Predictive Factors for Achieving Superior Pentafecta Outcomes Following Robot-Assisted Partial Nephrectomy in Patients with Localized Renal Cell Carcinoma

Abstract

Purpose:

To examine the perioperative outcomes following robot-assisted partial nephrectomy (RAPN) in patients with localized renal cell carcinoma (RCC) and to identify the predictors of Pentafecta achievement following RAPN.

Materials and Methods:

We retrospectively analyzed the data from 362 patients with RCC who underwent RAPN from 2008 to 2016. The criteria for Pentafecta achievement were defined as the Trifecta [warm ischemic time (WIT) ≤25 minutes, negative surgical margin, and no significant perioperative complications]; with the addition of renal function preservation, including over 90% preservation of the estimated glomerular filtration rate (e-GFR); and no stage upgrade of chronic kidney disease at 1 year after surgery. Multivariate logistic regression analysis was performed to determine the predictors of the Pentafecta outcomes.

Results:

Among 362 patients, 82.3% (n = 298) had clinical T1a tumors. The median tumor size was 2.9 cm [interquartile range (IQR) = 2.1–3.6] and median nephrometry score was 7 (IQR = 6–8). The median operative time was 220 minutes (IQR = 185–270) and median estimated blood loss was 150 mL (IQR = 100–200). The median WIT was 20 minutes (IQR = 16–26). The overall rate of postoperative complications was 18.8% (n = 68). The rates of Trifecta and Pentafecta achievement were 66.6% (n = 241/362) and 33.9% (n = 121/303), respectively. Notably, the preoperative e-GFR, hypertension, tumor size, L-component of the R.E.N.A.L score, and surgeon's experience were identified as the significant predictors of Pentafecta achievement. Additionally, patients with T1a tumors showed higher rates of Pentafecta achievement (45.7% vs 25.9%) compared with those of patients with T1b tumors. However, there was no significant difference in the Pentafecta accomplishment rates between the transperitoneal and retroperitoneal approaches.

Conclusions:

In summary, our data highlighted that tumor size and nephrometry score, which are tumor-related factors, as well as the surgeon's experience, a surgeon-related factor, appear to be the critical predictive factors for Pentafecta achievement following RAPN.

Introduction

Small renal masses (SRM) are more frequently detected due to the recent advancements in and frequent use of imaging modalities over the past few decades.¹ Nephron-sparing surgery has been recently considered an optimal therapeutic approach for SRM, such as localized T1a or T1b tumors, due to similar oncological outcomes and better preservation of kidney function as compared with radical nephrectomy (RN).² Particularly, recent meta-analyses have revealed that robot-assisted partial nephrectomy (RAPN) offers more favorable perioperative outcomes than those of conventional laparoscopic partial nephrectomy, including a lower conversion rate to RN, shorter duration of hospital stay, and shorter warm ischemic time (WIT).^3

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Considering the increase in the incidence of treating SRM with RAPN, the concept of Trifecta was introduced to assess the surgical outcomes of partial nephrectomy (PN), which was defined as a combination of a negative surgical margin, WIT ≤25 minutes, and no perioperative complications.⁸ More recently, the “Pentafecta” concept was suggested by Zargar and colleagues⁹ as the condition of Trifecta achievement in addition to the preservation of estimated glomerular filtration rate (e-GFR) over 90% and no upgrading of chronic kidney disease (CKD) stage at 1 year after surgery. To improve the perioperative outcomes following RAPN, it is crucial to select the appropriate candidates for RAPN and to accurately predict the surgical outcomes by using these standardized concepts.

Despite the clinical usefulness of the Pentafecta criteria, which aim for cancer control and the functional preservation of the kidney, very few data have been reported on patients with localized renal cell carcinoma (RCC) who underwent RAPN. In this study, we aimed to evaluate the Pentafecta outcomes following RAPN, and to identify the independent predictors of Pentafecta achievement.

Materials and Methods

Study population

We retrospectively reviewed the electronic medical records of 391 consecutive patients with localized RCC undergoing RAPN by a single surgeon (S.I.S.) between December 2008 and February 2016 at Samsung Medical Center. Among these patients, 29 patients with bilateral disease, ipsilateral multiple tumors, benign tumors in final pathological reports, or incomplete data were excluded. Ultimately, the data of 362 patients with a single and localized unilateral RCC were analyzed. The current study was approved by the Institutional Review Board of our institution, and written informed consent was not required due to the retrospective nature of this study.

