Abstract
Purpose of Review
To summarize current options available for robot-assisted partial nephrectomy
Recent Findings
Partial nephrectomy (PN) is a standard treatment option for management of cT1 renal masses. It may be carried out by multiple approaches. Robot-assisted (RA) PN is one such option. The goal of treatment is both correct oncological (negative surgical margins) and functional (preservation of sufficient amount of renal parenchyma of the operated kidney) outcome. Appropriate outcomes depend on multiple factors. There are many, but among others tumor characteristics (size, location, i.e., tumor complexity), patient baseline renal function, patient comorbidities, and performance status etc. Based on all these, the surgeon adapts the intervention for each mass/patient by preoperative planning, absence/use/duration of warm or cold ischemia, perioperative imaging, resection technique adapted to tumor location and depth of invasion, use of hemostatics, type and degree of renal parenchymal closure and others details. Nephroprotective agents have not shown efficacy so far. It should not be forgotten that surgeon’s experience plays a key role in the achievement of good results.
Summary
Although multiple factors have a role in the RA partial nephrectomy, surgeon experience and adaptation of technique of intervention have the crucial role in the achievement of both functional and oncological results.
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Introduction
The surgical treatment of renal tumors has been dynamically evolving in recent years. Advances in imaging and timely diagnosis have resulted in a stage shift of detected tumors. Furthermore, improvements in surgical techniques have led to increased utilization of renal parenchyma sparing approaches. Partial nephrectomy has become the preferred treatment option for the management of renal tumors technically feasible to resect without compromising the oncologic outcomes [1]. Initially, PN was used predominantly for cT1a renal tumors (= small renal masses). However, currently, its indication expanded to selected cT1b and cT2 renal lesions [2, 3].
Partial nephrectomy can be performed using an open, laparoscopic, or robotic-assisted approach.
The type of approach selected will depend on multiple factors, such as tumor-related factors, patient, surgeon, and institutional-related factors.
Robot-assisted PN (RAPN) is an attractive option because it combines the benefits of the minimally invasive approach with the dexterity of articulated instruments mimicking a surgeon´s hand. The first RAPN was carried out in 2002, by Gettman et al., and it is still an evolving technique [4]. Over time, RAPN increased in popularity and has shown certain benefits compared to open and laparoscopic PN [5, 6].
Besides it is clear oncological goal of removing a malignant tumor with negative margins, PN aims on maximizing the amount of preserved renal parenchyma to minimize the degradation of renal function and its potential long-term impacts [7].
The degree of renal function loss after this type of surgery can be due to underlying medical conditions and/or the surgical technique. Renal impairment with medical (= clinical) background is due to changes in the renal parenchyma related to aging, gender and comorbidities such as hypertension and diabetes. These changes progress with time and set the baseline for renal function before PN and the potential maximum recovery of renal function after PN [8, 9]. In other words, medical conditions define the quality of renal parenchyma and its perioperative fragility to surgical impact.
Surgery induced decrease in renal function following PN depends on temporary impairment of blood flow during PN, incompleteness/completeness of recovery from WI (if used), amount of non-tumoral tissue removed, as well as parenchymal damage due to reconstruction techniques used.. These factors are interrelated because they typically depend on the complexity of the renal tumor [10]. Tumors that are either large, centrally located, or with deeper invasion are often excised with longer WI times compared to less complex renal masses. Such tumors are also linked with greater blood loss and longer operating times [11].
Loss of renal function after PN in patients with two kidneys is reported to be on average 10% (88–91% preservation of renal function compared to preoperative values), which corresponds to a 20% decline in function, on the operated kidney. This correlates to the reported functional deterioration postoperatively in PN on solitary kidneys (functional preservation 76–86%) [9].
Despite these facts, surgeons have multiple options to decrease the likelihood of extended warm ischemia, as well as to prevent excessive resection and/or apply inaccurate suturing techniques.
