Trifecta and Pentafecta Outcomes in Laparoscopic and Robotic Nephron-Sparing Surgery for Highly Complex Renal Tumors: A Propensity Score-Matched Cohort Analysis

Abstract

Purpose:

To compare the trifecta and pentafecta outcomes of laparoscopic partial nephrectomy (LPN) and robotic partial nephrectomy (RPN) in highly complex renal tumors (RENAL nephrometry score ≥10) using a matched cohort analysis.

Methods:

Patients undergoing LPN or RPN for renal tumors with RENAL score ≥10 between January 2014 and December 2019 were matched using 1:2 propensity score match analysis based on age, body mass index, gender, laterality of tumor, RENAL score, and American Society of Anesthesiologists (ASA) score. The two groups were compared for trifecta and pentafecta outcomes.

Results:

Thirty patients undergoing LPN (Group A) were matched with 60 patients undergoing RPN (Group B). The mean age (standard deviation) was 53.7 (12.9) years. The median (interquartile range) RENAL score was 10 (10–11). In comparison, the mean warm ischemia time in Group A was significantly longer than that in Group B (26.2 vs 23.0 minutes, p = 0.013). The overall complication rate was 36.7% in Group A as compared with 20% in Group B (p = 0.440). The trifecta outcomes could be achieved in 11 patients (36.7%) in Group A compared with 40 patients (66.7%) in Group B (p = 0.012). Moreover, 10 patients (33.3%) in Group A and 28 patients (46.7%) in Group B achieved pentafecta outcomes (p = 0.227).

Conclusions:

In a matched cohort of patients undergoing nephron-sparing surgery for highly complex renal tumors (RENAL score ≥10), the robotic approach offers a superior advantage in the achievement of trifecta outcomes as compared with the laparoscopic approach. However, both LPN and RPN can achieve similar pentafecta outcomes.

Introduction

Nephron-sparing surgery (NSS) currently represents the standard of care for patients with renal masses ≤4 cm and for patients with renal masses ≥4 cm, when technically feasible.¹ The minimally invasive surgery for partial nephrectomy initially began for small renal masses but gradually expanded to complex renal tumors.² Both laparoscopic partial nephrectomy (LPN) and robotic partial nephrectomy (RPN) are popular for nephron preservation. LPN involves certain technical challenges because of intracorporeal suturing skills and increased warm ischemia time (WIT).³ The robotic platform with wristed instrumentation and three-dimensional magnified vision has allowed RPN to overcome the technical challenges in NSS and expand the arena of minimally invasive surgery to more complex and difficult renal tumors.⁴

Variable scoring systems have been used to stratify renal masses for the complexity of resection, however, RENAL nephrometry score is commonly used with RENAL score ≥10 defined as highly complex renal tumors.⁵ Few studies have reported outcomes of LPN and RPN in highly complex RENAL tumors (i.e., RENAL score ≥10).^3,6 However, reporting of these outcomes with baseline differences in these patients leads to high heterogeneity and difficult interpretation of results. Hung et al. first described the term “Trifecta” as a surrogate for effective partial nephrectomy.⁷ The “trifecta” outcomes included achievement of no complications, negative surgical margins, and WIT <25 minutes.

This concept was further expanded to “optimal” or “pentafecta” outcomes with the addition of 90% estimated glomerular filtration rate (eGFR) preservation and no chronic kidney disease (CKD) stage upgrading.⁸ The introduction of “trifecta” and “pentafecta” outcomes allowed systematic assessment of perioperative and long-term outcomes of NSS, which becomes more pertinent when increasingly complex renal tumors are being managed with minimal invasive NSS. In this study, we aim to compare the “trifecta” and “pentafecta” outcomes of patients with highly complex renal tumors (RENAL score ≥10) undergoing LPN or RPN using matched cohort analysis.

Materials and Methods

In an IRB-approved study (Ref No: TS/MSSH/DDF/SKT-2/EC/Uro/19-25), a retrospective analysis of a prospectively maintained database of patients undergoing LPN or RPN by a single surgeon between January 2014 and December 2019 at our institute was conducted. All patients underwent standard preoperative work-up along with cross-sectional imaging: contrast-enhanced computed tomography if the renal function was normal otherwise magnetic resonance imaging. RENAL nephrometry score was used to study tumor complexity on imaging.⁵ All patients who underwent LPN or RPN with a RENAL score ≥10 were included. Partial nephrectomy in all the patients included in the study was done as an elective indication.

