Percutaneous Ablation vs Robot-Assisted Partial Nephrectomy for Completely Endophytic Renal Masses: A Multicenter Trifecta Analysis with a Minimum 3-Year Follow-Up

Abstract

Purpose

: To compare outcomes of robot-assisted partial nephrectomy (RAPN) and percutaneous tumor ablation (PTA) for completely endophytic renal masses.

Methods

: Data of patients who underwent RAPN or PTA for treatment of completely endophytic (three points for “E” domain of R.E.N.A.L. score) were collected from seven high-volume U.S. and European centers. PTA included cryoablation, radiofrequency, or microwave ablation. Baseline characteristics, clinical, surgical, and postoperative outcomes were compared. Recurrence-free survival (RFS) was calculated with Kaplan–Meier analysis. Trifecta was used as arbitrary combined outcome parameter as proxy for treatment “quality.” Multivariable logistic regression model assessed predictors of trifecta failure.

Results

: One hundred fifty-two patients (RAPN, n = 60; PTA, n = 92) were included in the analysis. RAPN group was younger (p < 0.001), had lower American Society of Anesthesiologists score (p = 0.002), and higher baseline estimated glomerular filtration rate (p < 0.001). There was no difference in clinical tumor size, clinical T stage, and tumor complexity scores. PTA had significantly lower rate of overall (p < 0.001) and minor (p < 0.001) complications. ΔeGFR at 1 year was statistically higher for RAPN (−15.5 mL/min vs −3.1 mL/min; p = 0.005), no difference in ΔeGFR at last follow-up (p = 0.22) was observed. No difference in recurrences (RAPN, n = 2; PTA, n = 6) and RFS was found (p = 0.154). Trifecta achievement was higher for RAPN but not statistically different (65.3% vs 58.8%; p = 0.477). R.E.N.A.L. Nephrometry Score resulted predictive of trifecta failure (odds ratio = 1.47; confidence interval = 1.13–1.90; p = 0.004).

Conclusions:

PTA confirms to be an effective treatment for completely endophytic renal masses, offering low complications and good mid-term functional and oncologic outcomes. These outcomes compare favorably with those of RAPN, which seem to be the preferred option for younger and less comorbid patients.

Introduction

Robot-assisted partial nephrectomy (RAPN) is becoming the preferred method of nephron-sparing surgery (NSS) for renal tumors, including highly complex ones, in many institutions worldwide.^1,2 Percutaneous tumor ablation (PTA) is recognized by current guidelines as a safe NSS option, especially for unfit surgical candidates.^3,4

Completely endophytic renal masses represent a surgical challenge, given the absence of visual clues, the presence of intact overlying healthy parenchyma, and the likely proximity to vascular and caliceal structures.⁵ Over the years, several studies reported the outcomes of PN and PTA for cT1 renal masses.^6

–10 However, comparative analyses focusing on completely endophytic renal masses remain scanty.

The aim of this study was to compare the outcomes of RAPN and PTA for this specific indication in a multicenter international cohort of patients.

Materials and Methods

Study design and population

After institutional review board approval and data-sharing agreement, we collected data from seven high-volume U.S. and European centers. Patients who underwent RAPN or PTA for the treatment of a renal mass between 2010 and 2020 were included in the data set. Patients with previous kidney cancer surgery or multiple renal tumors were excluded. From the overall pool of 2660 patients, we extracted those cases where the renal mass had scored 3 points for the “E” domain of the R.E.N.A.L. nephrometry score (completely endophytic masses).¹¹

The PTA group included patients who underwent cryoablation, radiofrequency, or microwave ablation.¹² Malignancy was confirmed by biopsy done at the time of the procedure for PTA group or from the pathology report in the RAPN group. The follow-up protocol included contrast-enhanced CT at 1 to 3, 6, 9, 12 months, and then every 6 months after PTA. For RAPN cohort the protocol included contrast-enhanced CT at 6 months and then every 6 to 12 months for the first 2 years. The relapse was defined as the detection of a new enhancing lesion after RAPN or persisting/recurring enhancement after PTA (without a routine biopsy confirmation).