Preoperative Planning
Every PN starts well before the incision by careful preoperative planning and review of imaging data. Although both computed tomography (CT) or magnetic resonance imaging (MRI) may be used, a bi- or tri-phasic contrast-enhanced abdominal CT with slice thickness < 5 mm is a reference standard [12]. This allows the surgeon to build a mental roadmap with regards to vascular anatomy, collecting system variations and of course size and location of the tumor [13]. Thorough knowledge of vascular anatomy might be important for a decision on the level of clamping needed—main artery vs. segmental branch vs. microdissection [14, 15].
Preoperative imaging enables the estimation of the tumor complexity based on the nephrometry scoring systems. They reflect a likelihood of warm ischemia (WI) use and its potential extent, the risk of peri- and postoperative complications and an impact on post-operative renal function or other parameters. Great number of scoring systems exist, but they are not all validated [16, 17]. Additional information may be also retrieved from the appearance of peri-renal fat, that may predict its density and adherence, having an influence on the perirenal and peritumoral dissection. Such information may be stratified according to Mayo adhesive probability score, which translates into different length of surgery, degree of bleeding or conversion to open surgery or radical nephrectomy [18, 19].
Computer modeling technology may improve surgeon understanding of individual patient anatomy and tumor complexity. It has been shown that volume rendering and 3D computer reconstruction (Fig. 1) improved perception of deep structures, surgical planning, and decision-making, with latter resulting in change of plan in 19% [20, 21]. Further step in pre-surgical preparation may be a 3D printing of patient´s specific kidney/tumor model. They may be of various degree of complexity based on the available materials and technology. It has been shown that they are accurate in the understanding of surgical anatomy and deemed useful by urologist in surgical planning [22]. Despite the usefulness of 3D-printed models, they are not cheap to produce. This is especially true, as they are patient specific and may not be used more than for one potential intervention. This may be substituted be augmented reality (AR), where a 3D virtual model is fused in real time with in-field surgical situation to provide an information on the localization od renal tumor and its relationships to vital structures. In the study on high complexity tumors (PADUA ≥ 10) the use of 3D hyperaccuracy AR RAPN as compared to 2D information provided by intracorporeal ultrasonography (US) a decreased use of global WI (45.8 vs. 69.7%), lower rate of collecting system entry (10.4 vs. 45.5%) and higher rate of enucleation technique (62.5 vs. 37.5%) was found [23].
Temporary Ischemia and Its Alternatives
There is no doubt that oncological outcomes are important, and their achievement is best accomplished by complete removal of the tumor mass with negative surgical margins. Functional impact of surgery is however equally important. We should therefore aim at balancing good visibility from bloodless field and potential impact of ischemia due to a temporary vascular occlusion.
It has been shown that on solitary kidneys every minute of WI increases the risk of new onset of severe chronic kidney disease (CKD) (glomerular filtration rate = GFR < 15) by 6% [24]. But in the study median time of WI was 21 min (range 4–55), which is currently often outperformed. However, there is still ongoing debate where is the time limit of WI for potentially irreversible ischemic injury. Warm ischemia is the only modifiable surgical factor, as compared to quality of renal parenchyma, comorbidities, size, location, and complexity of renal tumor etc. [25]. Selected data from RECORD2 study show that approximately 25% of patients after PN experience acute kidney injury (AKI) based on the RIFLE criteria (risk/injury/failure/loss/end-stage). Of those, the risk for AKI after a WI of < 10 min vs > 20 min in low-risk group was 13% vs 28% and in the high-risk group it was 31% vs 77% [26]. Similarly, an analysis of 668 patients with two kidneys from U.S. multi-institutional database has shown that WI time over 20 min is associated with AKI at discharge (a weak correlation, Spearman’s rho 0.32) [27]. But the same study had shown that at 1 year after the PN there are no statistical difference in renal function.
The study of Ebbing et al. on 444 patients has shown that impact of WI is a dynamically changing even below 20 min, then rises more steeply above that limit. But still, with absence of significant GFR difference between ischemic and non-ischemic PN [28]. Therefore, despite the inconsistency of the literature data, if a global ischemia is necessary, it is reasonable to try to keep the WI below 20 min.
