Imaging-Guided Radiofrequency Ablation of Cystic Renal Neoplasms

Transcription

1 Vascular and Interventional Radiology Original Research Allen et al. Radiofrequency Ablation of Cystic Renal Neoplasms Vascular and Interventional Radiology Original Research Brian C. Allen 1 Michael Y. Chen David D. Childs Ronald J. Zagoria Allen BC, Chen MY, Childs DD, Zagoria RJ Keywords: ablation, Bosniak, cystic renal cell carcinoma, radiofrequency ablation DOI: /AJR Received June 1, 2012; accepted after revision July 20, All authors: Department of Radiology, Wake Forest Baptist Medical Center, Medical Center Blvd, 3rd Fl MRI, Winston-Salem, NC Address correspondence to B. C. Allen (bcallen2@wakehealth.edu). AJR 2013; 200: X/13/ American Roentgen Ray Society Imaging-Guided Radiofrequency Ablation of Cystic Renal Neoplasms OBJECTIVE. The purpose of this article is to determine whether percutaneous radiofrequency ablation (RFA) is effective and safe for the treatment of cystic renal neoplasms. MATERIALS AND METHODS. This is a retrospective review of imaging-guided RFA of Bosniak III and IV cysts from one institution. Thirty-eight subjects (19 men and 19 women; mean age, 71 years; age range, years) underwent RFA of 40 cystic neoplasms (Bosniak III, n = 25; Bosniak IV, n = 15). Percutaneous biopsy was performed in 90% (36/40) of lesions. For patients with imaging follow-up of at least 1 year (n = 21), the mean duration of surveillance was 2.8 years (range, years). The electronic medical record was reviewed for complications related to the procedure. Estimated glomerular filtration rate (GFR) was measured before RFA and at the last follow-up visit more than 6 months after the RFA session. RESULTS. According to percutaneous biopsy, 61.1% (22/36) of lesions were malignant, and 38.9% (14/36) of biopsies were inconclusive. There was no local tumor progression, and no subjects developed metastatic disease. One subject developed a new solid renal mass during the course of follow-up. Minor complications occurred in 5.3% (2/38) of ablations and included dysuria and mild hydronephrosis related to a blood clot in the ureter. There was one major complication (2.6%), a case of flash pulmonary edema. On average, estimated GFR decreased by 2.5 ml/min/1.73 m 2. CONCLUSION. Imaging-guided RFA is an effective and safe treatment of Bosniak III and IV cystic renal neoplasms with outcomes comparable to those of surgical therapies. C ystic renal lesions are common and are often identified as incidental findings on cross-sectional imaging performed for other reasons. The Bosniak classification was first introduced in 1986 and uses imaging features to stratify cystic renal lesions into categories with increasing risk of malignancy [1]. Briefly, slightly more than 50% of Bosniak III lesions are malignant and contain thickened walls or septations in which measureable enhancement is present [2 6]. Most Bosniak IV cystic lesions are malignant and contain enhancing soft-tissue components separate from the septations [1, 6]. Percutaneous radiofrequency ablation (RFA) is an accepted minimally invasive treatment of small solid renal neoplasms in patients who are poor operative candidates. Short, intermediate, and available long-term oncologic efficacies of RFA are comparable to those of surgical series [7 10]. The current standard of care for the treatment of Bosniak III and IV renal cysts is operative [7 10]. Very few data regarding thermal ablation of Bos- niak cysts are available in the literature. A single study suggested that thermal ablation was effective in the treatment of Bosniak III and IV cystic renal tumors [11]. The purpose of this work is to evaluate the efficacy of percutaneous RFA for the treatment of complex cystic renal masses. To the best of our knowledge, this is the largest series of patients with Bosniak III and IV renal cysts that have been treated with percutaneous RFA. Materials and Methods Our institutional review board approved this retrospective study, which was compliant with the HIPAA guidelines. A waiver of informed consent was obtained. Patient Population The radiology information system (RIS) was searched for all patients treated with percutaneous RFA from February 2002 until December 2011, resulting in a total of 558 subjects. The electronic medical record (EMR) and the RIS were then searched for subjects treated for Bosniak III and IV cystic renal neoplasms. The final study population consisted of AJR:200, June