Study design

Preoperatively, we performed routine laboratory tests and radiological evaluation for SRM using computed tomography or magnetic resonance imaging to determine the location, size, and characteristics of the tumors. RAPN was performed using the da Vinci Surgical System (Intuitive Surgical, Sunnyvale, CA) through the transperitoneal or retroperitoneal approach using surgical techniques in accordance with the standard protocol at our institution, as described elsewhere.¹⁰ We collected and evaluated data of the following clinicopathological variables: age at surgery, sex, the American Society of Anesthesiologists (ASA) classification, body mass index (BMI), tumor size and laterality, the R.E.N.A.L (radius, exophytic/endophytic properties, nearness of tumor to the collecting system or sinus in millimeters, anterior/posterior location relative to polar lines) nephrometry score as a standardized and quantifiable tool to evaluate renal tumors,¹¹ kidney function as measured by e-GFRs at baseline and postoperative 1 year, the presence and degree of CKD at baseline and postoperative 1 year, operative time and console time, estimated blood loss (EBL), WIT, and length of hospital stay. Postoperative complications were also examined and classified by the Clavien–Dindo classification.^12,13 For assessing R.E.N.A.L scores for surgery, two urologists (Drs. Gong and Seo) prospectively measured and recorded the R.E.N.A.L scores at the time of surgery, and another urologist (Dr. Kang) retrospectively reviewed and confirmed the previously measured scores.

With regard to the surgeon's experiences, we classified the overall study population into four groups according to the case number, including “less than 100,” “100 to 200,” “200 to 300,” and “more than 300 cases.” Supplementary Figure S1 (Supplementary Data are available online at www.liebertpub.com/end) represents the patterns of clinical outcomes, such as operative time, WIT, and EBL according to the groups of case numbers, indicating the surgeon's experiences indirectly. The primary endpoint of this study was Pentafecta achievement, which was defined as Trifecta achievement (WIT ≤25 minutes, negative surgical margin, and no significant perioperative complications (Clavien–Dindo grade ≥2) as the secondary endpoint in addition to the preservation of kidney function (e-GFR >90%) and no stage upgrade of CKD (up to CKD stages III–V) at postoperative 1 year.^8,9 Additionally, to examine the oncological outcomes after RAPN, we evaluated tumor recurrence and distant metastasis, as well as cancer-specific and all-cause mortalities during the follow-up periods.

Statistical analysis

Descriptive results are presented as median values with interquartile range (IQR) for continuous variables and as the proportion of events (%) for categorical variables. For the comparison of the values between the two groups, the Mann–Whitney U test was used for continuous variables and the Chi-square test was applied for categorical variables. To determine the independent predictors of the Trifecta and Pentafecta outcomes, we performed multivariate logistic regression analysis by adjusting for other clinicopathological variables. A two-sided p-value <0.05 was considered statistically significant. Statistical analysis was conducted using the IBM SPSS version 23 statistical package (SPSS, Inc., Chicago, IL).

Results

Table 1 presents the baseline demographics of the 362 patients with localized RCC who underwent RAPN. A total of 82.3% of patients had clinical T1a tumors (n = 298), whereas 17.4% (n = 63) and 0.3% (n = 1) of patients had clinical T1b and T2a tumors, respectively. The median tumor size was 2.9 cm (0.7–9.4) and the median R.E.N.A.L score was 7 (IQR = 6–8). Notably, ∼60% and 40% of patients had exophytic and entirely endophytic tumors, respectively. The median follow-up duration was 24.7 months. Although there was no local recurrence and no all-cause or cancer-specific mortalities during the study periods, distant metastasis occurred in two patients at 12 and 14 months after surgery. One patient had solitary lung metastasis and the other had multiple bone and lung metastases.

Table 1.

Baseline Characteristics of the Patients in the Present Study

Variables	N = 362
Age, years (median, IQR)	50 (42–58)
Sex, n (%)
Male	256 (70.7)
Female	106 (29.3)
BMI (kg/m²) (median, IQR)	25 (23–27)
Preoperative e-GFR (median, IQR)	85.7 (75.8–94.0)
Hypertension, n (%)	106 (29.3)
Diabetes, n (%)	49 (13.5)
Tumor size, cm (median, IQR)	2.9 (2.1–3.6)
R.E.N.A.L score (median, IQR)	7 (6–8)
Laterality, n (%)
Right	182 (50.3)
Left	180 (49.7)
Exophytic rate, n (%)
≥50% exophytic	140 (38.7)
<50% exophytic	85 (23.5)
Entire endophytic	137 (37.8)
ASA grade, n (%)
1	165 (45.6)
2	193 (53.3)
3	4 (1.1)
Clinical stage, n (%)
T1a	298 (82.3)
T1b	63 (17.4)
T2a	1 (0.3)
Histopathology, n (%)
Clear cell RCC	306 (84.5)
Papillary RCC	24 (6.6)
Chromophobe RCC	25 (6.9)
Other	7 (2.0)

ASA = American Society of Anesthesiologists; BMI = body mass index; e-GFR = estimated glomerular filtration rate; IQR = interquartile range; RCC = renal cell carcinoma.