To decrease the impact of WI we need either to reduce the duration of global WI or reduce its extent, by selective or superselective clamping.
The extreme decrease of WI is absence of vascular occlusion i.e. off-clamp PN (= clampless). This concept is certainly attractive, however data are somewhat conflicting. Analysis by Cacciamani et al. found that off-clamp PN performed better in short and long term compared to on-clamp [29]. But a retrospective analysis by Rosen et al. did not find a difference in the incidence of AKI or percentage change of GFR in off-clamp PN as compared to group with main artery clamping. There also no difference in positive surgical margin rate. There was a significantly increased blood loss in off-clamp group, 100 ml vs 50 ml in artery clamping [30]. This was not translated into increased transfusion rate and one can certainly argue that the difference is not clinically important. Another retrospective study however found an off-clamp approach favorable over on-clamp in PN, with postoperative GFR decrease of -2.2 ml/min/1.73m2 vs -9.7 ml/min/1.73m2 (p < 0.01). But again, the real clinical impact of such difference is arguable. Moreover, the amount of resected tissue (excisional volume loss) in the off-clamp group was significantly lower compared to on-clamp (-3.51cm3 vs -7.08cm3, p < 0.01), which indicates removal of twice as much of renal volume [31]. Also recent systematic review found the benefit of zero ischemia debatable with log(2) mean changes of GFR -1.37, -1.00, and-0.71 ml/min after cold, warm, and zero ischemia, respectively. There was a small (but significant) difference on the positive surgical margins rate with 4.8%, 4.0%, and 5.6% in patients after cold, warm, and zero ischemia (p < 0.01), respectively. The local recurrence rate was found in 3.2% and 3.1% of patients after WI and zero ischemia (p < 0.01), respectively [32].
Possible disadvantage of off-clamp (zero-ischemia) PN might be less clear working field due to various degree of parenchymal bleeding, which at least in less experienced hands may affect the surgical margin status. Results of CLOCK randomized control trial in patients with renal masses of RENAL (Radius, Exo-/endophytic, Nearness, Anterior/posterior, Location) score ≤ 10 have not found any functional difference between on-clamp and off-clamp PN and confirmed higher blood loss for off-clamp group [33]. Data also show that in comparable tumors and after long-term (usually after 6–12 months) the renal function is the same regardless of clamping technique [34, 35].
Another way of reducing global WI was introduced by Nguyen and Gill presenting a concept of early clamp removal after completion of the first (deeper) layer of renorhaphy in laparoscopic PN. This enabled a decrease of WI time by 50% [36]. British group of Stonier et al. has shown in systematic review that for RAPN, the decrease of WI time using early unclamping was -5.6 min, without compromising the operative time, estimated blood loss or complication rate. The decrease of WI seen in RAPN was lower compared to -15.4 min in laparoscopic PN group, most likely due to improved suturing skills [37].
Shortening of WI may be also achieved by changing the renorhaphy technique. It has been shown that the use of barbed sutures decreases the time of WI compered to non-barbed and running suture shorter compared to interrupted sutures [38]. However, the use of specific sutures or suturing technique is typically surgeon dependent.
As opposed to the effort reducing global WI, we may reduce the extent of parenchyma exposed to WI by selective [39] or superselective [14] clamping. This approach requires an identification of target vessel or vessels supplying a region with the tumor. Small bulldog clamps or selective clipping may ensure sufficiently blood less field in order to preserve the good visibility for resection. Retrospective analysis of Badani et al. in selected cohort of patients with solitary kidneys comparing full and selective clamping has shown that WI duration was similar in both groups under 15 min and no difference in the incidence of AKI, estimated blood loss or intra-operative complications was detected [39]. The same was true with not functional benefit if selective clamping was used in the patient with chronic kidney disease of grade 3–5 [40]. Others have found superselective clamping PN had more favorable short and long-term functional results [29]. This review however recognized low level of evidence of the analyzed studies.