Data collection

Baseline characteristics, clinic, pathologic, and postoperative (outcomes and follow-up) data were collected. Patient features included age, gender, body mass index (BMI), hypertension, diabetes, American Society of Anesthesiologists (ASA) score, preoperative hemoglobin level (Hb), preoperative creatinine, preoperative estimated glomerular filtration rate (eGFR), preoperative chronic kidney disease (CKD) stage, and solitary kidney status. Tumor characteristics included clinical tumor size (cm), clinical T stage, and R.E.N.A.L. score. Operative outcomes included operative time (OT), length of stay, postoperative Hb, differences in Hb level (ΔHb) by comparing preoperative Hb with Hb at discharge, intraprocedural complications, overall postprocedural complications (according to Clavien–Dindo classification¹³), and 30 days readmission.

Pathologic outcomes included benign and malignant histology. Further data on pathology tumor size, pathologic T status, and positive surgical margins were collected for patients undergoing RAPN. To evaluate functional outcomes eGFR at 1 year, eGFR at latest follow-up were collected; differences in eGFR (ΔeGFR) by comparing preoperative eGFR with eGFR at 1-year value and at the latest follow-up were evaluated. Data about new-onset CKD > III, upstaging CKD, recurrence, metastasis, and death were collected. Oncologic outcomes were restricted to malignant cases.

Analysis

Statistical analysis was conducted following current guidelines.¹⁴ Baseline characteristics, clinical, surgical, and postoperative outcomes were compared between the two groups (RAPN vs PTA). Kolmogorov–Smirnov (test K–S) was assessed to evaluate the data distribution. Mean ± standard deviation was adopted for normal distribution data. When no-normal distribution data, median and interquartile range was employed. Frequency (%) was reported for categorical data. To compare continuous variables t-test and Kruskal–Wallis H test were used according to the distribution. For categorical ones, Fisher's exact or Pearson chi-squared test were adopted to assess differences. Recurrence-free survival (RFS) was calculated with Kaplan–Meier analysis and long-rank test was used to assess differences among treatments.

Trifecta was used as an arbitrary combined outcome parameter as proxy for treatment “quality,” by only considering cases with malignant histology. A trifecta was defined as follows. For RAPN: no major complication + no significant (<25%) eGFR reduction from baseline + negative surgical margin. For PTA: no major complication + no significant (<25%) reduction from baseline + no technical failure (defined as no residual mass/enhancement at 6 months). We selected age (continuous variable), BMI (continuous variable), ASA score (continuous variable), R.E.N.A.L. Nephrometry Score (continuous variables), and type of procedure as parameters for univariable and multivariable logistic regression. Our model was assessed to find an independent predictor of Trifecta failure.

Results

Baseline characteristics

We retrieved 152 with completely endophytic masses. Among them, 60 underwent RAPN, and 92 PTA. Their clinical and pathologic characteristics are shown in Table 1. Median age of the RAPN group was significantly lower (56.4 years vs 63.4 years; p < 0.001). PTA patients presented higher ASA score rate (p = 0.002). Renal function of the PTA group was significantly worst, given lower baseline mean eGFR (69.7 + 26.8 mL/min vs 89.1 + 20.8 mL/min; p < 0.001) and rate of CKD >III stage (31.5% vs 5%; p < 0.001). Moreover, the PTA cohort presented a higher rate of solitary kidney (20.6% vs 5%; p < 0.001). No difference was observed in terms of clinical tumor size, clinical T stage, and tumor complexity scores.

Table 1.

Baseline Characteristics

	RAPN (n = 60)	PTA (n = 92)	p
Age, median (IQR)	56.4 (19.0–79.0)	63.4 (20–88)	<0.001
Gender, n (%)			0.819
Male	42	66
Female	18	26
BMI, kg/m², mean (SD)	28 (6.3)	28 (6.2)	0.937
Hypertension, n (%)	31 (51.7)	55 (59.8)	0.327
Diabetes, n (%)	10 (16.7)	26 (28.3)	0.102
ASA score, n (%)			0.002
1	2 (3.3)	1 (1.1)
2	35 (58.3)	35 (38)
3	23 (38.3)	50 (54.3)
Preoperative Hb, mean (SD)	14.1 (1.7)	13.6 (1.8)	0.129
Preoperative Cr, mL/, mean (SD)	0.9 (0.22)	1.3 (0.75)	<0.001
Preoperative eGFR, mL/min, mean (SD)	89.1 (20.8)	69.7 (26.8)	<0.001
CKD > stage III, n (%)	3 (5)	29 (31.5)	<0.001
Solitary kidney, n (%)	3 (5)	19 (20.6)	<0.001
Clinical tumor size, cm, mean (SD)	2.8 (0.99)	2.6 (1.57)	0.055
cT stage, n (%)			0.07
1a	46 (76.7)	85 (92.4)
1b	10 (16.6)	5 (5.4)
2a	4 (6.7)	2 (2.2)
RENAL score, median (IQR)	9 (7–11)	9 (6–12)	0.347

ASA = American Society of Anesthesiologists; BMI = body mass index; CKD = chronic kidney disease; eGFR = estimated glomerular filtration rate; Hb = hemoglobin level; IQR = interquartile range; PTA = percutaneous tumor ablation; RAPN = robot-assisted partial nephrectomy; RENAL = R.E.N.A.L. Nephrometry Score; SD = standard deviation.

