Comparison of Robot-Assisted and Laparoscopic Partial Nephrectomy for Completely Endophytic Renal Tumors: A High-Volume Center Experience

Abstract

Objectives:

To compare the perioperative, functional, and oncologic outcomes of robot-assisted partial nephrectomy (RAPN) and laparoscopic partial nephrectomy (LPN) for completely endophytic renal tumors (three points for the “E” element of the R.E.N.A.L. scoring system).

Materials and Methods:

We retrospectively reviewed patients who underwent either RAPN or LPN between 2013 and 2016. Baseline characteristics, perioperative, functional, and oncologic outcomes were compared. Univariable and multivariable logistic analyses were performed to determine factors associated with pentafecta achievement (ischemia time ≤25 minutes, negative margin, no perioperative complication, return of estimated glomerular filtration rate [eGFR] to >90% from baseline, and no chronic kidney disease upstaging).

Results:

No significant differences between RAPN vs LPN were noted for operating time (105 minutes vs 108 minutes, p = 0.916), estimated blood loss (50 mL vs 50 mL, p = 0.130), renal artery clamping time (20 minutes vs 20 minutes, p = 0.695), rate of positive margins (3.3% vs 2.0%, p = 1.000), and postoperative complication rates (18.0% vs 21.6%, p = 0.639). RAPN was associated with a higher direct cost ($11240 vs $5053, p < 0.001). There were no significant differences in pathology variables, rate of eGFR decline for postoperative 12-month (9.8% vs 10.6%, p = 0.901) functional follow-up. Multivariate analysis identified that only RENAL score was independently associated with the pentafecta achievement.

Conclusions:

For completely endophytic renal tumors, both RAPN and LPN have excellent and similar results. Both operation techniques remain viable options in the management of these cases.

Introduction

With the wide application of abdominal sectional imaging, more and more low-stage renal tumors have been identified.¹ Nephron-sparing procedure is at present the accepted standard of treatment for patients with renal masses ≤4 cm, also for patients with T1b malignances when technically feasible.^2,3 However, problems increase when renal tumors are completely endophytic and small, all treatment options must be evaluated to choose the best treatment for these patients. Nephron sparing procedure for completely endophytic masses is technically challenging because of the increased difficulty in tumor identification and substantial involvement, necessitating intraoperative ultrasound examination to identify tumors and make surgical plans.⁴ Unreasonable surgical plans of partial nephrectomy for endophytic tumors may lead to excessive warm ischemia time, positive margin, postoperative urinary leakage, vascular injury, even conversion to radical procedure.

In 2011, Chung and colleagues⁵ reported that laparoscopic partial nephrectomy (LPN) for endophytic tumors can achieve comparable perioperative outcomes when compared with exophytic tumors, demonstrating the technical feasibility and safety of LPN for completely intrarenal tumors. After that, a few institutions have reported similar experiences with successful LPN for completely endophytic tumor.^6,7 Surgical management of intrarenal tumors remains technically demanding and challenging, even when performed by experienced laparoscopic surgeons. Surgical robotic devices are more and more widely being used in complex endoscopic procedures and may promote the application of minimally invasive surgical techniques in such operations. Recently, several institutions have described their successful experience of robot-assisted partial nephrectomy (RAPN) for endophytic renal masses, and which can be a safe and effective alternative to open procedure.^8

–11 Nevertheless, the evidence of comparing the two minimal invasive approaches (LPN and RAPN) for treating completely endophytic tumors is lacking.

Therefore, in this study, we tried to compare the perioperative, functional, and oncologic results between RAPN and LPN for completely endophytic T1 renal masses.

