Robotic Partial Nephrectomy: Expanding Utilization,Advancing Innovation

Abstract

Robotic partial nephrectomy (RPN) is gaining increasing prominence for nephron-sparing surgery in the treatment of patients with localized kidney tumors. RPN offers the benefits of minimally invasive surgery with a shorter learning curve compared with its laparoscopic counterpart. While long-term data are awaited, RPN does provide short-term oncologic and functional outcomes comparable to open and laparoscopic partial nephrectomy. Furthermore, robotic surgery has facilitated technical innovation, including the elimination of warm ischemia, provided minimally invasive alternatives to patients with complex tumors, and importantly, has fuelled increased dissemination of partial nephrectomy surgery among community urologists.

Introduction

Partial nephrectomy (PN) is the standard of care for patients with T1a renal-cell carcinoma.^1

–4 There is considerable evidence that PN provides comparable overall survival and oncologic outcomes compared with radical nephrectomy (RN),^5

–8 while reducing the risk of chronic kidney disease (CKD) and long-term cardiovascular complications.^9,10 Despite this, EORTC 30904, a randomized trial comparing PN and RN, demonstrated improved overall survival for patients treated with RN and no difference in the incidence of end-stage renal disease.¹¹ Thus, the benefits of PN may hinge on patient selection and more nuanced technical aspects of surgery. However, based on the wealth of oncologic data and functional benefits of nephron sparing in the literature, PN rates have steadily increased over the past decade.^12,13

The goals of PN are summarized by the “trifecta”: complete oncologic resection to achieve negative surgical margins, maximal preservation of renal function, and avoidance of clinically significant perioperative hemorrhage.¹⁴ While open partial nephrectomy (OPN) was considered the reference standard in years past, robotic partial nephrectomy (RPN) is now assuming this mantle at centers with the requisite experience and volume.¹⁵ Laparoscopic partial nephrectomy (LPN) has been shown to provide comparable oncologic outcomes to OPN with decreased hospital admission rates, blood loss, and postoperative complications.¹⁶ However, LPN is a more technically challenging surgery than OPN or laparoscopic RN, requiring advanced laparoscopic skills for tumor resection and renal reconstruction.¹⁷

RPN is now an established approach¹⁸ offering many advantages compared with OPN and LPN.¹⁹ The robotic technique allows surgeons to overcome many of the technical challenges of pure laparoscopic surgery, thereby shortening the learning curve.^19
–21 Specifically, the robotic system provides optically magnified three-dimensional (3D) images, articulated instruments to replicate wrist-like dexterity and scaling of surgeon's movements for precise control.²⁰ This directly translates to greater intraoperative finesse and control for the surgeon, which allows for more precise and efficient tumor excision and renorrhaphy and decreased ischemia times. In this review, we discuss the role of RPN, including comparative oncologic, perioperative, and functional outcomes and costs. As mentioned, we believe that RPN is rapidly becoming the reference standard, allowing minimally invasive approaches for increasingly complex renal tumors and facilitating novel innovations in renal surgery.

Comparison of RPN and LPN

Despite the mounting experience with RPN, data comparing this technique to LPN are limited and early in maturity. There are currently no randomized trials to guide decision-making regarding LPN and RPN, and such trials are unlikely to be forthcoming given the rapid adoption of RPN. As a result, the best available evidence comes from meta-analyses of observational studies (section “MIS surgery among low-volume surgeons and centers”) assessing oncologic and functional outcomes. These comparisons are often temporally separated, with contemporaneous RPN cohorts being compared with historical LPN groups.

Oncologic outcomes

LPN provides comparable long-term oncologic outcomes to OPN for patients with T1 renal masses.^22
–24 In a recent meta-analysis, Leow et al. found that patients treated with RPN had a lower risk of positive surgical margin (risk ratio 0.53) than those treated with LPN.²⁵ In a single-center retrospective analysis, Wang et al. demonstrated an equivalent 3-year recurrence-free survival for patients treated with LPN and RPN (LPN: 95.2% and RPN: 97.1%; p = 0.71).²⁶

Long-term outcome data for LPN and OPN have been reported; however, such data for RPN have only recently become available. Among a multi-institutional matched cohort of patients treated for complex renal tumors, Wang et al. demonstrated an equivalent 5-year recurrence-free survival for patients treated with robotic (95.1%) and open (92.7%) PN (p = 0.48).²⁷ RPN affords excellent survival outcomes with a 5-year overall survival of 91.1% and a 5-year cancer-specific survival of 97.8%.²⁸

Thus, among patients with T1 renal tumors, the available evidence indicates that RPN provides comparable or better short- and intermediate-term oncologic outcomes to LPN and OPN. However, further study is required to assess long-term (10 years) results.

