Trifecta Outcomes in Renal Hilar Tumors: A Comparison Between Robotic and Open Partial Nephrectomy

Abstract

Objectives:

To report a comparative analysis of outcomes in patients who underwent excisions of renal hilar tumors using both open and robotic approaches.

Materials and Methods:

We retrospectively reviewed robotic and open patients who underwent partial nephrectomy of renal hilar tumors between 2011 and 2016. “Trifecta” was defined as negative surgical margins, no complications, and a glomerular filtration rate (GFR) preservation of ≥90% at last follow-up. Inverse probability of treatment weighting (IPTW) was applied to equilibrate treatment groups, minimize selection bias, and optimize inference on the basis of each patient's clinicodemographic characteristics.

Results:

One hundred robotic and 64 open patients had sufficient data for IPTW. After weighting, there were no statistical differences in baseline characteristics between the two groups (p < 0.05). On adjusted analyses, robotic partial nephrectomy (RPN) achieved equivalent rates of trifecta to open surgery (21.1% vs 13.9%, respectively, p = 0.387). There were no differences between robotic and open cohorts for negative margin rates (72.8% vs 90.4%, p = 0.124), absence of complications (68.6% vs 75.2%, p = 0.587), or GFR ≥90% (39.4% vs 21.6%, p = 0.111). The robotic cohort had a shorter mean length of stay (3.8 vs 5.0 days, p = 0.012), and no difference in estimated blood loss (253.3 vs 357.1, p = 0.091) or operating time (199.8 vs 200.4, p = 0.961).

Conclusions:

In our analysis both open and RPN for hilar tumors were equally likely to achieve a low “trifecta” outcome with a shorter mean length of stay in the robotic cohort.

Introduction

Current guidelines recommend partial nephrectomy (PN) as a standard surgical treatment for clinical T_1a renal tumors whenever technically feasible,¹ given the improved renal function preservation compared with radical nephrectomy² and equivalent cancer control.^3,4 With the diffusion of robotic surgery, experience with robot-assisted PN has exponentially grown over the last decade, and this has led to broaden the indication of the procedure to more complex tumors. Initially, clinical stage or size cutoffs were used to define complexity^5,6; however, in the last decades, more accurate standardized scoring systems have been introduced aimed to define renal mass complexity, such as the R.E.N.A.L. nephrometry score, the preoperative aspects and dimensions used for an anatomical (PADUA) classification, the Centrality Index, and most recently the renal tumor contact surface area.^7

–10 Nonetheless, hilar masses are still regarded as a separate entity. Their physical contact with the renal vessels in the region of the renal hilum made many to consider laparoscopic techniques unfeasible until Gill and colleagues first described laparoscopic PN for hilar tumors in 2005.¹¹ Despite these advances, the pure laparoscopic approach to such masses remains very challenging and thus robotic assistance has been shown to facilitate tumor resection as well as renorrhaphy, with the continued advantage of a minimally invasive approach.¹² Notwithstanding the proved feasibility of robotic PN for hilar masses, some authors still consider the open approach as the gold standard for such complex lesions.¹³ We therefore designed the present study to compare outcomes in patients undergoing open PN vs robotic PN for hilar tumors, which to our knowledge is the largest series of its kind.

Materials and Methods

We retrospectively reviewed patients who underwent PN of renal hilar tumors between 2011 and 2016. Hilar tumor was defined as a tumor located in the renal hilar region abutting the renal artery and/or vein.

Fourteen surgeons (nine open, four robotic, one both), all fellowship trained or having at least 1-year staff experience, were included in the study. The surgical technique for open and robotic multifocal PN at our institution has previously been described.^14,15 Cases were performed under either zero, cold, or warm ischemia, as per surgeon preference.

All specimens were analyzed by dedicated urological pathologists. A positive surgical margin was defined as extension of tumor to the inked surface of the resected specimen on final pathology.