Materials and Methods

Study patients

The present academic tertiary center has prospectively established a renal tumor database. We retrospectively reviewed patients who underwent either RAPN or LPN for renal mass between 2013 and 2016. The relevant data were extracted from our database. The complexity of renal tumor was evaluated with the R.E.N.A.L. scoring system¹² according to preoperative CT or MRI. Completely endophytic renal tumors were identified as cases attributed three points for the “E” element of the R.E.N.A.L. scoring system, which is applied to assess the endophytic/exophytic proportion of the renal mass. Representative images of CT or MRI is given in Figure 1. The RAPN and LPN surgical procedures were performed based on expertise and preference of the experienced, high-volume surgeons. All operations were performed by four surgeons (H.L., B.W., X.M., and X.Z.). They have individual experience of >50 LPN and 25 RAPN. Surgical procedures of RAPN and LPN were performed as previously described.^13,14 For all cases, a drop-in ultrasound probe was used to ascertain the location and depth of tumors, and corresponding surgical margin was planned. The hypothermic ischemic techniques (surface cooling with ice slush or endoscopic retrograde transureteral perfusion) were applied in some selected cases. Between 2013 and 2016, 1806 patients underwent partial nephrectomy for renal mass in our center. After excluding cases lacking the required information, 61 patients undergoing RAPN and 51 patients undergoing LPN were included. The medical ethics committee approved this study and informed consent was obtained from each of the included subjects.

FIG. 1.

Representative images of CT or MRI. White arrow point to renal tumor. (A) coronal section; (B) transverse section.

Study variables and outcomes

Patient baseline features included age, gender, American Society of Anesthesiologists (ASA) score, body mass index (BMI), Charlson comorbidity index (CCI) score, history of abdominal procedure, medical history of hypertension or diabetes, tumor laterality and size, anatomical characteristics of the mass, ischemic method, and preoperative estimated glomerular filtration rate (eGFR). Anatomic characteristics of the renal mass were assessed by two independent researchers in the light of the R.E.N.A.L. scoring system (K.L. and D.S.).¹² Any dispute was resolved by discussing with the senior researchers.

Baseline demographics and tumor features, operative, pathologic, functional, and oncologic outcomes were compared between RAPN and LPN. Operative variables included operating time, estimated blood loss, renal artery clamping time, conversion to radical or open, surgical margin status, postoperative hospital stay, direct cost, and postoperative relevant complications. The pathology slices of all patients were re-reviewed by a genitourinary pathologist. We recorded complications based on the modified Clavien–Dindo classification system.^15,16 Preoperative and postoperative eGFR was judged with the CKD-EPI equation.¹⁷ Changes in eGFR of postoperative 1 day and 12 months were calculated. Pentafecta achievement was considered as negative surgical margin, a ischemia time ≤25 minutes, no perioperative complications, return of eGFR to >90% from baseline, and no CKD upstaging.¹⁸ Upgrade of CKD stage was deemed as upgrading to stage III, IV, or V, did not embrace stage I to II. After operation, each patient was regularly followed-up. Details of local recurrence and distant metastasis were recorded.

Statistical analyses

The Kolmogorov–Smirnov test was used to test normality for all continuous variables. When normally distributed, they were presented as mean ± standard deviation. They were shown as median and interquartile range with a non-normal distribution. For continuous variables, the t independent test or Wilcoxon rank sum test was applied to test the differences. For categorical variables, the Pearson chi-squared or Fisher's exact test was used to check the differences. Univariable and multivariable logistic regression analyses were used to identify independent factors for predicting postoperative pentafecta achievement. Variables were selected based on results of univariable analysis and clinical experience for multivariable analysis. All statistical analyses were performed with R software (version 3.3.1). Statistical significance was considered as a two-sided p < 0.05.

Results

The study included 61 and 51 subjects treated with RAPN and LPN, respectively, for completely endophytic tumors. Patients' demographics and tumor characteristics are given in Table 1. Operation year distribution differed significantly between RAPN and LPN (p < 0.001). RAPN was increasingly performed every year; however, the number of LPN was stable. No significant difference was identified between approaches in the field of age, sex, BMI, ASA score, CCI score, medical history of hypertension or diabetes, abdominal procedure history, rate of solitary kidney, side and size of tumor, anatomical characteristics of the mass, rate of hilar mass, rate of hypothermic ischemia, and preoperative serum creatinine and eGFR (p > 0.05 for all).

Table 1.