Patients with renal tumors in solitary kidney or bilateral renal tumors undergoing partial nephrectomy were excluded. The senior surgeon had extensive experience in both laparoscopy and robotic surgery and the choice of surgery was based on patients' preferences because of financial constraints as robotic surgery poses a high financial burden for the patient. For LPN and RPN, a transperitoneal approach was used. The method of hilar control was consistent in both LPN and RPN groups. The renal artery was clamped in all cases and renal vein was separately clamped using bulldog clamps.

Renorraphy was performed in all cases in a similar manner and bolster was used if the defect was large as per the surgeon's discretion. Initially, a two-layer sliding renorraphy using a continuous 3-0 Vicryl or 3-0 V-loc suture for the inner layer and 2-0 Vicryl or 2-0 V-loc for the outer layer with Hem-o-lock clips were used. For the past 4 years, we have switched to 3-0 polydioxanone (PDS) for inner renorraphy and to 2-0 for outer renorraphy. PDS sutures are easier to pull at the end and can be tightened from both ends.

Preoperative data including demographics and tumor characteristics (Table 1) were recorded for all patients. eGFR was calculated from serum creatinine using the modification of diet in renal disease (MDRD) study equation and CKD was defined as eGFR <60 mL/min.⁹ Postoperative complications were identified within 30 days of surgery and complications were recorded as per the Clavien–Dindo scale.¹⁰

Table 1.

Comparison of Demographic and Tumor Characteristics of Patients Undergoing Laparoscopic Partial Nephrectomy (Group A) vs Robot-Assisted Partial Nephrectomy (Group B)

Parameter	Group A (n = 30)	Group B (n = 60)	p
Mean age, (SD), years	53.9 (15.3)	53.7 (11.6)	0.936
Gender (M/F), n	23 (76.7%)/07 (23.3%)	46 (76.7%)/14 (23.3%)	0.999
Mean body mass index, (SD), kg/m²	27.0 (2.6)	26.8 (4.0)	0.819
Laterality, n (%)			0.999
Right	14 (46.7%)	28 (46.7%)
Left	16 (53.3%)	32 (53.3%)
Median ASA score, (IQR)	1.5 (1–3)	1.5 (1–3)	0.999
Median tumor size, (IQR), cm	6.1 (4.9–7.6)	6.2 (4.5–7.9)	0.402
Median RENAL score, (IQR)	10 (10–11)	10 (10–11)	0.999
RENAL score, n (%)			0.999
10	19 (63.4%)	38 (63.4%)
11	10 (33.3%)	20 (33.3%)
12	1 (3.3%)	2 (3.3%)
Mean preoperative creatinine, (SD), mg/dL	1.03 (0.18)	1.01 (0.25)	0.521
Mean preoperative eGFR, (SD), mL/min per 1.73 m²	87.1 (21.2)	84.1 (20.7)	0.536

ASA = American Society of Anesthesiologists; eGFR = estimated glomerular filtration; IQR = interquartile range; SD = standard deviation.

All patients were categorized into the LPN group and RPN group. Using 1:2 propensity score match analysis, patients of LPN group (Group A) were matched with patients of the RPN group (Group B) in age, body mass index (BMI), gender, laterality of tumor, RENAL score, and American Society of Anesthesiologists (ASA) score. The two groups were compared for operative parameters, oncologic and functional outcomes in terms of trifecta, and pentafecta outcomes.

Trifecta outcomes were defined as achievement of no complications, negative surgical margins, and WIT <25 minutes.⁷ Pentafecta outcomes were defined as trifecta outcomes in addition to 90% eGFR preservation and no CKD stage upgrading.⁸ The preservation of eGFR was defined as a percentage ratio of postoperative eGFR to preoperative eGFR, 12 months after the surgery. CKD upstaging was defined as upstaging of CKD status to stage III, IV, or V. Upstaging from CKD stage I to CKD stage II was not clinically significant and, hence, was not used in the criteria.⁸

Statistical analysis

Continuous variables are expressed as mean ± standard deviation (SD) or median (interquartile range [IQR]) as appropriate. Categorical variables were compared using the chi-square test and continuous variables were compared using Student's t-test, multiple analysis of variance (ANOVA), Mann–Whitney test, or Kruskal–Wallis test as appropriate. To match baseline characteristics in the two groups, 1:2 propensity score matching was done.