Selective and superselective occlusion are interesting, but they require a presence of favorable vascular anatomy and preoperative planning by good quality imaging (preferably thin-layer contrast-enhanced computed tomography). This allows either multiplanar reconstruction (MPR) or maximum intensity projections (MIP) or three-dimensional volume rendering that allow better understanding of tumor-parenchyma contact extent and variation, plus enhance an identification of vascular anatomy specific for tumoral region [12]. However, recent study has shown that renal segments may often have multiple segmental vessels supply or target segment may have a blood supply by small branch from segmental artery feeding different segment [13]. There are significant variations to “common” vascular anatomy, which is found in only 70% of cases [41]. Use of selective/super-selective clamping is variable based on multiple factors (vascular anatomy, surgeon, solitary kidney etc.) and may vary from 8 to up to 50% [14, 39, 42]. Centrally located, hilar or polar tumors or PN in anatomically variant kidneys (e.g., horseshoe) [43,44,45].
Alternatively, some authors use both renal artery and vein clamping similarly to a whole hilum clamping in open PN. Hypothetically, both artery and vein clamping may reduce bleeding (”venous one”) and according to others a functional benefit is possible. The data across literature are inconsistent and often suffer from selection bias. Some authors have actually found that both artery and vein clamping increased the duration of warm ischemia and they hypothesized that dry resection field does not push the surgeon enough to close the defect rapidly [46]. Systematic review comparing artery-only with artery-vein clamping did not find any difference in WI time, surgery duration, bleeding and early GFR change [47].
Rare option that has been described for regional parenchymal occlusion during RAPN is a use of parenchymal compression by external clamp. It is assistant dependent and suitable only for conveniently located polar tumors [48]. In specific situations a repeated clamping might be an important option. It may be used if extensive bleeding is encountered after unclamping and accurate hemostasis need to be carried out [49] or in patients with multifocal tumors, where one-stage multiple PN is performed [50, 51].
Certain complex tumors may require longer vascular occlusion for safe dissection and suturing. Therefore, a cold ischemia (CI) may be applied aiming to decrease a functional impact from ischemia and reperfusion injury. Cold ischemia during RAPN may be accomplished by several techniques. Intracorporeal renal cooling with ice-slush has been proved to be effective in achieving renal temperature of 20 °C and safe [52]. Other techniques include perioperative intraarterial cooling with a catheter introduced into renal artery [4], retrograde ureteral cooling with ice-cold saline [53]. All reported options seem to be effective in achieving the desired temperature, but there is no comparison for evaluation of superiority. Exact cut-off time for CI during is even less clear compared to WI. Limited data from open PN indicate that it might be around 35 min [54]. But even in cases with longer CI (median 45 min vs 22 min of WI) in the setting of solitary kidneys the functional outcomes were comparable to shorter WI [55]. Besides complex tumors, the cohort of “at-risk” patient with underlying CKD seemed to benefit from CI more compared to patient with better preoperative renal function [56].
Preoperative Selective Embolization
Large or inconveniently located tumors may be sometimes resected after previous selective angioembolisation (SAE). This may potentially decrease the size of the tumor and reduce bleeding or to perform PN without vascular occlusion. It has been used for both in laparoscopic and RA PN [57, 58]. The delay between SAE and PN was only 1 day [58] or up-to 3 months with the idea of normalization of post-embolization inflammatory reaction and likely decrease of vascularity [57]. In the sub-group analysis of matched-pair comparison of PN performed for large angiomyolipomas (AML), patients with previous SAE in the RAPN cohort had shorter WI and better postoperative renal function [57].
Alternative to SAE which may aid in in nephron sparing surgery is a dye embolization of the tumor (mixture of blue dye and lipiodol for tumor coloring) followed by glue or coil SAE just before PN in hybrid operating room described by French group [59]. The aim of tumor coloration is visual recognition of tumor during laparoscopic PN without any vascular clamping and potentially reducing the risk of positive margins.