Perioperative outcomes

Leow et al. recently reviewed perioperative outcomes for 4919 patients treated with RPN and LPN in 25 separate studies.²⁵ Although patients treated by RPN had larger and more complex tumors, the conversion rate to open surgery or RN was lower. Furthermore, patients treated by RPN had shorter warm ischemia time (WIT), by an average of 4.3 minutes.^25,29 Choi et al. hypothesize that shorter warm ischemia may be due to the improved control and precision the robotic system offers, compared to traditional laparoscopic instruments, allowing surgeons to operate more quickly and effectively.²⁹

The impact of warm ischemia on renal function following PN is controversial. While a recent systematic review demonstrated no difference in renal function for patients with short durations of ischemia (<25 minutes) compared with zero ischemia,³⁰ other work has shown that each minute of warm ischemia may be associated with an increased risk of acute renal failure and new-onset stage IV CKD (adjusted odds ratios 1.05 and 1.06, respectively).³¹ Although the relative importance of ischemia duration compared to volume preservation for long-term renal function is controversial,^32,33 the difference in WIT observed in this study (4 minutes) may be clinically relevant. Moreover, as is discussed in greater detail later, robotics facilitates earlier proficiency with PN and proficiency for lower volume surgeons. Thus, the difference in WIT between the two techniques is likely greater for patients treated by surgeons with less experience or those with lower surgical volumes.

Leow et al. found that patients treated with RPN had a significantly lower risk of any (Clavien ≥1) or major (Clavien ≥3) complications.²⁵ Furthermore, there were no significant differences between RPN and LPN with respect to estimated blood loss (EBL), operative time, or hospital length of stay (LOS). In contrast, a smaller, previous systematic review and meta-analysis found that RPN was associated with a significant decrease in hospital LOS compared with LPN.²⁹

Functional outcomes

In meta-analyses by both Leow et al. and Choi et al., renal function preservation was similar between modalities. Patients undergoing RPN had similar pre- and postoperative estimated glomerular filtration rates (eGFRs) when compared with those treated with LPN.^25,29 While Choi et al. initially suggested that there was a smaller change in eGFR for patients undergoing RPN,²⁹ more recent evidence suggests that this change is similar for patients treated with RPN and LPN.²⁵

Cost

Numerous studies have examined the cost-effectiveness of robotic surgery in urology, focusing primarily on radical prostatectomy. Many advocate that the higher upfront costs of robot-assisted surgery, including infrastructure and disposable costs, can be offset by the shorter hospital stay, lower risk of short-term complications, and lower positive surgical margin rate, provided there is enough surgical volume.^15,34,35 While the corresponding literature for RPN is yet evolving, the available data suggest that RPN is likely cost equivalent to OPN.³⁶ Due to the purchase price of the robotic platform, maintenance costs, and disposables, RPN may be associated with higher operating room costs.^37,38 However, as diffusion of the robotic platform is occurring independent of its use in RPN, infrastructure costs are likely less significant than in analyses assessing the cost-effectiveness of robotic radical prostatectomy. Furthermore, robotic infrastructure costs are likely to decrease in the coming years as competitors to the current da Vinci surgical system become available.

Medical practice patterns and payers may significantly affect cost considerations. In the American context, while Mir et al. found costs of RPN to be marginally higher than OPN ($11,962/case vs $11,427/case, respectively),³⁸ others have demonstrated cost equivalence with respect to variable costs³⁶ and overall costs.³⁷ This is driven primarily by shorter hospital LOS.³⁷ Similarly, in the National Health Service in the United Kingdom, Hughes et al. showed that patients treated with RPN had significantly lower costs in the 1- and 3-year periods following surgery than patients treated by either OPN or LPN,¹⁵ primarily as a result of fewer hospitalizations and inpatient bed days.¹⁵ Patients treated with RPN incurred £766.47 ($997.10) less in healthcare resource costs in the 3 years following surgery than those treated with OPN and £317.57 ($413.13) less when compared with patients treated with LPN.¹⁵ However, this analysis did not consider operative costs.