Operative outcomes

Surgical outcomes are described in Table 2. Mean OT was statistically lower for PTA group (75.5 + 63.8 minutes vs 175.6 + 63.1 minutes; p < 0.001), along with postoperative mean Hb (p = 0.03) and ΔHb at discharge (p < 0.001). PTA had a significantly lower rate in terms of overall (2.2% vs 16.7%; p < 0.001) and minor (1.1% vs 15%; p < 0.001) postoperative complication rates. No difference was observed for Clavien–Dindo ≥3 complications (Supplementary Table S1). Also, there was no difference in the 30 days readmission rate (6.7% vs 5.4%).

Table 2.

Operative Outcome

	RAPN, N = 60 (39.5)	PTA, N = 92 (60.5)	p
OT, minutes, mean (SD)	175.6 (63.1)	75.5 (63.8)	<0.001
LOS, days, mean (SD)	4.03 (3.3)	3.1 (4.5)	0.20
Postoperative Hb, mean (SD)	11.5 (1.7)	12.5 (1.9)	0.03
Intraprocedural complications, n (%)	2 (3.3)	3 (3.2)	0.981
Postprocedural complications, n (%)
Overall	10 (16.7)	2 (2.2)	<0.001
Grade 1–2	9 (15)	1 (1.1)
Grade 3–4	1 (1.7)	1 (1.1)
30 Days readmissions, n (%)	3 (6.7)	5 (5.4)	0.970

LOS = length of stay; OT = operative time.

Renal function outcome

Changes in renal function are shown in Table 3. The ΔeGFR at 1 year for the RAPN group was significantly higher than PTA (−15.5 mL/min vs −3.1 mL/min; p = 0.005), but no differences in ΔeGFR at last follow-up (−13.5 vs −19.3, p = 0.22) was observed. New-onset CKD III rate was statistically higher in PTA (25% vs 11.7%, p = 0.02). No statistical difference was observed for upstaging CKD rate between groups (21.7% for RAPN vs 25% for PTA).

Table 3.

Tumor Pathology and Follow-Up

	RAPN (n = 60)	PTA (n = 92)	p
Pathology size, cm, mean (SD)	2.6 (0.7–5.7)
pT stage, n (%)
1a	48 (80)
1b	6 (10)
2a	3 (5)
2b	2 (3)
3a	1 (2)
Malignant, n (%)	38 (63.3)	59 (64.1)	0.878
Positive margins, n (%)	2 (3.3)
Follow-up, month, mean (SD)	40.4 (32)	35.6 (35.1)	0.725
eGFR at 1 year, mL/min, mean (SD)	75.9 (21.3)	63.2 (28.5)	0.06
Latest eGFR, mL/min, mean (SD)	74.9 (26.8)	57.9 (23.3)	0.003
ΔeGFR at 1 year, mean	−15.5 (17.2)	−3.1 (14.8)	0.005
ΔeGFR at latest F/Up, mean (SD)	−13.5 (19.2)	−19.3 (28.7)	0.22
New onset CKD III, n (%)	7 (11.7)	23 (25)	0.02
Recurrence, n (%)	2 (3.3)	6 (6.5)	0.428
Metastasis, n (%)	0 (0)	3 (3.3)	0.139
Death, n (%)	9 (15)	15 (15.1)	0.105
Trifecta achievement (%)	(65.3)	(58.8)	0.477

ΔeGFR = differences in eGFR.

Oncologic outcomes

Malignant histology was present in 63.3% of RAPN patients and in 64.1% of PTA patients (p = 0.878). Mean follow-up was not statistically different between groups, with a mean of 44.4 (32) and 35.6 (35.1) months for RAPN and PTA, respectively (Table 3). The number of recurrences was 2 for RAPN (3.3%) and 6 for PTA (6.5%), with no statistical difference. Metastases occurred in 3 patients (3.3%) in the PTA vs 0 in RAPN group, and no statistical difference was found (p = 0.139). Similar death rates were recorded in the two groups (9%). Kaplan–Meier analysis did not show any difference in RFS (p = 0.154) (Supplementary Fig. S1).