2 Allen et al. TABLE 1: Demographic Data and Tumor Characteristics Characteristic 38 subjects (19 men and 19 women) with a mean age of 71 years (range, years). Subjects underwent percutaneous RFA of 40 cysts; 25 were prospectively classified as Bosniak III and 15 were Bosniak IV. The baseline characteristics are tabulated in Table 1. Value Patient demographics (n = 38) Age at treatment (y), mean (range) 71 (46 95) Sex Male 19 (50) Female 19 (50) Race White 31 (82) African American 7 (18) Comorbidities 26 (68) Congestive heart failure 14 (37) Emphysema 4 (11) Combined cardiopulmonary 8 (21) Previous malignancy 16 (42) Renal cell carcinoma 2 (5) Transitional cell carcinoma 1 (3) Lung carcinoma 2 (5) Breast carcinoma 3 (8) Melanoma 3 (8) Lymphoma 2 (5) Colorectal carcinoma 1 (3) Thyroid carcinoma 1 (3) Uterine carcinoma 1 (3) Baseline renal function, estimated GFR (ml/min/1.73 m 2 ) > (58) (39) < 30 1 (3) Tumor characteristics (n = 40) Bosniak classification III 25 (62.5) IV 15 (37.5) Tumor size (cm) Mean (range) 2.3 ( ) < 2 16 (40) (35) > 3 10 (25) Pathologic diagnosis 36 (90) Renal cell carcinoma 22 (61.1) Inconclusive or nondiagnostic 14 (38.9) Note Except where noted otherwise, data are no. (%) of patients or tumors. GFR = glomerular filtration rate. Pretreatment Evaluation All subjects were evaluated and referred by a urologist before RFA and were considered to be at increased risk for developing complications during or after renal surgery because of comorbidities. The pretreatment evaluation for all subjects included abdominal imaging with CT or MRI before and after the IV administration of contrast material, thoracic imaging with a chest radiograph or CT, and routine laboratory studies including coagulation studies and estimated glomerular filtration rate (GFR). CT was performed using MDCT scanners, primarily a 16-MDCT scanner (LightSpeed 16, GE Healthcare). Our renal CT protocol included unenhanced imaging of the kidneys. Then, after the IV administration of 125 ml of iohexol (350 mg I/ ml; Omnipaque 350, GE Healthcare), corticomedullary and nephrographic phase imaging was performed at approximately 60 and 120 seconds after contrast administration, respectively. MRI was performed on a 1.5-T MRI unit (Signa, GE Healthcare). Our protocol included axial fat-suppressed 3D gradient-echo T1-weighted imaging before and after the IV administration of 0.1 mmol/kg body weight of gadobenate dimeglumine (MultiHance, Bracco Imaging) at a rate of 2 ml/s followed by a saline bolus of 20 ml at 2 ml/s. Dynamic images in the corticomedullary and nephrographic phases were obtained in the axial plane. Coronal images in the nephrographic and delayed phase were also obtained. Subtraction datasets were created and reviewed to assess for enhancement. Comorbidities precluding surgery included hypertension and congestive heart failure (n = 14), emphysema (n = 4), and cardiac and pulmonary disease (n = 8). Two subjects had previously treated renal cell carcinoma, and 14 subjects had another primary neoplasm (Table 1). RFA Technique In patients with lesions in close proximity to the ureter, an end-hole ureteric stent was placed immediately before RFA. One subject had a stent placed before ablation. The ureteric stent was perfused with chilled sterile water and 5% dextrose solution during the RFA to cool the ureter and pelvicalyceal system. Hydrodissection was not required in any patient in this series. All patients were given conscious sedation with continuous monitoring of vital signs and local anesthesia at the puncture site. Typically, at least one neoplasm in each patient was biopsied immediately before the ablation procedure using CT guidance with a cytotechnologist on site. All neoplasms were ablated on the basis of preprocedural imaging, because a final pathologic diagnosis was not available at the time of the procedure. If the final pathologic diagnosis was benign, a single follow-up renal CT or MRI was performed to assess for complications. Using a coaxial technique, a combination of fine-needle aspirates and core biopsies were obtained through a 19-gauge introducer needle. Using the preprocedure imaging that was performed with IV contrast agent, 1366 AJR:200, June 2013