Peri- and postoperative outcomes are summarized in Table 2. The transperitoneal and retroperitoneal approaches were adopted as similar rates (53.6% vs 46.4%, respectively). The median operative time was 220 minutes (IQR = 185–270) and median EBL was 150 mL (IQR = 100–200). The median WIT was 20 minutes (IQR = 16–26). While the overall rate of postoperative complications was 18.8% (n = 68), only 1.4% of patients (n = 5) experienced grade 3 complications, such as urine leakage (n = 3) and postoperative bleeding (n = 2). The rate of Trifecta achievement was 66.6% (n = 241). Of note, ∼50% of patients with Trifecta failure had prolonged WIT of more than 25 minutes. Among a total of 362 patients, the Pentafecta outcomes of 303 patients were ultimately assessed and the rate of Pentafecta achievement was 39.9% (n = 121). The CKD status of 25 patients (6.9%) eventually deteriorated to CKD stage III (n = 22), stage IV (n = 2), and stage V (n = 1), respectively.

Table 2.

Peri- and Postoperative Outcomes of Robot-Assisted Partial Nephrectomy

Variables
Approach, n (%)
Transperitoneal	194 (53.6)
Retroperitoneal	168 (46.4)
Intraoperative outcomes (median, IQR)
Operative time, minutes	220 (185–270)
WIT, minutes	20 (16–26)
EBL, mL	150 (100–200)
Intraoperative complications, n (%)
Blood transfusion	2 (0.5)
Ureteric injury	1 (0.3)
Bowel injury	1 (0.3)
Liver injury	1 (0.3)
Conversion to RN	2 (0.6)
Open conversion	0
Hospital stay, days (median, IQR)	7 (7–8)
Postoperative complication, n (%)
Grade 1	44 (12.2)
Grade 2	19 (5.2)
Grade 3	5 (1.4)
Grade 4	0
Trifecta achievement, n (%)
Yes	241 (66.6)
No	121 (33.4)
Cause of Trifecta failure, n (%)
PSM	0
WIT >25 minutes	103 (28.5)
Complications ≥ grade 2	28 (7.7)
Pentafecta achievement, n (%)
Yes	121 (39.9)
No	182 (60.1)
90% e-GFR preservation, n (%)	208 (57.5)
Upstaging to CKD III–V, n (%)	25 (6.9)

CKD = chronic kidney disease; EBL = estimated blood loss; PSM = positive surgical margin; WIT = warm ischemic time.

Interestingly, when we examined the peri- and postoperative outcomes according to tumor stage (T1a vs T1b), patients with T1a tumors showed higher rates of Trifecta (71.3% vs 51.7%) and Pentafecta achievement (45.7% vs 25.9%), respectively, compared with those of patients with T1b tumors (Table 3). In T1b cases, a longer operative time and increased WIT was observed compared with those in T1a cases. Of note, the proportion of WIT >25 minutes was significantly higher in patients with T1b tumors than in those with T1a tumors (44.8% vs 23.2%). Additionally, we compared the results of the Trifecta and Pentafecta outcomes according to the approach methods, and found that there were no significant differences between the transperitoneal and retroperitoneal approaches (data not shown).

Table 3.

Peri- and Postoperative Outcomes of T1a vs T1b Tumors

Variables	T1a (N = 164)	T1b (N = 58)	p
Intraoperative outcomes (mean, SD)
Operative times, minutes	232.3 ± 66.5	266.8 ± 86.4	0.002
WIT, minutes	20.7 ± 8.1	25.6 ± 9.1	<0.001
EBL, mL	167.1 ± 153.4	213.6 ± 175.7	0.057
Median LOS, days (IQR)	7 (7–8)	7 (7–8)	0.599
Trifecta achievement, n (%)			0.007
Yes	117 (71.3)	30 (51.7)
No	47 (28.7)	28 (48.3)
Cause of Trifecta failure, n (%)
PSM	0	0
WIT >25 minutes	38 (23.2)	26 (44.8)	0.002
Complications ≥ grade 2	37 (22.6)	14 (24.1)	0.806
Pentafecta achievement, n (%)			0.008
Yes	75 (45.7)	15 (25.9)
No	89 (54.3)	43 (74.1)
90% e-GFR preservation, n (%)	94 (57.3)	27 (46.6)	0.157
Upstaging to CKD III–V, n (%)	8 (4.9)	6 (10.3)	0.204

LOS = length of hospital stay; SD = standard deviation.