Patients' Demographics and Tumor Characteristics

	RAPN	LPN	p
No. of patients	61	51
Age, years, mean (SD)	48.2 (11.6)	47.3 (12.3)	0.664
Surgical cases per year, n (%)			<0.001
2013	0 (0.0)	13 (25.5)
2014	9 (14.8)	10 (19.6)
2015	17 (27.9)	16 (31.4)
2016	35 (57.4)	12 (23.5)
Male patients, n (%)	47 (77.0)	38 (74.5)	0.754
BMI, kg/m², mean (SD)	25.1 (3.5)	25.4 (4.0)	0.588
ASA score, n (%)			1.000
1 and 2	59 (96.7)	50 (98.0)
3 and 4	2 (3.3)	1 (2.0)
CCI score, n (%)			1.000
0–1	55 (90.2)	46 (90.2)
≥2	6 (9.8)	5 (9.8)
Presence of diabetes, n (%)	5 (8.2)	9 (17.6)	0.159
Presence of hypertension, n (%)	13 (21.3)	15 (29.4)	0.384
Previous abdominal procedure, n (%)	12 (19.7)	9 (17.6)	0.813
Solitary kidney, n (%)	3 (4.9)	1 (2.0)	0.624
Left tumor, n (%)	29 (47.5)	25 (49.0)	1.000
Tumor size, cm, median (IQR)	2.3 (2.1–2.8)	2.5 (1.8–3.0)	0.927
R.E.N.A.L. score, median (IQR)	9 (8–10)	8 (7–10)	0.442
R.E.N.A.L. complexity class, n (%)			0.279
Low (4–6)	2 (3.3)	5 (9.8)
Moderate (7–9)	39 (63.9)	27 (52.9)
High (10–12)	20 (32.8)	19 (37.3)
Anterior/posterior aspect, n (%)			0.724
Anterior	19 (31.1)	13 (25.5)
Posterior	13 (21.3)	10 (19.6)
Not determined	29 (47.5)	28 (54.9)
Hilar tumor, n (%)	14 (23.0)	8 (15.7)	0.353
Hypothermic ischemia, n (%)	8 (13.1)	3 (5.9)	0.224
Preoperative creatinine (μmol/L), median (IQR)	74.0 (65.3–87.7)	73.4 (64.7–86.4)	0.429
Preoperative eGFR (mL/min/1.73 m²), median (IQR)	100.9 (88.9–108.3)	97.3 (89.5–105.5)	0.668

ASA = American Society of Anesthesiologists; BMI = body mass index; CCI = Charlson comorbidity index; eGFR = estimated glomerular filtration rate; IQR = interquartile range; LPN = laparoscopic partial nephrectomy; RAPN = robot-assisted partial nephrectomy; SD = standard deviation.

The perioperative results are detailed in Table 2. Patients undergoing RAPN had a similar median operating time (105 minutes vs 108 minutes, p = 0.916), median blood loss (50 mL vs 50 mL, p = 0.130), median ischemia time (20 minutes vs 20 minutes, p = 0.695), median postoperative hospital stay (6 days vs 6 days, p = 0.114), and rate of positive surgical margin (3.3% vs 2.0%, p = 1.000) compared with patients undergoing LPN. There are no conversions to radical or open procedure and transfusions occurred for patients in both two groups. The patients in the RAPN group had a lower rate of total (18.1% vs 21.6%) and minor (14.8% vs 21.6%) postoperative complications, a higher proportion of major postoperative complications (3.3% vs 0.0%); however, these differences were not statistically significant (p > 0.05 for all).

Table 2.