Due to an improved understanding of the more limited role of warm ischemia in determining ultimate renal functional preservation,¹⁶ the definition for trifecta, our primary outcome, was modified to include negative margins, no Clavien grade ≥1 complications, and a glomerular filtration rate (GFR) preservation of ≥90% at last follow-up. GFR was calculated using the Modification of Diet in Renal Disease (MDRD) formula.¹⁷ Secondary outcomes included each of the trifecta variables as well as length of stay, operating time, and estimated blood loss.

The Clavien–Dindo grading system was used to score postoperative complications within 30 days. Creatinine was measured preoperatively within 1 month of PN, and at 3- to 6-month intervals during postoperative follow-up.

Descriptive statistics were used to describe the patient population according to treatment status. Differences between cohorts for categorical baseline characteristics and perioperative outcomes were compared using the χ² test or fisher's exact test for low frequency variables. Continuous variables were described by median and interquartile range, and the Wilcoxon rank-sum test was used to compare differences. Inverse probability of treatment weighting (IPTW) was applied to equilibrate treatment groups with regard to clinicodemographic characteristics. To minimize bias and maximize precision of the propensity score model, all variables that might affect the primary outcome based off a priori hypotheses were included. Variables that could be influenced by treatment choice were explicitly excluded. This left us with the following: age, sex, race, Charlson's comorbidity index, body mass index (kg/m²), preoperative GFR, R.E.N.A.L. score (4–6: low, 7–9: moderate, 10–12: high), tumor size, average number of hilar cases per surgeon. Chi-squared tests, standardized differences, and propensity score histograms were used to compare treatment groups pre- and postweighting. Propensity-weighted adjusted logistic regressions with robust standard errors were employed to determine the relationship between the treatment group and primary and secondary outcomes.

All statistical testing was two-sided, and a p value of <0.05 was considered statistically significant. STATA 13 software (STATA, College Station, TX) was used for all statistical analyses.

Results

Between 2011 and 2016, 100 robotic and 64 open PN patients had sufficient data for IPTW. At baseline, the robotic cohort had a higher number of hilar cases per year per surgeon compared with the open cohort (3.83 vs 1.67, p = 0.000), as well as a lower median tumor size (3.5 vs 4.3 cm, p = 0.003) (Table 1).

Table 1.

Patients' Demographics and Tumor Characteristics

	Unadjusted			Adjusted (propensity weighted)
Variable	RAPN (N = 100)	OPN (N = 64)	p	RAPN	OPN	p
Patient variables
Age, years (SD)	60.30 (13.48)	62.80 (11.27)	0.254	62.42 (12.82)	60.25 (11.24)	0.487
Hilar cases per year per surgeon (IQR)	3.83 (3.83–6.33)	1.67 (1.42–4.0)	0.000	3.83 (1.67–3.83)	4.0 (1.67–4.0)	0.354
White race (%)	88 (88)	58 (90.62)	0.60	82.3 (92.2)	69.76 (94.59)	0.498
Male (%)	60 (60)	32 (50)	0.208	47.70 (53.45)	45.21 (61.3)	0.553
CCI (%)			0.546
0	47 (47)	27 (42.19)		35.21 (39.45)	33.63 (45.60)	0.632
≥1	53 (53)	37 (57.81)		54.04 (60.55)	40.12 (54.40)
BMI category (%)			0.247			0.991
≤25	23 (23)	10 (15.62)		14.63 (16.39)	15.0 (20.33)
25–30	34 (34)	22 (34.38)		36.46 (40.86)	24.71 (33.51)
30–35	27 (27)	19 (29.69)		26.68 (29.9)	24.3 (33.02)
≥35	16 (16)	13 (20.31)		11.47 (12.85)	9.69 (13.13)
Preoperative eGFR, mL/minute/1.73 m² (IQR)	81.78 (65.24–93.22)	73.62 (51.35–93.1)	0.078	71.98 (54.75–89.99)	78.84 (62.21–95.17)	0.250
Tumor variables
Tumor size, cm (IQR)	3.5 (2.7–4.5)	4.3 (3.5–5.5)	0.003	4.20 (3.0–5.1)	4.20 (3.3–5.1)	0.993
R.E.N.A.L. complexity class (%)			0.107			0.356
Low (4–6)	4 (4)	1 (1.56)		2.27 (2.54)	0.84 (1.14)
Moderate (7–9)	52 (52)	27 (42.19)		39.19 (43.19)	43.4 (58.84)
High (10–12)	44 (44)	36 (56.25)		47.8 (53.55)	29.51 (40.02)