Intraoperative Imaging and Visual Guidance
Meticulous preoperative planning helps surgeon for intraoperative cognitive guidance. However, tissue flexibility, distortion and more intrarenally placed tumors pose sometimes problems. Therefore, intraoperative imaging is useful in such cases. There are two reasons for imaging: tumor limits/depth verification and/ identification and check of vascular supply into specific renal region in case with interest of selective clamping.
The easiest way of rapid visualization is an intracorporeal ultrasound (US). It can be performed by a laparoscopic probe and carried out by an assistant (Fig. 2) or preferentially by drop-in US probes managed by console surgeon. The are no major difference in the perioperative outcomes or margin rate, but the latter has the advantage of surgeon autonomy [60]. B-mode imaging may be complemented by color Doppler or CEUS (contrast-enhanced ultrasound) with identification of peritumoral vessels and control of absence of vascular flow in case with selective / super-selective clamping. Ultrasound image may be projected to TilePro display of robotic console [12, 14, 61].
TilePro display may be used for any other imaging/visualization/reconstruction complementing the camera information. One of such options is an augmented reality fused images allowing elastic fusion and real-time assessment of topography of tumor, vessels and collecting system [23, 62].
Complementary information may be obtained by a near-infrared imaging (NIR). It requires an intravenous administration of a fluorophore indocyanine green (ICG) with under infrared light give shining light green color of area that is vascularized [44, 62]. Clinical use consists of identification of vascularization and control of absence of blood flow in selective clamping or to assess correct renal reperfusion after reconstruction. Especially more complex (high nephrometry scores) or challenging cases (endophytic tumors) may benefit from use of NIR imaging [62, 63].
Resection Technique
Removal of tumors mass may be carried out in multiple ways adapted to their complexity and shape. Classical “resection” (or “wedge resection”) is a removal of tumor with enough of healthy renal parenchyma in order to keep negative surgical margin. Variants of resection included polar (upper/lower) and midsegmental resection or heminephrectomy. Technique of simple enucleation (SE) use a natural plane created by tumor pseudocapsule, which often present, without additional overlying parenchyma [64, 65]. Based on the degree of combination of the aforementioned techniques based on tumor anatomy a hybrid enucleation, pure or hybrid enucleoresection can be distinguished. Degree of resection/enucleation can be classified by SIB (surface-intermediate-base margin) score. [64]. In reality, surgeon adapts the degree of tissue dissection according to multiple patient and tumor factors. Anyway, more extensive resection means lower parenchymal preservation and vice versa. In comparison of oncological safety of SE compared to pure resection no major differences were found at 5 and 10 years in progression-free and cancer-specific survival, although positive margin rate (PSM) was higher in pure resection group. Important selection bias was however noted [66, 67].
Preservation of parenchymal volume is causally related to tumor complexity resulting in the amount of healthy parenchyma removed and the parenchyma devascularized by tumor excision and/or subsequent renorrhaphy. Surgeon´s experience has an important role [68].
Suturing Technique
Reconstruction of parenchymal defect following PN should ensure appropriate hemostasis and watertight closure of possible pelvicalyceal system breaches, with possible closure of excision site. Various renorrhaphy techniques are typically preferred. They are adapted to surgeon’s preference, skills and clinical situation. A combination of suturing and various hemostatic materials is common.
In RAPN, the robotic system´s abilities certainly facilitate suturing. Smaller and/or superficial defects may be closed in one-layer, larger and/or deeper defects in two layers. Single-layer technique is faster with regard to WI and total operative time, but there was no difference in blood loss or urine leaks [38]. Even for two-layer closure and early-unclamping may be used to decrease WI. Tightening the primary layer may be carried out or selective hemostasis may be added if necessary. Two-layer suture is linked with increased %volume loss based on semi-automated assessment CT scans [69].
