13,14). Monitoring also can be performed with MR imaging, but prolonged time with an MR unit (3–4 hours) (18) and MR imaging–compatible ablation equipment is required. In addition, considerable anesthetic control of patient breathing must be attained to allow for nearly 60 seconds of breath-holding during image acquisition (18).
Second, multiple cryoprobes can be used simultaneously in the treatment of large tumors. Unlike RF ablation, in which treatment of tumors larger than 3 cm in diameter is difficult (4,6,22,23), cryoablation has enabled the successful generation of ablation zones larger than 8 cm in diameter. Of note, the mean tumor size in our series of patients was 3.4 cm, which is larger than the sizes reported in recent RF ablation studies (3,4,6,22–24).
Third, direct monitoring of the cryoablation procedure with CT allows the treatment of tumors in critical locations, such as adjacent to the renal pelvis, ureter, or bowel. The probe-specific control of the cryoablation system permits regulation of individual cryoprobes to slow or stop the freezing process if the growing ice ball approaches a vital structure. Tumors in anterior, lateral, or posterior locations of the kidney can be treated percutaneously. Vital adjacent structures can be manipulated from the ablation site with both RF and cryoablation techniques. When necessary, water can be percutaneously injected to shift critical structures away from the area being treated (25).
Percutaneous cryoablation has two advantages over the laparoscopic approach. Most important, the ablation zone can be carefully monitored with intermittent CT, as described earlier. With intraoperative cryoablation, US guidance is used, and the acoustic shadow of the ice ball precludes the imaging of deep tissues. As a result, only the leading edge of the ice ball is seen. Depending on the degree of tumor exposure during surgery and the ability to capture images from different perspectives, the extent of ablation in some patients may be estimated only on the basis of the diameter of the ice ball (12).
In general, percutaneous cryoablation is less invasive than the corresponding laparoscopic method (26). Probes are inserted percutaneously, and the procedure frequently does not require manipulation of intraabdominal contents. The patient leaves the CT suite with a small bandage over the puncture site or sites. Although we and others (18) prefer to use general anesthesia during the procedure for respiratory control and general patient comfort, percutaneous cryoablation can also be performed with the patient receiving conscious sedation (27). After percutaneous or laparoscopic cryoablation, the patient usually spends a night in the hospital and is discharged the next day with a prescription for nonnarcotic pain medication to be administered as needed.
There are two inherent limitations of percutaneous cryoablation compared with the laparoscopic method. First, potential bleeding cannot be controlled directly during percutaneous cryoablation without intraarterial access and fluoroscopy. Indeed, angiography was performed in one of our patients to further evaluate hemorrhage, although embolization was not required. In contrast, bleeding may be controlled directly during laparoscopic surgery. This advantage must be viewed in the context of the higher risks associated with a more invasive procedure; researchers in a multi-institutional review (28) found that three (37.5%) of eight laparoscopic ablation complications were attributable to the surgical technique, not to the ablation itself.
A second limitation of percutaneous cryoablation is the treatment of renal tumors in the inferior pole of the kidney, adjacent to the ureter. These tumors are difficult to treat percutaneously because the kidney and ureter are fixed within the Gerota fascia, and hydrodisplacement is limited; such tumors are ideally suited for laparoscopic cryoablation.
When we used the CTCAE specifications, we had a clinically important complication rate of 2%. This is comparable to the 7.4% complication rate (two of 27 procedures) achieved by Silverman et al (18), who treated tumors with a range in diameter of 1.0–4.6 cm (mean, 2.6 cm), and the 4.8% complication rate (one of 21 procedures) achieved by Shingleton and Sewell (19), who treated tumors with a range in diameter of 1.8–7.0 cm (mean, 3.2 cm). Our complication rate was also within the range of 0%–5.6% that was reported in the percutaneous RF ablation literature (3,4,6,23,29). The hemorrhagic complications in our series involved the largest tumors that were treated; the tumors were 6.7 and 7.2 cm in diameter and required six and seven cryoprobes, respectively. It is possible that for the treatment of larger tumors, which require a greater number of cryoprobes, there may be an increased risk of bleeding. Our overall complication rate was 8% (three of 40 patients).
It is interesting that Shingleton and Sewell (19) used an introducer sheath during percutaneous cryoablation in their study. After the ablation, the cryoprobe tract was packed with pledgets to facilitate hemostasis. No bleeding complications occurred in their series, which included one tumor larger than 5 cm in diameter. This method of tract control in the ablation of larger tumors warrants further investigation.
An important limitation of this study concerns the conundrum of differentiation between technical failure and local tumor progression. We chose to define technical success as the extension of the ice ball 5 mm beyond the tumor margin during the ablation procedure. Such technical success may be seen only in retrospect by observing the location of enhancement on follow-up images. At short-term follow-up (
6 months), marginal enhancement of the ablation site is equivalent to suboptimal marginal treatment (ie, technical failure), whereas central enhancement or tumor enlargement is indicative of true local progression of tumor. Regardless, a patient with a viable tumor warrants further treatment consideration.
An additional limitation of this study is our decision to treat tumors irrespective of biopsy findings. Core kidney biopsy has a nondiagnostic rate of 20% (8) and a 20% false-negative rate (9). Because we do not want to neglect a pathologically occult malignancy, we do not allow results of the kidney biopsy to be used for guiding treatment.
In conclusion, percutaneous cryoablation with US guidance and CT monitoring appears to be safe and effective for the treatment of solid renal masses. Compared with percutaneous RF ablation, cryoablation can be used to treat larger tumors and tumors in critical locations. More long-term follow-up studies will be needed to further substantiate the effectiveness of this treatment.
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ADVANCES IN KNOWLEDGE |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONADVANCES IN KNOWLEDGEReferences |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Abbreviations: CTCAE = Common Terminology Criteria for Adverse Events • FOV = field of view • RCC = renal cell carcinoma • RF = radiofrequency
Authors stated no financial relationship to disclose.
Author contributions: Guarantors of integrity of entire study, T.D.A., M.A.F.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, T.D.A., M.A.F., M.R.C.; clinical studies, T.D.A., M.R.C., J.W.C., D.E.P.; statistical analysis, T.D.A.; and manuscript editing, all authors
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This article has been cited by other articles:
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  R. N. Uppot, S. G. Silverman, R. J. Zagoria, K. Tuncali, D. D. Childs, and D. A. Gervais Imaging-Guided Percutaneous Ablation of Renal Cell Carcinoma: A Primer of How We Do It Am. J. Roentgenol., June 1, 2009; 192(6): 1558 - 1570. [Abstract] [Full Text] [PDF]
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J. L. Hinshaw, A. M. Shadid, S. Y. Nakada, S. P. Hedican, T. C. Winter III, and F. T. Lee Jr. Comparison of Percutaneous and Laparoscopic Cryoablation for the Treatment of Solid Renal Masses Am. J. Roentgenol., October 1, 2008; 191(4): 1159 - 1168. [Abstract] [Full Text] [PDF]
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