BMI = body mass index; CCI = Charlson's Comorbidity Index; eGFR = estimated glomerular filtration rate; IQR = interquartile range; OPN = open partial nephrectomy; RAPN = robot-assisted partial nephrectomy; SD = standard deviation.

On unadjusted analyses, robotic partial nephrectomy (RPN) achieved equivalent outcomes to open surgery, including trifecta (26.4% vs 14.8%, respectively, p = 0.089), negative margin rates (92.5% vs 84.5%, p = 0.135), absence of complications (73.7% vs 61.3%, p = 0.097), and GFR ≥90% (39% vs 28.1%, p = 0.0154).

After inverse probability treatment weighting, there were no statistical differences in baseline characteristics between the two groups (p < 0.05). On adjusted analyses (Fig. 1), RPN achieved equivalent rates of trifecta to open surgery (21.1% vs 13.9%, respectively, p = 0.387). There were no differences between robotic and open cohorts for negative margin rates (72.8% vs 90.4%, p = 0.124), absence of complications (68.6% vs 75.2%, p = 0.587), or GFR ≥90% (39.4% vs 21.6%, p = 0.111). The robotic cohort had a shorter mean length of stay (3.8 vs 5.0 days, p = 0.012), and no difference in estimated blood loss (253.3 vs 357.1, p = 0.091) or operating time (199.8 vs 200.4, p = 0.961). There was no statistically significant difference in rates of conversion to radical nephrectomy in the robotic group compared with open (6% vs 7.8%, p = 0.653) (Table 2).

FIG. 1.

Adjusted analyses show equivalent rates of trifecta (21.1% vs 13.9%, p = 0.387); negative margin rates (72.8% vs 90.4%, p = 0.124); GFR >90% (39.4% vs 21.6%, p = 0.111); and absence of complications (68.6% vs 75.2%, p = 0.587)—robotic vs open partial nephrectomy, respectively. GFR = glomerular filtration rate.

Table 2.

Intraoperative and Postoperative Outcomes, Unadjusted

Variable	RAPN (N = 100), n (%)	OPN (N = 64), n (%)	p
Ischemia type			<0.001
Warm ischemia	44 (44)	7
Cold ischemia	8 (8)	85
Zero ischemia	2 (2)	6
Intraoperative complications
Conversion to open	0 (0.0)	n/a
Conversion to radical	6 (6)	5 (7.8)	0.653
Postoperative complications, Grade I–V	26 (26.2)	24 (38.7)	0.10
Major complications, Grade III–V	6 (6.1)	8 (12.9)	0.08
Grade I complications	9 (9.0)	1 (1.6)
Grade II complications	11 (11)	15 (24.2)
Grade III complications	0 (0)	6 (9.7)
Grade IV complications	6 (6.0)	2 (3.2)
Grade V complications	1 (1.0)	0 (0.0)
Postoperative complications, detailed
Arrhythmia	5	1
Urinary tract infection	2	1
Anemia	0 → embolization, 2 → transfusion	2 → embolization, 4 → transfusion^a
Urine leak	1	4
Ileus	5	2
Surgical site infection	3	4
Pneumonia	4	1
Acute kidney injury	3	2
Deep venous thrombosis	0	1 (with PE)
Myocardial infarction	0	1
Clostridium difficile infection	0	1
Hyponatremia	0	1 (req. ICU)
Delirium	1	0

One anemia with transfusion occurred in the patient who had pneumonia.