Trifecta outcome

Trifecta achievement was higher for the RAPN group but without being statistically different (65.3% vs 58.8%; p = 0.477) (Table 3). At multivariable analysis, RENAL score was found to be predictive of trifecta failure (odds ratio [OR] 1.47; confidence interval [CI] 1.13–1.90; p = 0.004) (Table 4).

Table 4.

Univariate and Multivariate Logistic Regression Analysis Evaluating the Predictive Value of Baseline Patient and Tumor Characteristics on Trifecta Failure Among Patients with Proven Malignant Histology

	Univariate analysis			Multivariate analysis
	OR	95% CI	p	OR	95% CI	p
Age	0.99	0.97–1.03	0.923	0.99	0.96–1.02	0.489
BMI	0.95	0.90–1.01	0.111	0.95	0.89–1.01	0.100
ASA score	1.23	0.65–2.32	0.521	1.36	0.67–2.76	0.391
RENAL score	1.42	1.12–1.80	0.003	1.47	1.13–1.90	0.004
PTA procedure	0.76	0.35–1.62	0.477	1.12	0.45–2.77	0.805

Age, BMI, ASA score, and RENAL score were considered as continuous variables. The PTA procedure was a dichotomous variable.

Discussion

To the best of our knowledge, herein we report the first analysis looking at the comparative outcomes of RAPN vs PTA in the specific subset of patients with a completely endophytic renal mass. The feasibility of RAPN for completely endophytic was first reported in a single institution experience in 2009.¹⁵ Only a single-arm study reported that percutaneous cryoablation is a safe and effective approach in a cohort of 47 patients with completely endophytic renal.¹⁶ Our analysis offers some interesting observations that may contribute to the debate on these high-complexity cases.

PTA is classically reported as a safe and effective treatment for small renal masses, with excellent oncologic efficacy and a low complication rate.¹⁷ This evidence led to the implementation of these procedures, especially for surgical unfit and comorbid patients.^3,4,9 In a recent study, cryoablation has been proved to be a specifically valuable option even for high-complexity preoperative aspects and dimensions used for an anatomical classification ≥10 (PADUA) renal tumors.¹⁸ This evidence is consistent with our finding where PTA approach was adopted in older and more comorbid patients with completely endophytic renal masses. In an analysis based on the Surveillance, Epidemiology, and End Results (SEER) data, Larcher et al found that when PTA is chosen over PN, the reduction in the risk of complications is greatest in high-risk patients and, therefore, they concluded that these are the patients who might represent ideal PTA candidates.¹⁹

Renal function preservation is one of the key outcomes after NSS.^20

–23 In our series, we observed a worse ΔeGFR at 1 year for RAPN, whereas no difference at the ΔeGFR at latest F/Up was detected. In looking at these findings, we need to consider the different baseline characteristics of our cohorts. Indeed, renal function of PTA was significantly worse than RAPN group in terms of lower baseline mean eGFR (69.7 vs 89.1; p < 0.001) and rate of CKD >III stage (31.5% vs 5%; p < 0.001). Similarly, in a recent comparative study, preoperative eGFR was significantly higher in RAPN than PTA cohort and no difference in eGFR preservation throughout years was detected.²⁴ In contrast, the worsening of renal function at the latest PTA follow-up may be explained by the baseline selection bias, because of a worse baseline renal function and overall higher rate of comorbidities among PTA patients.

This could also explain the higher rate of new-onset CKD III in PTA cohort after treatment. Several studies showed that patients undergoing surgery had an initial eGFR drop starting from the postoperative period, with a partial recovery at 6 months and a complete stabilization up to 1 year.²⁵ In a meta-analysis of literature, a lower decline of renal function for radiofrequency ablation vs PN (mean difference = 5.31, p = 0.003) and no significant difference between cryoablation and PN (mean difference = −0.19, p = 0.921) or microwave and PN (mean difference = −4.4, p = 0.393).²⁶ However, one must consider that, over the years, technology in ablative procedures has developed, and when pooling outcomes of distinct systems and techniques in a single analysis group, this may carry an intrinsic bias. This uncertain evidence has been recently reported by Abu-Ghanem et al who highlighted the inadequacy of the current data and the incapacity to make any strong and clear conclusions.²⁷

