Laparoscopic Radiofrequency Ablation of Small Renal Tumors: Long-Term Oncologic Outcomes

Abstract

Introduction:

Unlike percutaneous radiofrequency ablation (RFA) of small renal tumors, there are limited data assessing the long-term efficacy of laparoscopic RFA. Although the ablation cannot be visualized as reliably as with cryoablation, laparoscopic RFA allows for improved mobilization and placement of probes under direct vision. We reviewed our experience with laparoscopic RFA to assess long-term oncologic outcomes.

Methods:

We performed a retrospective study of all patients who had undergone laparoscopic RFA for pT1a renal tumors from April 2000 to April 2010. Demographic, clinical, and radiologic data were assessed to determine indications and evidence for recurrence of disease. Radiologic recurrence was defined as any new enhancement (>10 HU) after absence of enhancement on initial negative 6-week computed tomography.

Results:

Data were available for 79 patients who had 111 small renal masses treated over the 10-year period. The median tumor diameter was 2.2 cm and intraoperative biopsy identified renal cell carcinoma in 77%. The median follow-up was 59 months with an estimated 5-year recurrence-free survival of 93.3%. The overall rate of complications was 8.8% with a 3.8% rate of major complications.

Conclusions:

Long-term experience with laparoscopic RFA demonstrates that it is a safe and effective option for the treatment of small renal tumors. Five-year oncologic outcomes appear to be comparable to extirpation.

Introduction

The widespread use of cross-sectional abdominal imaging over the last 20 years has increased the diagnosis of incidentally detected, low-stage renal tumors, resulting in a change in their management.^1,2 This development has prompted urologists to investigate less invasive strategies aimed at maintaining local tumor control, while preserving the renal function and improving patient quality of life outcomes.^3,4 Renal tumor ablation, when compared with extirpative treatment, has been associated with a low rate of complications, less morbidity, and improved recuperation. Recently, it has become an increasingly acceptable approach in the management of small renal tumors as the number of institutions performing renal mass ablation is increasing. A percutaneous approach, compared with laparoscopic, has historically been the preferred method for the management of small renal masses undergoing radiofrequency ablation (RFA) due to its less invasive nature. However, in certain scenarios, critical structures such as the ureter or bowel may exist in close proximity to the renal tumor. In these instances, a laparoscopic approach may be necessary to mobilize these structures away from the renal tumor thereby allowing direct visualization and delivery of ablative treatment. Currently, the experience and follow-up of patients who have undergone a laparoscopic approach in the RFA literature are limited.^5

–8 We reviewed our experience with laparoscopic RFA to assess oncologic outcomes, safety, and efficacy and provide the longest follow-up in the literature to date.

Patients and Methods

Institutional review board approval was gained to retrospectively review all patients who underwent laparoscopic RFA from April 2000 to April 2010 at a single institution. There were a total of 80 patients identified who underwent laparoscopic RFA over this timeframe. Seventy-nine of those patients had available clinical data and were included in the study. All patients presented with an enhancing renal tumor seen on cross-sectional imaging and each elected to undergo laparoscopic RFA. Intraoperative incisional biopsies (5 mm cup forceps) were obtained routinely after ablation.⁸ Biopsy was done after ablation as an earlier study from our institution demonstrates that histological architecture is maintained in the tissue after RFA is performed.⁹ Tissue samples were examined with hematoxylin–eosin staining, and in some cases, immunohistochemical staining was performed to assist in the diagnosis.

All patients were treated with a Model 1500×Rita 250 watt radiofrequency generator with Starburst XL probes (AngioDynamics, Latham, NY) as previously described.⁸ Briefly, probes were inserted percutaneously under laparoscopic guidance after exposure of the renal tumor. Laparoscopic ultrasound was used to confirm proper probe deployment. The probe tines were deployed 5–10 mm beyond the diameter of the lesion, and ablation was performed in two, size-determined cycles to a target temperature of 105°C. A contrast-enhanced computed tomography (CT) scan was obtained 6 weeks postoperatively to confirm complete ablation of the target lesion. Radiologic surveillance consisted of contrast-enhanced axial imaging at 6 months, 12 months, and at least annually thereafter. Pretreatment and follow-up serum creatinine and glomerular filtration rate (GFR) were obtained and recorded, as were comorbidities, ASA score, age, and postoperative pathology results.

Incomplete ablation was defined as residual enhancement of the target lesion at 6 weeks of follow up. Recurrence was defined as an increase in the tumor size or enhancement (>10 HU) in the vicinity of the treated tumor.

Descriptive analysis was performed to characterize the patient population. The paired t-test was employed for evaluation of the changes in creatinine and estimated glomerular filtration rate (eGFR) after treatment. Estimated GFR was calculated using the abbreviated MDRD equation. The Kaplan–Meier method was used to determine an estimated a 5-year overall and recurrence-free survival.