3 Radiofrequency Ablation of Cystic Renal Neoplasms septations and nodular components were targeted for biopsy. The cysts were not aspirated before or after biopsy. Inadvertent spillage of cyst contents into the retroperitoneum was not noted to occur after biopsy. Typically, all neoplasms in a single kidney were treated in a single session. For subjects with neoplasms in both kidneys, different sessions were used for each kidney. In the two patients who had two neoplasms ablated in this investigation, both Bosniak cysts were located in the same kidney and were ablated during the same procedure. Nearly all patients were treated in the prone position. The ablation technique adhered to in this study has been previously reported for the treatment of solid renal masses [12]. Using CT guidance, RFA was completed with a 200-Watt generator system using the impedance control setting and saline-cooled treatment probes (Cool-tip, Covidien). Overlapping ablations were performed according to tumor size and shape, with the intent to destroy the entire mass and at least a 5-mm margin of surrounding normal A C renal parenchyma (Fig. 1). Ablations were continued for 8 minutes unless the generator, because of a rapid increase in tissue impedance, automatically switched to energy pulsing twice. When this occurred, ablation was continued until the next even minute after a minimum of 4 minutes. Tissue temperature was recorded after each ablation and, if it was below 50 C, another ablation in the same location was performed. A contrast-enhanced (if estimated GFR > 45 ml/min/1.73 m 2 ; n = 35 subjects) or unenhanced (if estimated GFR < 45 ml/ min/1.73 m 2 ; n = 3 subjects) CT scan was obtained before terminating the ablation session to assess for the adequacy of tumor ablation and immediate complications. Recognition of continued contrast enhancement within the neoplasm was interpreted as incomplete tumor ablation, and an additional tumor ablation was performed with the intent of destroying the remaining viable tumor. If IV contrast agent was not administered, unenhanced images were reviewed to ensure adequate coverage of the neoplasm. Fig year-old woman with Bosniak III cyst. A, IV contrast agent enhanced preablation axial CT through upper pole of right kidney shows cystic lesion (arrow) with thickened septations and measureable enhancement. B, Postablation contrast-enhanced CT, with patient prone, shows complete ablation of cystic lesion (arrow) and no measurable enhancement within ablation zone. C, Approximately 1 year after ablation, T1-weighted fat-suppressed contrastenhanced MRI (TR/TE, 4.184/2.008) obtained after IV administration of 16 ml of gadobenate dimeglumine shows ablation changes (arrow) in upper pole of right kidney, without residual enhancement to suggest recurrent neoplasm. After completion of the procedure, patients were transferred to a short stay area in the hospital, where their vital signs were monitored hourly; antiemetics and analgesics were administered on an as-needed basis. Patients were discharged if they had no signs of complication with stable vital signs, no evidence of active bleeding (e.g., stable blood pressure, heart rate, hematocrit, and hemoglobin level), and no pain requiring IV analgesics. Preprocedure Imaging Analysis Analysis of the data included review of pretreatment, treatment, and follow-up scans for each treated tumor. A board-certified fellowship-trained abdominal imager with 1 year of experience measured the preprocedural diameter of each treated neoplasm on a PACS, using electronic calipers on the axial image showing the greatest diameter. Location of the tumor was classified by dividing the craniocaudal length of the kidney into upper, middle, and lower thirds. The tumor location was categorized as being B AJR:200, June

4 Allen et al. exophytic (> 25% of tumor circumference contacting the perirenal fat) or nonexophytic. All neoplasms were prospectively evaluated and characterized by a board-certified abdominal imager at the time of image acquisition and were classified as either a Bosniak III or IV cyst. Twenty-one tumors (52.5%) were located in the right kidney, and 19 tumors (47.5%) were in the left kidney. Sixteen (40%) tumors were in the upper pole, 16 (40%) were interpolar, and eight (20%) were lower pole tumors. Seventy-five percent (30/40) of the tumors were classified as exophytic, and 25% (10/40) of the tumors were nonexophytic. Overall tumor size ranged from 1.0 to 4.2 cm (mean tumor size, 2.3 cm). Forty percent (16/40) of tumors were 2 cm or smaller in diameter, 35% (14/40) of tumors measured 2 3 cm in diameter, and 25% (10/40) of tumors were greater than 3 cm in diameter (Table 1). Postprocedure Imaging Analysis Using the RIS and the EMR, reports from follow-up CT and MRI examinations were reviewed. All dictated reports were reviewed by a board-certified fellowship-trained abdominal imager at the time of imaging acquisition. The presence of local tumor progression, metachronous renal neoplasia, and metastatic disease was recorded. Safety Analysis Using