Concerning surgical outcomes, mean OT (75.5 + 63.8 minute vs 175.6 + 63.1 minute; p < 0.001), postoperative mean Hb (p = 0.03), and ΔHb at discharge (p < 0.001) were statistically lower for PTA group, considering no difference in clinical tumor size, clinical T stage, and tumor complexity scores among groups. Furthermore, in accordance with the previous reports,⁶ overall and minor postoperative complication rates were lower for PTA group (16.7% vs 2.2% and 15% vs 1.1%, respectively), whereas no difference was observed for high-grade complications. Similar findings were described by Bianchi et al who reported a lower rate of overall postoperative complications (11.7% vs 24.8%) compared with PN group (p < 0.001),⁸ and by Rivero et al in their meta-analysis (13% vs 17.6%; OR, 0.49; 95% CI 0.25–0.94; p < 0.05).⁶ This finding likely reflects the overall higher degree of invasiveness of RAPN procedure, which carries low risk of major complications in patients with small renal mass.²⁸

In addition, even if a trifecta composite outcome is not systematically reported for PTA, we decided to use it as a measure of treatment efficacy and safety, or, one might say, “quality” metrics.²⁹ For the present analysis, this was arbitrarily defined in a slightly different way for RAPN and PTA. We adopted the concept of “technical failure,” which was defined as “positive margin” for RAPN cases (a widely accepted parameter), and as “no residual mass/enhancement at 6 months” for PTA, based on the evidence that 6 months is a reliable time point to determine the technical success of a PTA treatment.³⁰

Trifecta was achieved in 65.3% and 58.8% of cases, respectively, with no statistical difference between the two groups. Furthermore, multivariate regression model showed RENAL score to be predictive of trifecta failure (OR 1.47; CI 1.13–1.90; p = 0.004). In a recent multicenter analysis, Carbonara et al reported how trifecta achievement in patients undergoing RAPN was lower in completely endophytic than mesophytic and exophytic tumors.⁵

To note, in our analysis the mean tumor size was 2.6 cm for the PTA group, which according to current guidelines might be the best size range for PTA. Mean follow-up was not statistically different between groups (mean 44.4 and 35.6 months for RAPN and PTA, respectively). The number of recurrences was 2 for RAPN (3.3%) and 6 for PTA (6.5%), with no statistical difference, and metastases occurred in 3 PTA patients (3.3%) vs none RAPN patient, also without statistical difference (p = 0.139). The Kaplan–Meier analysis did not show any difference in RFS (p = 0.154).

Overall, we could not detect any significant difference in terms of major oncologic outcomes. Similarly, in the latest analysis from the Mayo Clinic group on a total of 1798 patients with >6 years of follow-up, no significant differences between PN and ablative procedures were reported in terms of major oncologic outcomes for cT1 disease.⁷ In one of the most up-to-date meta-analyses on the subject, Rivero et al also found no significative difference in local recurrence (hazard ratio [HR], 1.32; p = 0.22) and in risk of metastasis (HR, 1.83; p = 0.23) between groups.⁶

Our study carries intrinsic limitations, mostly related to the retrospective design. A patient-selection bias may certainly be present, and it should be considered when interpreting our study findings. The absence of standardized pre- and postoperative management among the different centers may have also influenced the outcomes. More specifically, merging different sources of ablation in the specific setting of endophytic masses might be regarded as another bias to be accounted for.

Conclusions

In a contemporary multicenter analysis, PTA confirms to be a safe and effective treatment option for completely endophytic renal masses, offering low complication rates, and good mid-term functional and oncologic outcomes. These outcomes compare favorably with those of RAPN, which remains the preferred NSS option for younger and less comorbid patients.

Footnotes

Authors' Contributions

Conceptualization, data curation, methodology, and writing—original draft (equal) by S.D.P. Conceptualization, data curation, and methodology (equal) by A.T.B. Data curation and supervision (equal) by I.D. Data curation (lead) by A.C. Supervision (lead) by R.S., G.C., C.C., C.I., V.M., J.E., G.B., L.J.H., and F.J.K. Data curation and writing—review and editing (equal) by L.B. Supervision and writing—review and editing (equal) by U.C., D.L., and G.L. Supervision, project administration, and writing—review and editing (equal) by J.K. Conceptualization, data curation, formal analysis, project administration, and writing—original draft (equal) by R.A.

Author Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

Supplementary Material

Supplementary Figure S1

Supplementary Table S1

Abbreviations Used

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