Results

Patient demographic data are listed in Table 1. Our patient population had a mean age of 63.8 years and a mean ASA score of 2.6. A total of 111 tumors in 79 patients were treated with laparoscopic RFA. The mean size of the treated renal mass was 2.2 cm with a range of 0.9–4.2 cm. Six patients had solitary kidneys and 15 patients were diagnosed with pretreatment chronic kidney disease.

Table 1.

Patient and Tumor Characteristics

Patients, n	79
Total number of tumors	111
Single tumors	47
Multiple tumors	22
Bilateral tumors	10
Median age, years (range)	63.8 (18–35)
Mean ASA (SD)^*	2.6 (SD)
CKD ≥3	24
Mean size, cm (SD)^**	2.2 (SD)
Location, n (%)
Right	62 (55.9)
Left	49 (44.1)
Upper pole	26 (23.4)
Midpole	53 (47.7)
Lower pole	32 (28.8)
Anterior	55 (49.5)
Lateral	38 (34.2)
Posterior	18 (16.2)
Biopsy data, n (%)
RCC	61 (77.2)
AML	6 (7.6)
Oncocytoma	8 (10)
Nondiagnostic	4 (5.1)

SD value=2.1; ^**SD value=1.8.

CKD=chronic kidney disease.

Table 2 lists perioperative outcomes. Mean OR time was 164 minutes (range 65–335 minutes) with a mean estimated blood loss of 29 mL (range 0–400 mL). Mean length of stay (LOS) was 1.8 days (range of 0–12 days). One patient required a 12-day hospitalization due to a persistent ileus and ultimately was found to have renal pelvis obstruction. The overall rate of complications was 8.8% (n=7). Four (5.1%) of these complications were minor (Clavien grade 1–2). Three (3.8%) complications were major (Clavien grade 3b) with two patients requiring repeat surgery for obstruction of the collecting system at the ureteropelvic junction, one patient requiring conversion to laparoscopic nephrectomy, and one patient requiring stent placement for urinary fistula. The mean tumor size of the patients with grade 3b complications was 3.2 cm.

Table 2.

Perioperative Outcomes

Mean LOS (days)	1.8 (0–12)
Mean OR time (minutes)	164.3 (65–335)
Mean ablation time (minutes)	13.6 (3–32)
Overall complications, n (%)	7 (8.8)
Minor (<Clavian 3), n (%)	4 (5.1)
Major (≥Clavian 3), n (%)	3 (3.8)
Incomplete ablation, n (%)	2 (2.5)
Recurrence, n (%)	5 (6.3)
GFR (mL/minute/1.73 m²)
Mean pretreatment (SD)^*	65.86
Mean post-treatment (SD)^**	62.02
Change in GFR, mean (SD)^***	3.84
Median follow-up, months (range)	59 (2–120)

SD value=33.8; ^**SD value=30.6; ^***SD value=4.9.

GFR=glomerular filtration rate; LOS=length of stay; OR=operating room.

The median follow-up was 59 months. Two patients (2.5%) had incomplete ablation of their lesions on follow-up CT at 6 weeks and both patients were treated successfully with salvage percutaneous ablation. The estimated 5-year recurrence-free survival was 93.3% with only three patients having recurrence of disease. The two patients with persistent enhancing lesions on follow-up imaging at 6 weeks were included in the recurrence-free survival calculation (Fig. 1). Of the five patients who had recurrence or persistent disease, the mean tumor size was 2.1 cm and the mean and median time to recurrence were 55.5 and 39 months, respectively. The 5-year recurrence-free survival among the patients with biopsy proven RCC was 92%. Both 5-year cancer-specific survival and metastatic-free survival were 100% in our cohort. The estimated 5-year overall survival for our cohort of patients was 72% (Fig. 2). GFR data were collected during pretreatment evaluation and repeated at 12 months. Mean pretreatment GFR was 65.9 mL/minute/1.73 m² and 12-month mean post-treatment GFR was 62.0 mL/minute/1.73 m² representing a decrease in GFR of 5.8% over 12 months, although this change was not statistically significant.

FIG. 1.

Five-year disease-free survival curve.

FIG. 2.

Five-year overall survival.