The cost of RPN must be considered in the context of clinical outcomes. While this work is in its nascence, current evidence suggests that RPN has a limited incremental cost of ∼$5000 per avoided complication compared with OPN, making RPN a cost-effective means of avoiding perioperative complications.³⁹

Role of Robotics in Expanding Utilization of Minimally Invasive Surgery PN

MIS surgery among low-volume surgeons and centers

LPN can be a technically challenging procedure, requiring considerable surgeon expertise. With the limited degree of motion of laparoscopic instruments, it can be difficult to accurately follow the angle of the tumor as well as reconstruct the parenchymal defect.⁴⁰ Furthermore, LPN has been shown to have a steep learning curve.⁴¹ As a result, uptake of LPN has remained limited, and recommendations have been made to limit use of LPN to surgeons with advanced laparoscopic skills.^4,42

In contrast, RPN has been shown to have a shorter learning curve.^43,44 Leow et al. ²⁵ examined the benefits of RPN in low-volume (<24 cases/year/center) and high-volume centers. They found that operative time and LOS were lower for patients treated with RPN than LPN in low-volume centers, while no significant difference was found in high-volume centers.²⁵ Furthermore, oncologic and perioperative outcomes were at least comparable between patients treated with RPN and LPN, even at low-volume centers. High-volume surgeons likely have sufficient laparoscopic proficiency to mitigate many of the advantages of the robotic platform.^13,45 Supporting this hypothesis, recent population-based evidence has shown that increasing diffusion of the robotic platform across the United States has resulted in increasing rates of PN.^13,46 Thus, the diffusion of the robotic platform has resulted in more patients receiving guideline-recommended care.

Tumor complexity

The robotic platform allows surgeons improved dexterity and 3D depth perception, compared to laparoscopic surgery. This should, in theory, facilitate minimally invasive approaches for tumors with greater complexity, such as larger size, hilar location, deeper penetration with renal sinus, or collecting system involvement, and also large contact surface areas.⁴⁷ Among patients with a RENAL nephrometry score (Radius, Exophytic/endophytic, Nearness to collecting system, Anterior/posterior, Location relative to polar lines) ≥7, the use of RPN resulted in shorter operative times, shorter hospital LOS, and shorter WIT with equivalent functional and oncologic outcomes compared with LPN.²⁵ Advanced tumors (clinical T3 disease with renal vein involvement) have been effectively treated minimally invasively utilizing robotic assistance. In a series of four patients undergoing RPN for T3a tumors, WIT was <25 minutes, no patients required blood transfusion, hospital stay was 1 day, with one patient requiring readmission for ileus.⁴⁸

Tumor multifocality

Patients with asynchronous multifocal tumors (such as those with hereditary renal-cell carcinoma) are likely to require repeated renal surgeries, and renal preservation is of utmost importance to prevent end-stage renal disease. The robotic approach may allow for aggressive strategies to preserve renal parenchyma, such as enucleation, or to decrease ischemia, such as unclamped PN.⁴⁹ The impact on this approach for modifying the course of CKD in these patients remains to be elucidated.

Repeat or salvage surgery

The use of robotics has allowed for MIS in patients for whom open surgery was previously required. In a single-center experience of nine patients with previous ipsilateral PN, Autorino et al. demonstrated good functional and oncologic outcomes with no intraoperative complications, no renal unit losses, no positive margins, and no significant difference in pre- and postoperative eGFR.⁵⁰ The authors note that minimally invasive repeat renal surgery is more technically demanding than initial surgery, but demonstrate its feasibility.

While the available data are limited to a single case series, RPN has also proven useful in patients following failure of radioablative therapy with good perioperative (WIT 18 minutes) and functional outcomes (stable renal function).⁵¹

With the ongoing evolution of robotic surgery, we believe that RPN offers the potential for even more patients to undergo minimally invasive PN and avoid the morbidity of open surgery or complete renal unit loss.

Robotic retroperitoneal PN

While minimally invasive PN has traditionally been performed through a transperitoneal (TP) approach, a retroperitoneal (RP) approach offers potential advantages. Most notably, the RP approach allows for improved access to posterior tumors and renal vasculature, allows for an MIS approach in patients with multiple peritoneal adhesions or “hostile abdomens,” and can reduce potential injury to abdominal organs.^52
–54 Using an RP approach is more difficult due to the small working space and unfamiliar orientation to anatomical structures and, as a result, is less commonly performed than the TP approach.⁵⁵ Pure laparoscopic surgery in the retroperitoneum is difficult, as the small working space makes the suturing necessary for renorrhaphy challenging.^56,57 In this study, the robotic approach has the advantage of improved maneuverability and the Endo-Wrist for suturing.