the EMR and reviewing postprocedural clinic visits, emergency department visits and imaging studies, all complications attributable to the RFA procedure were recorded. Complications were graded using the Society of Interventional Radiology (SIR) Classification System for Complications by Outcome [13]. Class A and B complications were considered as minor, and class C or higher complications were considered as major. Renal Function Analysis The abbreviated Modified Diet for Renal Disease equation was used to estimate GFR [14]. Global renal function was classified using the Kidney Disease Outcome Quality Initiative classification of chronic renal disease, with estimated GFR greater than 60 ml/min/1.73 m 2 classified as normal or mild reduction, ml/min/1.73 m 2 as moderate reduction, ml/min/1.73 m 2 as severe reduction, and less than 15 ml/min/1.73 m 2 as renal failure [15]. Renal function (i.e., estimated GFR) was measured before percutaneous RFA, 1 6 months after each RFA session, and at the last follow-up visit, which was more than 6 months after the last RFA session, to evaluate the short- and long-term effects on renal function. Of the 38 subjects, 22 had a baseline estimated GFR of greater than 60 ml/min/1.73 m 2, 15 had a baseline estimated GFR of ml/min/1.73 m 2, and one had an estimated GFR of less than 30 ml/ min/1.73 m 2 (Table 1). Statistical Analysis Results were initially analyzed using descriptive statistics. The paired Student t test was used to evaluate the significance of the short- and long-term effect on renal function of RFA as compared with the baseline. All statistical analyses were performed using StatView software (version 4.5, Abacus Concepts). Results Percutaneous Biopsy Percutaneous biopsy was performed in 90% (36/40) of lesions. According to results of percutaneous biopsy, 61.1% (22/36) of lesions were malignant, 38.9% (14/36) of biopsies were inconclusive, and no lesions were definitively benign. Of the 21 Bosniak III lesions that were biopsied, 57% were malignant (12/21) and 42.9% (9/21) were indeterminate or nondiagnostic. Of the 15 Bosniak IV lesions that were biopsied, 67% (10/15) were malignant and 33% (5/15) were indeterminate or nondiagnostic. Efficacy Technical success for percutaneous RFA of cystic renal masses was 100%; all 40 Bosniak cysts were adequately treated, according to immediate postprocedural imaging. Thirty-one subjects (81.6%) had at least one locally performed follow-up examination. No residual disease was suspected on postablation or follow-up imaging; the primary treatment effectiveness was 100% (32/32 neoplasms). In subjects with at least 1 year of imaging surveillance (n = 21), there was no local tumor progression and no subjects developed metastatic disease, with an average follow-up of 2.82 years (range, years; median, 2.9 years). One subject developed a new solid renal mass during the course of follow-up, which has not yet been treated. Safety Minor complications (SIR class A) occurred in 5.3% (2/38) of subjects and included dysuria and mild hydronephrosis related to a blood clot in the ureter; these complications did not require treatment. There was one (2.6%) major complication (SIR class C), a case of flash pulmonary edema that required transfer to the emergency department for further treatment. Renal Function Results Longer than 6-month follow-up estimated GFR data were available for 24 subjects. On average, estimated GFR decreased by 2.5 ml/min/1.73 m 2. In 50% (12/24) of subjects, estimated GFR increased, stayed the same, or decreased by less than 10%. Estimated GFR decreased by 10 29% in 25% (6/24) of subjects and by greater than 30% in 25% (6/24) of subjects. There was no difference in tumor size, location, Bosniak classification, or baseline estimated GFR between subjects with no decline in renal function and those with more severe decline in renal function. Discussion Slightly more than 50% of Bosniak III cystic lesions and most Bosniak IV cystic lesions are malignant [3, 5, 6]. There are data suggesting that active surveillance for patients with small solid renal neoplasms and Bosniak III and IV cysts is a reasonable management option in patients who have medical comorbidities or a short life expectancy [5, 16, 17]. However, there are no prospective studies available, and the current standard of care for both Bosniak III and IV lesions is surgical [6]. Although thermal ablation is an accepted therapy for the treatment of solid renal lesions in patients who are poor surgical candidates, there are very few data regarding the treatment of complex cysts