The propensity score was calculated for each patient using a multivariable logistic regression model based on age, BMI, gender, laterality of tumor, RENAL score, and ASA score. A 1:2 matching was used for optimal estimation of treatment effect with improved precision. Subgroup analysis was then performed. All statistical tests were two sided. Statistical significance was taken as p < 0.05. Data were analyzed using IBM SPSS Statistics software (version 20.0, Chicago, IL).

Results

Of 211 patients who underwent minimally invasive surgery (LPN or RPN) during the study period, 99 patients who had RENAL scores ≥10 were screened. Of them, 33 patients underwent LPN whereas 66 patients underwent RPN. Thirty patients of the LPN group (Group A) were matched to 60 patients of the RPN group (Group B) using 1:2 propensity score matching.

The mean (SD) age of the study population was 53.7 (12.9) years and was similar in both groups (Table 1). The baseline clinical factors and tumor characteristics including RENAL score are mentioned in Table 1. Among the perioperative complications, 11 patients (36.7%) in Group A and 12 patients (20%) in Group B suffered from perioperative complications (p = 0.440) (Table 2). Three patients (10%) in group A and two patients (3.3%) in group B received postoperative blood transfusion (Grade II). The major postoperative complications (defined as Clavien–Dindo Grade III or more) occurred in five (16.7%) patients in group A and four (6.7%) patients in group B (p = 0.136).

Table 2.

Comparison of Perioperative Outcomes of Patients Undergoing Laparoscopic Partial Nephrectomy (Group A) vs Robot-Assisted Partial nephrectomy (Group B)

Parameter	Group A (n = 30)	Group B (n = 60)	p
Mean operative time, (±SD), (minutes)	228.5 (37.3)	204.5 (32.9)	0.002^*
Median blood loss (IQR), mL	200 (150–300)	150 (100–200)	0.046^*
Mean WIT, (±SD), (minutes)	26.2 (5.7)	22.0 (5.5)	0.013^*
Median postoperative day 1 drain output (IQR), mL	100 (80–200)	115 (100–175)	0.875
Mean hospital stay (SD), days	4.2 (1.6)	3.6 (1.4)	0.073
Clavien–Dindo complications, n (%)			0.440
Grade I	3 (10%)	6 (10%)
Grade II	3 (10%)	2 (3.3%)
Grade III	3 (10%)	2 (3.3%)
Grade IV	2 (6.7%)	2 (3.3%)
Pathologic T stage, n (%)			0.625
pT1a	1 (3.3%)	6 (10%)
pT1b	25 (83.3%)	45 (75%)
pT2a	3 (10%)	8 (13.3%)
pT2b	1 (3.3%)	1 (1.7%)
Tumor histology, n (%)			0.901
Clear cell carcinoma	24 (80%)	52 (86.7%)
Papillary carcinoma	2 (6.7%)	5 (8.3%)
Chromophobe carcinoma	1 (3.3%)	1 (1.7%)
Cystic RCC	1 (3.3%)	0
Mixed epithelial stromal tumor	1 (3.3%)	1 (1.7%)
Benign	1 (3.3%)	1 (1.7%)
Margin positive	2 (6.7%)	0 (0%)	<0.001^*
Fuhrman grade	n = 26	n = 57	0.602
Grade 1, n (%)	5 (19.2%)	12 (21.1%)
Grade 2, n (%)	16 (61.5%)	38 (66.7%)
Grade 3, n (%)	3 (11.5%)	6 (10.5%)
Grade 4, n (%)	2 (7.7%)	1 (1.7%)

^*p < 0.05 is considered significant.

RCC = renal cell carcinoma; WIT = warm ischemia time.