Perioperative Outcomes

Variable	RAPN	LPN	p
Operating time, minutes, median (IQR)	105 (90–134)	108 (90–131)	0.916
Estimated blood loss, mL, median (IQR)	50 (20–100)	50 (30–100)	0.130
Renal artery clamping time, minutes, median (IQR)	20 (15–30)	20 (16–30)	0.695
Transfusion, n (%)	0 (0.0)	0 (0.0)
Conversion to radical, n (%)	0 (0.0)	0 (0.0)
Conversion to open, n (%)	0 (0.0)	0 (0.0)
Positive surgical margin, n (%)	2 (3.3)	1 (2.0)	1.000
Postoperative hospital stay, days, median (IQR)	6 (5–7)	6 (5–7)	0.114
Direct cost ($), median (IQR)	11240 (10623–11926)	5053 (4490–5764)	<0.001
Postoperative complications, n (%)	11 (18.0)	11 (21.6)	0.639
Minor	9 (14.8)	11 (21.6)	0.348
Clavien 1	6 (9.8)	5 (9.8)
Clavien 2	3 (4.9)	6 (11.8)
Major	2 (3.3)	0 (0.0)	0.500
Clavien 3	1 (1.6)	0 (0.0)
Clavien 4	1 (1.6)	0 (0.0)

Pathology results and follow-up data are summarized in Table 3. According to pathology reports, 98.4% (60/61) and 92.2% (47/51) renal masses in RAPN and LPN group were malignant tumors, 90.0% (54/61) and 83.0% (39/51) renal masses in RAPN and LPN group were clear cell renal-cell carcinomas. A small part of patients had a pathologic T1b tumor, a Fuhrman grade 3 to 4 tumor, and a tumor with necrosis. No significant difference was identified between approaches in the field of tumor histology, pathology stage, Fuhrman grade, and tumor necrosis (p > 0.05 for all). After operation, the eGFR was higher in the RAPN group at day 1 (87.2 mL/min/1.73 m² vs 76.4 mL/min/1.73 m²) and month 12 (94.5 mL/min/1.73 m² vs 83.8 mL/min/1.73 m²), the proportion of eGFR decrease was lower in the RAPN group at day 1 (13.6% vs 22.4%) and month 12 (9.8% vs 10.6%); however, all these differences were not significant (p > 0.05 for all). Patients belonging to LPN group had a longer median follow-up time (39.2 months vs 27.3 months, p < 0.001). During the follow-up time, no local recurrence and distant metastasis appeared in these patients in both approaches.

Table 3.

Pathology Outcomes and Follow-Up Data

Variable	RAPN	LPN	p
Tumor histology, n (%)
Malignant	60 (98.4)	47 (92.2)	0.175
Clear cell RCC	54 (90.0)	39 (83.0)
Papillary RCC	0 (0.0)	1 (2.1)
Chromophobe RCC	2 (3.3)	3 (6.4)
Cystic RCC	2 (3.3)	0 (0.0)
Translocation RCC	1 (1.7)	1 (2.1)
Other types	1 (1.7)	3 (6.4)
Pathology stage, n (%)			1.000
T1a	57 (95.0)	45 (95.7)
T1b	3 (5.0)	2 (4.3)
Fuhrman grade, n (%)			0.393
Low (1–2)	52 (96.3)	34 (91.9)
High (3–4)	2 (3.7)	3 (8.1)
Tumor necrosis, n (%)	4 (6.6)	2 (3.9)	0.687
Postoperative eGFR, median (IQR)
1-Day eGFR, mL/min/1.73 m²	87.2 (65.8–98.5)	76.4 (64.9–91.6)	0.295
1-Day % eGFR decline	13.6 (7.1–25.7)	22.4 (5.8–36.1)	0.244
12-Month eGFR, mL/min/1.73 m²	94.5 (74.9–103.4)	83.8 (79.6–101.5)	0.809
12-Month % eGFR decline	9.8 (2.1–19.6)	10.6 (5.4–17.0)	0.901
Follow-up, months, median (IQR)	27.3 (23.8–36.3)	39.2 (29.7–54.2)	<0.001
Oncologic outcomes, n (%)
Local recurrence	0 (0.0)	0 (0.0)
Distant metastasis	0 (0.0)	0 (0.0)

RCC = renal-cell carcinoma.