A review by Xia et al. compared TP-RPN to RP-RPN and found RP-RPN to be equal to TP-RPN for complications, conversions, WIT, EBL, and positive surgical margins.⁵⁸ Furthermore, RP-RPN had shorter operative time than TP-RPN (p = 0.05, 153.4 minutes vs 183.3 minutes, respectively).⁵⁸ While this review did not examine LOS, others have found RP-RPN to be associated with a shorter hospital LOS compared with TP-RPN.⁵² Furthermore, recent evidence suggests that an RP approach may facilitate RPN in patients with previous abdominal surgery by avoiding intraperitoneal adhesions.⁵⁹ Thus, the robotic platform has enabled the emergence and uptake of RP-PN as an important approach in the armamentarium for select tumors and patients.

Limitations and Potential Concerns in RPN Uptake

Lack of haptic feedback

When surgeons transition from open or laparoscopic surgery to robotic surgery, they must train themselves to operate without tactile feedback. Robotic surgeons have learned to use visual cues to replace tactile cues in a process known as sensory substitution.⁶⁰ Owing to improved visualization, increased dexterity, tremor filtering, and motion scaling provided by the robotic platform compared to laparoscopic or open surgery, robotic surgeons can use visual cues instead of tactile ones to estimate tissue thickness and strength.⁶⁰ Recent work in general and cardiac surgery demonstrates that patients undergoing robotic surgery are no more likely to experience a haptic feedback-related complication than those undergoing open or laparoscopic surgery.^61
–63 However, this is a learned skill.^60,64

System failure

A system failure of the robotic system is a rare but potentially dangerous complication. The system failure of the robot is a rare event, occurring at a rate of 0.38%–2.4%.^65,66 However, in the case of system failure, conversion rates are low, ranging from 0.17% to 16%.⁶⁶ In addition, patient injury as a result of system failure is uncommon, occurring in fewer than 5% of patients.⁶⁵ Mandatory robotic training includes instruction, including team-based simulation, on the management of system failures.

Conversion to open or laparoscopic surgery

RPN requires preparedness on the team to convert to traditional laparoscopy, open PN, or radical surgery to optimize oncologic control and patient safety. The reported rates of conversion to open surgery for RPN range from 0% to 5%, and RPN has a lower rate of conversion to open surgery or radical resection than LPN.²⁹ In the event of vascular hemorrhage, the dexterity and control of the robotic system and extra nonworking arm allow hemostasis control either with suturing or other hemostatic approaches (e.g., Weck clips, additional bulldog clamps). Arguably, the visualization afforded by the robotic platform exceeds that which could be achieved following open conversion in many cases. In the event that open conversion is required, the robotic system can be rapidly undocked in a controlled manner. The bedside assistant is key in temporizing while the operating surgeon scrubs. For this reason, simulation and “disaster planning,” as well as the use of routine PN checklists, are important in mitigating the uncertainty associated with these rare vascular emergencies.⁶⁷

Risk of port site metastasis

Atypical recurrence patterns are a concern following robotic oncologic procedures.⁶⁸ In kidney cancer surgery, a total of 16 port site metastases have been reported,⁶⁹ of which only four were associated with PN. Of these, 9 (56%) had no identifiable cause with regard to surgical technique and 13 (81%) had multiple sites of metastasis.⁶⁹ Therefore, it is likely that in the vast majority of patients, port site metastases are the result of tumor biology (aggressive phenotype) rather than surgical technique.

Limitations of literary evidence

As with the adoption of many new medical technologies in surgery, RPN has gained considerable clinical traction, without randomized data. Thus, the evidentiary base on which this review is based depends on case series and retrospective, observational cohort studies with their intrinsic biases. The most relevant of these is a selection bias among patients undergoing PN. However, in our experience, patients with complex or advanced renal masses are more likely to receive RPN than LPN due to the technical benefits described previously. The recently reported randomized controlled trial comparing open and robotic prostatectomy provides hope that randomized data may be able to inform this question.⁷⁰ In fact, a trial comparing robotic and LPN is currently registered with ClinicalTrials.gov (NCT02933398) but has not yet commenced recruitment. This study is designed to address intraoperative and perioperative outcomes. Such a trial is unlikely to be feasible in the United States, given the growing adoption of the robotic platform, patient interest in this technology, and the costs associated with such a trial.