In major complications in group A, one patient (3.3%) underwent Double-J stenting for suspected urinoma (Grade IIIA), two patients (6.7%) underwent re-exploration for hemorrhage (Grade IIIB), and two patients (6.7%) were shifted to postoperative intensive care unit (Grade IV). However, in group B, one patient (1.5%) underwent Double-J stenting for postoperative urinoma (Grade IIIA), one patient underwent re-exploration for hemorrhage (Grade IIIB), and two patients (3.3%) were shifted to postoperative intensive care unit (Grade IV).

The overall complication rate (p = 0.440) and major complication rate (p = 0.136) were similar in both the groups. Table 2 highlights the histopathologic characteristics in both the groups that were similar except positive surgical margin. Two patients (6.7%) in Group A had a positive surgical margin as compared with no patient in Group B.

In terms of renal function outcomes on postoperative day 1 and at 1 year follow-up, there was a significant decline in eGFR from the preoperative period on postoperative day 1 (p < 0.001) and at 1-year follow-up (p < 0.001) for the entire cohort, however, the decline was statistically similar in Group A (LPN) and Group B (RPN). Table 3 describes the detailed functional outcomes in terms of eGFR for 1-year follow-up. In terms of oncologic outcomes, there were two local recurrences (6.7%) in Group A as compared with one local recurrence (1.7%) in Group B (p = 0.257). There were no distant recurrences. These patients underwent repeat surgical management and one patient was kept on active surveillance and there has been no distant recurrence till date.

Table 3.

Comparison of Follow-Up Outcomes of Patients Undergoing Laparoscopic Partial Nephrectomy (Group A) vs Robot-Assisted Partial nephrectomy (Group B)

Parameter	Overall (n = 90)	Group A (n = 30)	Group B (n = 60)	p
Renal function outcomes
Preoperative
Serum creatinine, mean (SD), mg/dL	1.06 (0.23)	1.03 (0.18)	1.01 (0.25)	0.521
eGFR, mean (SD), mL/min per 1.73 m²	85.1 (20.8)	87.1 (21.2)	84.1 (20.7)	0.536
Postoperative day 1
Serum creatinine, mean (SD), mg/dL	1.14 (0.35)	1.13 (0.35)	1.15 (0.36)	0.834
eGFR, mean (SD), mL/min per 1.73 m²	69.5 (18.3)	69.3 (18.2)	69.6 (18.5)	0.923
eGFR decline, median (IQR), mL/min/1.73 m²	−11.5 (5.7–22.3)	−16.7 (9.2–26.5)	−10.5 (2.8–21.3)	0.102
% eGFR decline, median (IQR), %	−17 (8–24)%	−20.5 (11–26)%	−13.5 (5–23)%	0.084
Postoperative follow-up at 1 year
Serum creatinine, mean (SD), mg/dL	1.15 (0.25)	1.17 (0.35)	1.15 (0.19)	0.724
eGFR, mean (SD), mL/min per 1.73 m²	69.9 (15.4)	71.5 (17.8)	69.1 (14.2)	0.488
eGFR decline, median (IQR), mL/min per 1.73 m²	−7.9 (5.1–24.1)	−8.9 (6.5–20.8)	−6.9 (4.2–25.1)	0.155
% eGFR decline, median (IQR), %	−8 (7–28)%	−9 (8–28)%	−8 (6.5–29.5)%	0.143
% eGFR preserved at 12 months, median (IQR), %	92 (72–93)%	91 (72–92)%	92 (70.5–93.5)%	0.537
eGFR >90% preserved, n (%)	57 (63.3%)	18 (60%)	39 (65%)	0.643
No CKD upstaging, n (%)	83 (92.2%)	26 (86.7%)	57 (95%)	0.164
Oncologic outcomes, n (%)
Local recurrence	03 (3.3%)	02 (6.7%)	01 (1.7%)	0.257
Distant recurrence	0	0	0

CKD = chronic kidney disease; eGFR = estimated glomerular filtration rate.

Stratifying our results in trifecta and pentafecta outcomes (Table 4), 40 patients (66.7%) in Group B achieved trifecta outcomes, which was significantly higher than 11 patients (36.7%) in Group A (p = 0.012). In contrast, the pentafecta outcomes were achieved in 10 patients (33.3%) in Group A and in 28 patients (46.7%) in Group B, which were statistically similar.