Discussion

Within the realm of tissue ablation, different techniques have been implemented to target renal tumors. In the cryoablation literature, a laparoscopic approach has been preferred over a percutaneous approach. This may be because the expanding ice ball is easily visualized on ultrasound, allowing for the identification of an adequate ablation margin. For RFA, this relationship is reversed with more studies reporting a percutaneous technique as compared with a laparoscopic one. The reasons for this are not clear, although the relative difficulty of RFA probe placement with ultrasound guidance and the lack of a clearly defined ablation zone may be contributing factors. Despite these drawbacks, a laparoscopic approach may be preferred for RFA in certain situations where the proximity of critical structures to the renal tumor is of concern. Laparoscopic RFA allows for the mobilization of the ureter, bowel, and other structures away from the ablation zone and theoretically ensures their safety. For this reason, complications of in situ ablation of small renal tumors have been relatively low.^10

–13 Within our series, the overall complication rate was 8.8% with only 3.8% of patients suffering major complications (≥Clavien grade 3). In contrast to the cryoablation literature, hemorrhage was not an observed complication; however, two of the three major complications were related to injury to the ureter or collecting system. The patients who suffered ureteropelvic junction obstruction had tumors that were more anteriorly and medially located. These complications occurred early in our series and as our experience progressed, patients with more medially located tumors or tumors close to the collecting system were ultimately excluded from undergoing laparoscopic RFA. The surgical complications encountered in our series were felt to be due to the direct use of the RFA probe and location of the tumor, not directly due to laparoscopic dissection techniques.

Previous studies have reported similar complication rates. In 2004, Johnson et al. described a series of 139 cryoablations and 133 RFAs and found an overall complication rate of 11%, with 1.8% classified as major events.¹³ A meta-analysis by Novick et al. reported a 4.9% incidence of major complications after cryoablation and a 6.0% rate of major complications after RFA.¹⁴ Whereas this and other data suggest that complication rates between cryoablation and RFA appear similar, it has been widely reported that the risk of major urologic complications is lower with ablative techniques when compared with either open or laparoscopic partial nephrectomy.

As for oncologic outcomes of laparoscopic RFA, a recent series by Ji et al. demonstrated local tumor control in 98.1%.⁶ Within our series, oncologic outcomes where comparable with an estimated 5-year recurrence-free survival of 93.3% and a 5-year metastatic-free survival of 100%. In comparison to percutaneous series, there appears to be no difference in oncologic outcome measures.⁸ Whereas the vast majority of RFA studies demonstrate favorable oncologic outcomes, follow-up is limited and this is a common criticism of ablation therapy Thus the importance of this study, which provides 5-year follow-up data (median 59 months) demonstrating lasting efficacy for laparoscopic RFA.

Oncologic outcomes of RFA are often compared with extirpative therapy, with a somewhat increased rate of local recurrence seen in RFA series. However, distant recurrence remains an uncommon event using either technique with multiple studies confirming this result. Levinson et al. published one of the first long-term RFA reviews, which demonstrated a 90.3% recurrence-free survival and a 100% disease-specific survival.¹⁰ Although recent data suggest that residual tumor after local treatment may predispose patients to distant recurrence, this was not seen in our series as no patients developed metastatic disease.¹⁵ This may be, in part, the result of aggressively treating all patients with residual tumor (enhancement at 6 weeks) with immediate reablation. Joniau et al. showed that the success rate for RFA could be improved with repeated ablations increasing from 86.9% after a single treatment to 93.8% after two or more treatments.¹¹ This ability to perform RFA in succession is an additional advantage of ablative therapies. Indeed, our success rates for ablation approaches 100% when success after reablation is considered. In addition, the overall survival is similar between patients undergoing RFA and those undergoing active surveillance for small renal masses.^16,17

One of the purported advantages of tumor ablation over extirpative treatment is renal function preservation. A recent study from the Cleveland Clinic reviewed 427 patients who underwent robotic-assisted laparoscopic partial nephrectomy with a mean tumor size of 3.0 cm. They found a mean decrease in eGFR of 8% at a median follow-up less than 18 months.¹⁸ We found a decrease in mean eGFR of 5.8% at a 1-year follow-up. Thirty percent (n=24) of patients in our study had CKD stage 3 or greater before treatment such that, distinguishing the proportion of renal function loss from RFA versus the natural history of their pre-existing comorbidities was difficult. Nevertheless, there was no statistical loss in eGFR at 1 year. Multiple prospective reviews have shown a similar minimal effect of renal tumor RFA on renal function.^19,20

Several limitations of our study should be discussed. First, this was a retrospective study making the selection bias a concern, namely, selecting for sicker, older patients as well as smaller and anterior tumors. In addition, the sample size is limited; however, when compared with previous laparoscopic RFA series, the follow-up period is significantly improved. Another limitation of this study is the analysis of renal function. Reporting renal function at 1 year may not truly give insight as to the effect of nephron damage due to RFA; however, a longer follow-up would allow competing risk factors to obfuscate the issue, given a population with multiple comorbidities and pre-existing CKD. Lastly, lack of contrast enhancement was used as a surrogate for tumor destruction as opposed to ablation zone biopsy. Although this has been previously debated, numerous studies support this as a suitable method for following patients after RFA.

Conclusion

RFA through a laparoscopic approach is safe and effective in selected patients. Long-term outcomes are excellent using this approach in terms of both local and distant oncologic control and can be performed without a compromise to renal function.

Footnotes

Disclosure Statement

No competing financial interests exist.

Abbreviations Used

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