Finally, we performed multivariate logistic regression analysis to identify the predictive factors for Trifecta and Pentafecta achievement following RAPN (Table 4). For the Trifecta achievement, tumor size, endophytic property (E-component in R.E.N.A.L score), tumor location relative to polar line (L-component in R.E.N.A.L score), and the surgeon's experience were found to be the independent predictors. More importantly, preoperative e-GFR, hypertension, tumor size, tumor location relative to polar line, and the surgeon's experience were identified as the significant predictors of Pentafecta achievement.

Table 4.

Multivariate Logistic Regression Analysis to Identify the Predictive Factors for Trifecta and Pentafecta Achievement Following Robot-Assisted Partial Nephrectomy

Variables	OR	Trifecta 95% CI	p	OR	Pentafecta 95% CI	p
BMI (kg/m²)	1.08	0.99, 1.17	0.078	1.09	0.99, 1.19	0.068
Preoperative e-GFR				0.98	0.96, 0.99	0.029
Hypertension				0.53	0.29, 0.97	0.042
Tumor size (cm)	0.48	0.37, 0.63	<0.001	0.51	0.39, 0.66	<0.001
R.E.N.A.L score
E–component
1	Reference
2	0.34	0.16, 0.71	0.004
3	0.28	0.14, 0.58	0.001
N-component
1	Reference
2	1.74	0.87, 3.45	0.114
3	0.78	0.39, 1.55	0.480
L-component
1	Reference			Reference
2	0.48	0.23, 0.99	0.049	0.97	0.50, 1.88	0.934
3	0.25	0.12, 0.53	<0.001	0.41	0.21, 0.79	0.008
No. of cases
<100	Reference			Reference
100–200	7.75	3.56, 16.87	<0.001	4.78	2.35, 9.72	<0.001
200–300	8.78	4.12, 18.71	<0.001	6.89	3.40, 13.93	<0.001
>300	6.01	2.51, 14.37	<0.001	13.83	0.83, 229.89	0.067

CI = confidence interval; OR = odds ratio.

Discussion

Since the Trifecta assessment for evaluating the perioperative results of RAPN has a few drawbacks, the Pentafecta concept has been recently introduced as a new and more comprehensive method for reporting outcomes in RAPN by modifying the basic Trifecta criteria.⁹ Although the Pentafecta is superior to the Trifecta for the assessment of functional and oncological outcomes, only two studies have reported on Pentafecta outcomes after RAPN.^9,14 In this context, the present study provides valuable data on the peri- and postoperative outcomes of RAPN, particularly in terms of Pentafecta achievement, by analyzing 362 consecutive patients. Notably, the rate of Pentafecta achievement was ∼40%, whereas the rate of Trifecta achievement was 67%. More importantly, we identified preoperative e-GFR, the presence of hypertension, tumor size, L-score component (location relative to polar line), and the surgeon's experience as the critical predictors of Pentafecta achievement following RAPN after adjusting for various clinical factors.

Likewise, Zargar and colleagues⁹ reviewed 2892 consecutive cases of RAPN from 5 tertiary centers, and finally analyzed 670 patients with complete functional data. In that study, the rate of Pentafecta achievement was 38.5% (n = 258), and the significant predictors of Pentafecta success were the tumor size, Charlson comorbidity index, EBL, and preoperative e-GFR in multivariate analysis. In particular, for a 1-cm increase in tumor size, the risk of Pentafecta failure rose about 32% [odds ratio (OR) = 0.68; 95% confidence interval = 0.53, 0.88]. Kim and colleagues¹⁴ also reported that the Pentafecta was achieved in 38.3% (n = 23) and 26.7% (n = 16) of patients with T1a and T1b tumors, respectively, in a propensity score-matched cohort of 120 patients. Interestingly, only the R.E.N.A.L score (OR = 0.80), and the L-component (OR = 0.63) in particular, persisted as an independent predictor of Pentafecta achievement. While the rates of Pentafecta achievement were similar between studies, ranging from 38% to 40%, the predictive factors for Pentafecta success were not consistent.