Table 4.

Comparison of Trifecta and Pentafecta Outcomes in Patients Undergoing Laparoscopic Partial Nephrectomy (Group A) vs Robot-Assisted Partial nephrectomy (Group B)

Outcome parameter	Group A (n = 30)	Group B (n = 60)	p
Negative margins, n (%)	28 (93.3%)	60 (100%)	<0.001
No postoperative complications, n (%)	19 (63.3%)	48 (80%)	0.404
WIT <25 minutes, n (%)	17 (56.7%)	47 (78.3%)	0.013^*
Trifecta outcomes achieved, n (%)	11 (36.7%)	40 (66.7%)	0.012^*
eGFR >90% preserved, n (%)	18 (60%)	39 (65%)	0.643
No CKD upstaging, n (%)	26 (86.7%)	57 (95%)	0.164
Pentafecta outcomes achieved, n (%)	10 (33.3%)	28 (46.7%)	0.227

p < 0.05 is considered significant.

Discussion

Our study has tried to systematically compare the perioperative and functional outcomes of NSS through laparoscopic and robotic approaches in a unique cohort of highly complex renal tumors using a matched cohort analysis. We found higher WIT, higher operative time, higher blood loss, and similar complication rate in LPN as compared with RPN. The achievement of trifecta outcomes was significantly higher in the RPN group (66.7%) than in the LPN group (36.7%). The eGFR preservation was similar in both cohorts and pentafecta outcomes were achieved at a similar rate in both groups. Our study also highlights an important concern that despite difference in trifecta outcomes, the pentafecta outcomes that mainly comprise renal function preservation largely remain similar in the two groups.

Various studies have reported the outcomes of NSS in complex renal tumors. Rogers and colleagues initially reported 11 patients of complex hilar tumor managed with RPN with mean WIT of 28.9 minutes and no positive surgical margins.⁴ Abedali et al.¹¹ did a matched cohort comparison of 148 patients undergoing RPN with 74 patients undergoing open partial nephrectomy (OPN) for intermediate and high complex renal tumors. The intraoperative blood loss, WIT, and hospital stay were significantly higher in the OPN group than in the RPN group. Kim and colleagues also reported similar results.⁶

Few series have compared the outcomes of LPN and RPN in complex renal tumors, but most of the studies have used RENAL score ≥7 as the inclusion criteria for complex tumors. Long and colleagues¹² compared 182 LPN with 199 RPN in patients with renal tumors having a RENAL score ≥7. They found a significantly higher rate of conversion to radical nephrectomy in the LPN group but reported similar WIT, blood loss, blood transfusion rate, and postoperative complication rate in both groups. However, they found a significantly higher decline in eGFR in the LPN group than in the RPN group. Jang et al.³ also reported similar perioperative and functional outcomes. However, baseline differences make the inference difficult.

In terms of perioperative outcomes, we found longer WIT and higher estimated blood loss in the LPN group than in the RPN group. Similar results were reported in a multicenter analysis by Zargar et al.⁸ They compared 1185 RPN patients with 646 LPN patients and reported significantly lower WIT and EBL, despite higher tumor complexity (RENAL score), in the RPN group. Even for experienced laparoscopic surgeon, RPN has been shown to be associated with lower WIT.¹³ In a single-surgeon series of 146 LPNs and 137 RPNs, RPN was associated with decreased WIT even after adjusting for learning curve and tumor complexity.¹³ RPN with three-dimensional magnified vision, better ergonomics, and wrist articulation helps in decreasing blood loss and suturing time involving complex maneuvers of suturing of vessels/collecting system and renorrhaphy.¹³

A systematic review involving 766 patients comparing RPN and LPN also reported shorter WIT with RPN.¹⁴ In our study, 17 patients (56.7%) in the LPN group as compared with 47 (78.3%) patients in the RPN group achieved WIT <25 minutes (p = 0.013). This was the major reason for achieving lower rate of trifecta outcome in the LPN group (11, 36.7%) as compared with the RPN group (40, 66.7%) (p = 0.012), despite similar complication rate in the two groups. Furthermore, this longer WIT did not translate into worse eGFR and renal function outcomes at 1 year and, hence, led to similar pentafecta rates between LPN and RPN groups.