Pentafecta achievement and the five components were examined between the two groups (Table 4). No significant difference was identified for each component (p > 0.05 for all). Moreover, rates of pentafecta achievement were comparable between RAPN and LPN (42.6% vs 37.3%, p = 0.564). Finally, univariable and multivariable analyses identified that only RENAL score (odds ratio [OR] = 0.629, 95% confidence interval [CI] = 0.456, 0.869, p = 0.005) was an independent predictor for postoperative pentafecta achievement (Table 5).

Table 4.

Pentafecta Analysis Comparing Robot-Assisted Partial Nephrectomy and Laparoscopic Partial Nephrectomy

Outcome	RAPN	LPN	p
Negative margins	59 (96.7)	50 (98.0)	1.000
No complications	50 (82.0)	40 (78.4)	0.639
Ischemia time ≤25 minutes	41 (67.2)	32 (62.7)	0.621
eGFR >90% of preop	43 (70.5)	34 (66.7)	0.664
No CKD upstaging	58 (95.1)	50 (98.0)	0.624
“Pentafecta”	26 (42.6)	19 (37.3)	0.564

CKD = chronic kidney disease.

Table 5.

Univariable and Multivariable Analysis for Factors Associated with Achieving Pentafecta

Variable	Univariate		Multivariate
Variable	OR (95% CI)	p	OR (95% CI)	p
Age	1.008 (0.976, 1.041)	0.634
BMI	0.996 (0.899, 1.102)	0.933
Sex (male vs female)	1.190 (0.487, 2.905)	0.702
Diabetes	0.364 (0.095, 1.386)	0.138
Hypertension	1.408 (0.594, 3.340)	0.437
CCI (≥2 vs 0–1)	0.527 (0.132, 2.104)	0.364	0.308 (0.062, 1.521)	0.148
ASA score (3 + 4 vs 1 + 2)	0.739 (0.065, 8.396)	0.807
Previous abdominal procedure	1.146 (0.438, 2.996)	0.781
Tumor laterality (right vs. left)	0.709 (0.332, 1.514)	0.375
Preoperative eGFR	0.993 (0.968, 1.018)	0.576	0.985 (0.957, 1.015)	0.323
RENAL score	0.661 (0.484, 0.902)	0.009	0.629 (0.456, 0.869)	0.005
Surgical approach (retros vs trans)	1.157 (0.516, 2.596)	0.723
Surgical type (RAPN vs LPN)	1.251 (0.584, 2.679)	0.564	1.408 (0.627, 3.161)	0.407

CI = confidence interval; OR = odds ratio.

Discussion

With the progress of surgical techniques and the improvement of the biological understanding of renal malignant tumors, partial nephrectomy and minimally invasive techniques have been applied more often.¹⁹ The completely endophytic renal tumor, represents a kind of highly complex mass, which places huge difficulties and challenges for nephron-sparing procedure. Owing to the development of minimally invasive techniques, many institutions have described the feasibility and safety of LPN and RAPN for managing this type of renal masses.^{5

–11,20} Despite the comparison between LPN and RAPN for kidney cancer been well researched, for subgroup of completely endophytic tumors, the relevant data remain demanding.

This study directly compared the perioperative, functional, and oncologic results of RAPN and LPN for completely endophytic masses. First, the baseline features between the two groups were compared. We found that year of treatment differed significantly between RAPN and LPN (p < 0.001). RAPN was increasingly performed every year; however, the number of LPN was stable. The difference was mainly caused by the development trend of minimally invasive techniques. The other variables were similar between RAPN and LPN. Hence, there was a good comparability between the two groups.

Although the benefits of robotic procedure have been proven by many studies,²¹ according to our results, RAPN seems to have no significant advantages compared with LPN as for perioperative, functional, and oncologic results. The detailed outcomes contained operating time, blood loss, ischemia time, positive surgical margin, postoperative hospital stay, rate of postoperative complications, tumor histology, pathology stage, Fuhrman grade, and tumor necrosis, change of eGFR. In our study, all surgical procedures were conducted by skilled, high-volume surgeons. Experience with the technique may make the advantages of robotic surgical equipment inconspicuous. Moreover, although belonging to completely endophytic renal tumors, some of them are just close to the renal cortical surface. After tumor identification, the partial nephrectomy for them seems to be not so difficult. However, because of the expensive surgical instruments, the direct cost was higher for patients undergoing RAPN, which is consistent with previous literatures.^22,23