Interestingly, we found that a WIT of more than 25 minutes was observed as the most frequent cause of Pentafecta failure. Thompson and colleagues showed that WIT < 25 minutes was significantly associated with the incidence of stage IV CKD development.¹⁵ Lane and colleagues also reported that a WIT of more than 25 minutes affected the incidence of stage IV CKD following PN.¹⁶ More importantly, a recent collaborative review of the literature, including 91 studies, suggested that WIT was significantly correlated with the volume of residual functional parenchyma following nephron-sparing surgery and, therefore, prolonged WITs more than 25 minutes should be avoided during PN.¹⁷ Hence, we believe that preoperative selection of appropriate candidates for RAPN, such as patients with a smaller tumor size, lower R.E.N.A.L score, and better kidney function, may be the most crucial factor in reducing the WIT during RAPN, along with the higher level of expertise of the surgeon.

One of the key findings of the present study was that both the tumor-related factors (tumor size and L-component in the R.E.N.A.L score) and the surgeon-related factor (number of cases) were shown to be the independent predictors of Pentafecta achievement, in addition to the Trifecta outcomes. Although the study by Kim and colleagues¹⁴ demonstrated comparable Pentafecta outcomes between T1a and T1b tumors, in our data, the Trifecta and Pentafecta achievement rates were remarkably lower in T1b tumors compared with T1a tumors (51.7% vs 71.3% for Trifecta; 25.9% vs 45.7% for Pentafecta, respectively). Moreover, T1b cases showed longer operative times and WIT compared with the T1a cases. Paulucci and colleagues¹⁸ reported that a surgeon's experience was significantly associated with an increased rate of successful Trifecta achievement, less EBL, fewer transfusions, lower WIT, and a shorter duration of hospital stay in an analysis of a total of 960 cases of RAPN. The authors highlighted the continuous refinement of perioperative outcomes beyond the initial learning curve of RAPN.¹⁸ Taken together, surgeons should pay more attention to the larger and centrally located tumors in the performance of RAPN, particularly the less experienced surgeons, to achieve superior Trifecta and Pentafecta outcomes.

We should acknowledge the several limitations in this study. First, there was an unavoidable selection bias due to the retrospective nature of this study. Second, although we adjusted various clinical variables by conducting multivariate analysis, there are still additional potential confounding factors associated with patient-related variables, such as racial differences, performance status, and the amounts of visceral fat that could be influencing the Pentafecta outcomes of RAPN. In this context, the study population enrolled is likely not fully representative of those in Western countries. For example, ∼50% of our patients had a normal BMI, and the median BMI of the overall population was 25. Additionally, most patients had a good performance status (ASA 0 or 1). These favorable baseline characteristics can affect the achievement of Trifecta/Pentafecta following RAPN. Third, since our data were collected from a single tertiary center, a relatively small sample size was another pitfall of our study. Finally, although we compared the surgical outcomes, such as operative time, WIT, and EBL, according to the case numbers to reduce intraobserver variations, we analyzed only a single surgeon's data at our institution. Thus, interobserver variations should be validated in the future by comparing the outcomes between different surgeons having different surgical experiences. Accordingly, further concrete evidence can be accumulated by internal and external validation studies to confirm our findings. Nevertheless, the current study augments the existing limited evidence of Pentafecta outcomes and its predictive factors after RAPN in patients with RCC.

Conclusions

In summary, the present study showed that the rate of Pentafecta achievement was ∼40%, which was comparable to that shown in previous reports. Additionally, the achievement rate of Pentafecta was higher in cases of T1a tumors than that in cases of T1b tumors, but no significant difference was found between the transperitoneal and retroperitoneal approaches. Finally, multivariate analysis revealed that the predictors of Pentafecta achievement were preoperative e-GFR, the presence of hypertension, tumor size, L-score component, and surgeon's experience. Our data provide valuable information on the outcomes after RAPN and highlight the factors involved in Pentafecta achievement as well as its predictive factors.

Footnotes

Acknowledgments

This work was supported by a research grant from the National Research Foundation (NRF) of Korea funded by the Ministry of Science, ICT & Future Planning (MSIP) (Grant No. 2017R1A2B4010568). This research was also supported by a grant of the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea (Grant No. HI17C0025).

Author Disclosure Statement

No competing financial interests exist.

Abbreviations Used

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