ICU = intensive care unit; PE = Pulmonary Embolism.

Additionally, there were no significant differences between the groups in their pathological outcomes with regard to tumor stage, tumor grade, malignant pathology, and malignant subtype (Table 3). Two patients developed local recurrence in each cohort, and two patients in the RPN group developed metastatic disease (one of which who had local recurrence) compared with one patient in the open PN cohort. The open PN had a longer follow-up compared with the robotic PN group (29.3 vs 16.6 months, p = 0.003).

Table 3.

Pathological Outcomes and Follow-Up Data, Unadjusted

Variable	RAPN (N = 100)	OPN (N = 64)	p
N (%)
Malignant disease	80 (80)	58 (90.6)	0.07
T stage			0.10
T_1a	46 (56.1)	25 (43.1)
T_1b	20 (24.4)	16 (27.6)
T_2a	1 (1.2)	1 (1.7)
T_2b	0 (0.0)	0 (0.0)
T_3a	12 (18.3)	16 (27.6)
Malignant pathology			0.15
Clear cell RCC	54 (67.5)	47 (81)
Papillary RCC	8 (10)	8 (13.8)
Chromophobe RCC	11 (13.8)	2 (3.5)
Mixed component of RCC	2 (2.5)	1 (1.7)
Other	5 (6.25)	0 (0)
Tumor grade
1 + 2	28 (50.9)	30 (46.9)
3 + 4	27 (51.1)	34 (53.1)
Median (IQR)
Follow-up, months	16.6 (7.7–27.2)	29.3 (12.3–44.8)	0.003
Latest eGFR, mL/minute/1.73 m²	69.4 (54.2–84.4)	58.4 (42.4–78.0)	0.02
Latest follow-up percent eGFR preservation	86.1 (73.9–96.1)	83.0 (67.8–92.3)	0.15
GFR ≥90% preservation, n (%)	39 (39)	18 (28.1)	0.15
Oncologic outcomes, n (%)	3 (3.8)	3 (5.2)
Local recurrence	2 (2.5)	2 (3.5)
Metastasis	2 (2.5) one point with local/metastatic	1 (1.7)

GFR = glomerular filtration rate; RCC = renal cell carcinoma.

Discussion

Minimally invasive PN offers multiple advantages to patients when compared with open PN, including decreased length of stay, blood loss, and avoidance of a painful flank incision.¹⁸ With these advantages in mind, laparoscopic PN has been shown to have similar oncologic efficacy to open PN; however, several shortcomings have included a steep learning curve as well as reports of higher postoperative morbidity.¹⁸ By 2010, robot-assisted PN overtook laparoscopic PN as the most commonly performed minimally invasive PN in the United States likely owing to the improved ergonomics, decreased technical challenges, three-dimensional vision, and increased precision.¹⁹ Most interestingly, studies have demonstrated improved outcomes with robot-assisted vs laparoscopic PN with regard to warm ischemia time, complication rates, and positive margins even in the hands of experienced laparoscopic surgeons.²⁰

Renal hilar tumors pose additional technical challenges to urologic surgeons due to their anatomic location. Early studies of laparoscopic PN for hilar masses demonstrated feasibility of resection,^21

–24 however, complication rates were not insignificant, including one study which demonstrated nine complications in six patients.²² Most of these studies concluded that PN of hilar tumors should be performed by advanced laparoscopists. With the increased use of robotics, studies have shown comparable risk of adverse outcomes for patients undergoing robotic PN for hilar vs nonhilar tumors.^25,26 However, some urologists still consider open PN as the preferred method of nephron-sparing surgery for complex tumors.¹³