The perioperative, functional, and oncologic outcomes in our study were excellent and similar to other cohorts. We have previously validated the predictive role of ABC scoring system in minimally invasive partial nephrectomy.²⁴ The reported outcomes were similar to those of this study. For most of endophytic renal tumors, after identifying tumor margins, the difficulty of the operation is comparable with that of conventional partial nephrectomy. Hence, the results were relatively understandable. Histopathological examination revealed that most patients had malignant tumors. Most tumors were pT1a, Fuhrman grade 1 to 2, without tumor necrosis, which means most of them were low-stage and low-risk tumors. Owing to the small masses and short ischemia time, the decline of renal function was acceptable at 1-year follow-up. After the operation, during the follow-up, no local recurrence and distant metastasis appeared in these patients of two approaches. The oncologic outcomes were similar to previous literatures.^2,3

Recently, many outcome achievements were applied to assess the surgical outcomes of nephron-sparing nephrectomy. The most widely used were MIC, trifecta and pentafecta achievement. Among them, pentafecta achievement takes more elements into account, which represents the most comprehensive evaluation system. Therefore, pentafecta achievement and the five components were also examined between the two groups. Because the perioperative and functional outcomes were similar between the two groups, no significant difference was identified for each component. Moreover, rates of pentafecta achievement were comparable between RAPN and LPN (42.6% vs 37.3%, p = 0.564). Univariable and multivariable analyses identified that only RENAL score (OR = 0.629, 95% CI = 0.456, 0.869, p = 0.005) was an independent predictor for postoperative pentafecta achievement. The surgical approach was not a significant predictor for postoperative pentafecta achievement. Several studies have investigated the factor predicting pentafecta achievement after RAPN. Kang and colleagues²⁵ have retrospectively analyzed the data from 362 patients, and identified that preoperative eGFR, hypertension, and tumor size were independently correlated with the pentafecta achievement. Stroup et al.²⁶ have compared surgical outcomes between transperitoneal RAPN and retroperitoneal RAPN. Their results indicated that RENAL score and baseline eGFR were independently associated with pentafecta achievement. Castellucci and colleagues²⁷ have retrospectively analyzed 123 patients from single-center database, and discovered that only age was the factor predicting pentafecta achievement, but not the PADUA score and preoperative eGFR. Different inclusion criteria, study population, and analysis variables may partly explain the inconsistent results.

Because of the wide use and significant benefits of robotic operation, indications for RAPN and LPN seem to be the current research focus. Our results showed that both these two approaches can achieve excellent and comparable results in the field of perioperative, functional, and oncologic results for completely endophytic renal tumors. However, the direct cost was higher for patients undergoing RAPN. During clinical work, the choice to use LPN or RAPN is complex. For patients with completely endophytic tumors, selection of surgical approach should be in the light of relevant experience and preference of surgeon with either surgical approach.

There are several limitations for this study. First, this is a retrospective comparative study with small sample size. Although most variables were comparable between these two groups, RAPN were performed more recently because of the development trend of minimally invasive techniques. Potential selection biases or confounders may affect the results. Second, all the procedures were performed by experienced doctors. An inexperienced doctor should interpret these results with caution. For inexperienced doctors, it may be easier to perform partial nephrectomy for completely endophytic renal tumors with robotic surgical system. Despite these limitations, our study represents one of the largest cohorts about minimally invasive nephron-sparing nephrectomy for intrarenal masses, and initially compared the perioperative, functional and oncologic results between RAPN and LPN.

In summary, for patients with completely intrarenal masses, RAPN and LPN could provide excellent and comparable results in the field of perioperative, functional, and oncologic outcomes. However, the direct cost was much higher for patients undergoing RAPN. Both procedure techniques remain viable options in the management of these cases. Selection of surgical approach should be in the light of relevant experience and preference of surgeon with either surgical approach.

Footnotes

Author Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

Abbreviations Used

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