with percutaneous RFA [11]. The purpose of this work is to evaluate the efficacy of percutaneous RFA for the treatment of Bosniak III and IV cystic lesions. There is a concern regarding cyst puncture and spillage of cyst contents leading to tumor seeding in the retroperitoneum, because tract seeding has occurred after percutaneous biopsy of solid renal neoplasms [4, 18 20]. In this series, both fine-needle aspirates and core biopsies were performed using coaxial technique, but the cysts were not aspirated, nor were the ablation tracts ablated at the conclusion of the procedure. There were no cases of retroperitoneal or tract seeding. Other investigators have anecdotally aspirated complex cysts or have injected a sclerosant to solidify lesions before ablation, to prevent spillage of cyst contents and retroperitoneal seeding. Currently, there is no proven method for the periablational management of complex renal cysts because very little has been written in the literature. The current study suggests that no additional maneuvers are needed to safely ablate cystic renal tumors. Given the lack of retroperitoneal seeding in our investigation, this complication is likely a rare occurrence. According to results of percutaneous biopsy, just over half of the Bosniak III cysts were proven malignant, which is concordant with the available literature [3, 5, 6, 21]. However, none of the Bosniak III lesions could be confirmed as benign, limiting the utility of a negative biopsy result. Only 67% of the Bosniak IV cysts were proven malignant; the remaining samples were nondiagnostic. Because a large number of cystic tumor biopsies were 1368 AJR:200, June 2013

5 Radiofrequency Ablation of Cystic Renal Neoplasms nondiagnostic and because a definitive diagnosis of a benign lesion was uncommon in this series, the decision to ablate was based on preprocedural imaging. If a benign diagnosis could be made reliably and routinely, biopsy and ablation could occur on different dates, making ablation unnecessary in the setting of a benign lesion. With an average follow-up of 2.82 years, there was no local progression. The rate of untreated neoplasm and local tumor progression for percutaneous RFA of cystic renal neoplasms in this series compares to that seen in percutaneous RFA of small solid renal neoplasms [7, 12, 22, 23]. Because longterm results are limited, active surveillance is required, as it is after the ablation of solid renal neoplasms, to identify both local tumor progression and new renal neoplasms [24]. The safety and renal function results are similar to those seen with percutaneous RFA of solid renal neoplasms. A meta-analysis of percutaneous thermal ablation of solid renal neoplasms found a major complication rate of 3% [25]. The one major complication in this series was a case of flash pulmonary edema, which required transfer of the patient to the emergency department. On average, estimated GFR decreased by 2.5 ml/min/1.73 m 2 in this series of patients, which was not statistically significant. Previous work has shown that a single application of percutaneous RFA does not significantly affect estimated GFR [26]. This also compares favorably to the reported 10 13% decrease in estimated GFR after partial nephrectomy for solitary renal tumors [27, 28]. A number of our subjects had more significant reductions in estimated GFR. There was no difference in tumor size, Bosniak classification, tumor location, or baseline estimated GFR between subjects with no decline in renal function and those with more severe decline in renal function. Because the subject population is small and long-term follow-up is not available, the actual cause of the decline in renal function is unknown. There are limitations to this study. Although this is the largest, to our knowledge, series of Bosniak III and IV cysts treated with RFA, percutaneous therapy for cystic renal neoplasms remains rare, both at our institution and within the literature. Although the initial findings are favorable, the small number of patients and the lack of long-term follow-up limit recommendations regarding the treatment of cystic renal neoplasms in all patients. However, thermal ablation may be a reasonable alternative to active surveillance in patients who are poor surgical candidates. In conclusion, RFA for small Bosniak III and IV cysts in patients who are poor operative candidates is effective, and the outcomes compare favorably with those of the surgical treatment of cystic renal neoplasms. References 1. Bosniak MA. 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