In the largest series of robotic PN for hilar tumors, we retrospectively compared trifecta outcomes for 100 patients undergoing robotic PN vs 64 open PN patients. With the improved understanding that parenchymal preservation may actually be driving functional outcomes compared with warm ischemia time, our trifecta definition included a GFR preservation of ≥90%, along with negative surgical margins and zero complications.^16,27 When comparing baseline characteristics, the average tumor size for the robotic cohort was significantly smaller compared with the open cohort (3.5 vs 4.3 cm, p = 0.003). However, there was no difference in the complexity of the tumors based on R.E.N.A.L. scores. Additionally, there was a significant difference in the number of hilar cases per year per surgeon in the robotic PN vs the open PN (3.83 vs 1.67, respectively, p = 0.000). These data are likely reflective of the increased utilization of robotic PN in our institution.

IPTW was used to equilibrate the groups before comparing trifecta outcomes. RPN achieved equivalent rates of trifecta to open surgery for hilar tumors, without any differences in margin rates, complications, and GFR preservation of 90%. There were no differences in estimated blood loss and the RPN group had a significantly shorter length of stay of 3.8 vs 5.0 days (p = 0.012), the latter being a consistent finding in the literature when compared with open PN.^28
–30 Additionally, previous studies have demonstrated higher operative times for robotic PN, including a 2013 meta-analysis, which found a weighted mean difference of 40 minutes for robotic PN vs open PN^28,30; however, our findings reveal that at a high volume center there is no difference in operative time between robotic PN for open PN for these complex partial nephrectomies even with the inclusion of docking time and port placement.

When breaking down our trifecta outcomes, we can see similarities with the published data on PN for hilar tumors. In the only other study comparing robotic vs open PN for hilar tumors, Miyake and coworkers found equivalent outcomes between the two groups in terms of negative margins, complication rates, and percentage decrease in estimated glomerular filtration rate (eGFR).³⁰ Our raw positive margin rate of 7.5% in the robotic PN cohort is somewhat higher than a previously published meta-analysis on robotic vs open PN (positive margins: 3.3% vs 4.0%, respectively)²⁸; however, this is not unexpected given the challenging resection of a hilar tumor. Studies of minimally invasive PN for hilar tumors have shown positive margin rates from 0% to 9.1%; however, the small sample size in these studies (range n = 7–43 patients) makes it difficult to make meaningful comparisons.^{21

–25,31

–34}

There were no significant differences in complication rates between the robotic and open cohort, nor were there differences in pathological outcomes between the two groups. Two patients in each group developed a local recurrence, whereas metastatic disease occurred in two patients in the robotic group (one of whom had local recurrence) compared with one in the open group.

It is difficult to draw conclusions with regard to oncological outcomes given the short and varying follow-up between the robotic vs open cohort (16.6 vs 29.3 months, p = 0.003). Although these data were prospectively collected, another limitation of our study is its retrospective design and the inherent potential for selection bias. We attempted to limit objective cofounders with the use of propensity weighting. Additionally, a unified approach to ischemia was not used, as most open partial nephrectomy (OPN) cases underwent cold ischemia and most robotic PN patients underwent warm ischemia. These differences in ischemia could have potentially impacted renal functional outcomes. Regarding the evaluation of renal function, we concur that while the use of eGFR is a practical option, ideally a nuclear renal scan would have increased the quality of functional outcomes report. Moreover, CT scan-based volumetric assessment would have been valuable in such study.

Conclusions

This study demonstrates that both open and RPN for hilar tumors are likely to achieve a low “trifecta” outcome, modified as including negative margins, GFR preservation of >90%, and zero complications. Patients who underwent robotic approach for these complex tumors had shorter length of stay. The high surgical volume at our institution may limit the generalizability of the findings.

Footnotes

Author Disclosure Statement

J.H.K. certifies that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the article (e.g., employment/affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: Endocare, Inc., Intuitive—J.H.K. (consultant). All other authors have no industrial relationship to disclose.

Abbreviations Used

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