Surgical Innovations

Since its introduction over a decade ago, RPN has undergone numerous innovations to improve nephron sparing through (1) preserving normal renal parenchyma and (2) minimizing ischemia to healthy parenchyma.^71,72 It is believed that the preservation of renal function may confer a survival benefit among patients with sporadic, solitary tumors, particularly those with prior kidney disease in addition to those with multifocal disease and hereditary syndromes.⁷³ Furthermore, the mounting expertise with robotic surgery has allowed the development of innovative approaches to locally advanced tumors, including vena cava surgery.

Renal parenchyma preservation

Recently, studies have examined the effect of surgical approach (open, laparoscopic, or robotic) on the extent of renal parenchymal preservation. Takagi et al. showed that minimally invasive PN was associated with a higher rate of preservation of renal function (95% vs 92%) and a greater volume of normal parenchyma spared (84% vs 79%) than OPN.⁷⁴ This difference was not statistically significant, however, this study was limited by a relatively small sample size (n = 279) and the authors included RPN and LPN in the same group. More recently, Maurice et al. found that among 880 patients who underwent PN, RPN was associated with preservation of an additional 7.3 cm³ of normal renal parenchyma, compared with OPN.⁷⁵ Oh et al. also found that RPN was associated with narrower peritumoral margins compared with OPN.⁷⁶ This finding remained significant in multivariate analysis and with propensity score matching.

Zero ischemia

Both the duration of ischemia and ischemia type (warm vs cold) contribute to development of acute kidney injury.^32,33 While most are in agreement that prolonged ischemia >25 minutes is detrimental,³¹ the relative impact of renal parenchyma preservation and ischemia remains controversial.³² We have been particularly interested in the observation that volume-adjusted renal function outcomes demonstrate improvement with ongoing technical innovation, proceeding from conventional hilar clamping to early unclamping and now to superselective and completely unclamped techniques.³³ In addition, retrospective assessment of CT volumetric-adjusted eGFR demonstrated that actual eGFR mirrored predicted eGFR in the superselective clamping cohort, whereas main renal artery clamping resulted in lower actual eGFR compared with predicted eGFR, suggesting a detrimental effect of ischemia even after adjusting for volume loss.¹⁴ This benefit to eGFR may be greatest in patients with solitary kidney, advanced age, or underlying CKD.⁸ We have therefore developed zero-ischemia approaches for RPN.^77
–79

Initially, using renal microvascular dissection with selective clamping of tertiary or higher order arterial branches, we ensured that normal blood flow is maintained to the remainder of the kidney, minimizing ischemic injury. Our most recent approach to zero-ischemia RPN involves performing the surgery completely unclamped using a “minimal margin” technique.⁸⁰ Herein, we take advantage of the unique, radially oriented, intrarenal architecture and intrarenal vascular anatomy, as well as the histologically distinct layer of the tumor–parenchymal interface. Early comparative data demonstrate decreased blood loss and transfusion rates, decreased development of de novo CKD stage 3 with similar positive margin rates compared to our previous technique.⁸⁰ While uptake of the zero-ischemia technique remains limited to centers with advanced robotic expertise due to its technical demands, a recent systematic review found that zero ischemia may be beneficial in patients with impaired renal function.⁸¹

Innovations in renal surgery

The experience gained through RPN has advanced the utilization of robotic surgery for locally complex tumors, once considered to be only possible with open surgery. We have recently described the first series of robotic, level-III inferior vena cava thrombectomy.⁸² All cases were effectively completed robotically without conversion to open surgery and without mortality rate.⁸² While we believe this procedure should currently only be approached by expert robotic surgeons, it nevertheless demonstrates the potential of robotic surgery in patients with advanced disease. This is only the beginning of innovations in advanced urologic procedures that will be possible using the robotic platform.⁸³

Conclusion

RPN is becoming the standard-of-care for patients eligible for nephron-sparing surgery (NSS). With its technologic advances, robotics seems to have improved perioperative outcomes, shortened the learning curve for surgeons allowing for wide dissemination, and provided equivalent oncologic outcomes to OPN. As surgeons become increasingly familiar with robotic technology, it has allowed tumors of increasing complexity to be considered for NSS. Furthermore, surgeons have been improving functional outcomes by maximizing preservation of vascularized normal parenchyma and minimizing ischemia. As we continue to innovate, RPN will likely further distinguish itself from its predecessors, toward our ultimate goal of improved patient outcomes.

Footnotes

Author Disclosure Statement

I.S.G. declares conflict of interest for EDAP, Mimic, Hansen Medical.

Abbreviations Used

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