The “trifecta” and “pentafecta” outcomes provide standardized reporting of outcomes in NSS. Kim et al.¹⁵ compared the trifecta and pentafecta outcomes in a matched cohort of 60 patients undergoing RPN with T1a and T1b disease. The trifecta outcomes could be achieved in 65.3% in the T1a group as compared with 43.3% in Group B (p = 0.017). However, the achievement of pentafecta outcomes was 38.3% in the T1a group as compared with 26.7% in the T1b group (p = 0.172). In another similar study, Castellucci and colleagues¹⁶ compared 85 patients with <4 cm renal tumor with 38 patients with >4 cm tumor. They found significantly higher achievement of trifecata and pentafecta outcomes in tumors <4 cm.

However, literature is scarce on trifecta and pentafecta outcomes in NSS for complex renal tumors. Gu and colleagues¹⁷ compared 61 patients undergoing RPN with 51 patients undergoing LPN with completely endophytic T1 tumors. Among them, 20 patients (32.8%) in the RPN group and 19 patients (37.3%) in the LPN group had a RENAL score ≥10. They found similar operative time, blood loss, and WIT in the two groups.

This was contrary to the results of our study, which could be explained because of smaller tumor size with lower RENAL scores, and variable surgeons' experience with laparoscopy. However, they reported that 66%–70% of patients had >90% preservation of eGFR at 1 year, which was similar to the results of our study. They reported the achievement of pentafecta outcomes in 37.3% in the LPN group and 42.6% in the RPN group (p = 0.564). This was similar to our results, although the cohort of patients included in our study had more complex tumors with higher stage and RENAL scores.

Our study has several strengths. This study compared for the first time the trifecta and pentafecta outcomes in LPN and RPN systematically in a unique subset of patients with highly complex renal tumors (RENAL score ≥10). Our results showed lower trifecta but similar pentafecta outcomes in the laparoscopic cohort. This could easily be explained by longer WIT in the LPN group and higher margin positivity owing to the technical difficulty in this cohort. However, this longer WIT might not necessarily translate to a higher decline in eGFR and the development of CKD.^18
–20 Moreover, a matched cohort analysis allowed us to address the baseline confounding factors, which make the inference in various other studies difficult.

However, our study has several limitations. Limited sample size with a retrospective study design comes with an inherent bias. Our study involves cases done by a single surgeon experienced extensively in laparoscopy and robotic surgery, hence, the single-surgeon–single-center nature of this study might limit its application to other centers. Robotic surgery has been performed more commonly in recent years, hence, the initial surgical experience of partial nephrectomy with laparoscopy might have introduced a bias in favor of robotic surgery. This could have been potentiated with a possible selection bias because of the nonrandomized study design.

All the histopathology specimens could not be reviewed by a single pathologist; however, the reporting was done by experienced genitourinary pathologists. Furthermore, the added cost of use of the robotic platform for these complex surgeries might be balanced owing to better performance in terms of complications and trifecta outcomes. However, we did not study comparative cost analysis between the two approaches. Moreover, the volume of renal parenchyma preserved might be a critical predictor for trifecta and pentafecta outcomes in complex renal tumors and this could not be studied.

Conclusion

In a matched cohort of patients undergoing NSS for highly complex renal tumors (RENAL score ≥10), the robotic approach offers a superior advantage in the achievement of trifecta outcomes as compared with the laparoscopic approach. However, both LPN and RPN can achieve similar pentafecta outcomes.

Footnotes

Availability of Data and Material

The authors confirm the availability of and access to all data reported in this study.

Code Availability

Appropriate codes were used to maintain patient confidentiality in data management software.

Authors' Contributions

Protocol/project development was done by P.D., R.M., S.C., and A.K. Data collection or management was taken care of by H.G., B.D., A.B., A.S., R.K., and A.K. Data analysis was carried out by H.G., A.B., and R.K. Article writing and editing were carried out by H.G., B.D., and A.K.

Author Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

Abbreviations Used

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