Sutureless PN was also reported. It may be used for superficial cortical tumors and may be followed by resection bed coagulation (bipolar or argon-beam) or apposition of hemostatic materials such as oxidized cellulose, FloSeal or Tachosil patch or others [70, 71]. In this selected group, reported results are usually favorable.
With regard to type of suturing, some surgeons prefer interrupted sutures with “sliding-clip” technique (securing the end by non- or absorbable clips outside renal parenchyma), others use running sutures with clips at the two ends of suture. Running sutures (of any kind) are linked with shorter operating time, WI time, occurrence of postoperative complications and lower transfusion rate [38]. No difference in urine leaks were found. Knot-tying technique is very seldom used as it may prolong WI. In particular situations, oversewing of bleeding vessels might be necessary if the parenchymal defect is large and not suitable for parenchymal approximation, as this may further impair vascularization of the remaining parenchyma (Fig. 3). Another indication might be hilar resection or closure of collecting system opening.
Based on surgeon´s preference, barbed or non-barbed sutures may be used. According to a systematic review, barbed suture use resulted in shorter WI, but postoperative complications were similar compared to non-barbed ones [38]. Barbed sutures are easy to use, but their opponents point out an inability to bidirectional tension adjustment, if continuous bleeding occurs.
Hemostatic Materials
Bleeding control can achieved also be application of various hemostatic materials. They are used alone or in addition to suturing. The most commonly used are various modification of oxidized cellulose. It may be used to cover the resection defect, in the combination with other sealants or as a bolster to prevent sutures cutting through the parenchyma. There are four groups of sealants/adhesives available: fibrin sealants, collagen-based adhesives, hydrogel, and glutaraldehyde-based adhesive [38, 71].
Utilization of hemostatic materials or glues/sealants/adhesives is based on surgeon preference on an individual basis. But in larger studies, the real benefits on decrease of bleeding or alteration of peri-/postoperative outcome have not been shown [72].
Nephroprotective Agents
Multiple studies were carried out on potential nephroprotective ability of various compounds. Unfortunately, we do not have a pharmacological agent with protective characteristics against ischemia and/or reperfusion [9]. Neither mannitol, formerly the most frequently used in such indication, did not alter any short- or long-term renal function in PN [73].
Approach
Both transperitoneal and retroperitoneal (retroperitoneoscopic) approach have been used for RAPN. Retroperitoneal approach is suitable for posteriorly located tumors and patients with likely intraabdominal adhesions from previous surgeries, but there is a limited number of surgeons who are using it due to perceived complexity. In a comparison of both options, Arora et al. found that there were no clinically significant differences in WI time, intra- and postoperative complications and PSM rate [74]. Another study has found that retroperitoneal approach is linked with shorter operating time and lower costs [75].
However, comparison of both approaches might be inherently affected by selection bias related to tumor location.
Surgeon Experience
There is a uniform agreement across literature that experience of the surgeon affects both functional and oncological outcomes [9, 65, 68]. Owing to the maneuvering abilities of robotic instruments and more natural way of the surgery, the learning curve of RAPN is shorter compared to laparoscopic PN.
Results of PN are certainly affected by tumor complexity, every surgeon naturally has little nuances in the technique starting from preferred port distribution, instruments used, hilar control, resection/enucleation technique, suturing and others that influence the outcomes.
Authors in the analysis of 1222 PN from 11 institutions have divided a hospital volume (HV) and surgical volume (SV) into quartiles. They were for HV low < 20/year, moderate 20–44/y, high 45–70/y, and very high > 70/year, whereas for SV it was low < 7/y, moderate 7–14/y, high 15–30/y, and very high > 30/y. The rate of trifecta achievement rate increased significantly with surgeon volume (SV) (69.9% vs 72.8% vs 73% vs 86.1%) and hospital volume (HV) (60.3% vs 72.3% vs 86.2% vs 82.4%). Surgeon volume was linked with PSM rate, WI and operative time. Major complication rate was a function of HV [76].
Omidele et al. found “positive outcomes” after more than 61–90 cases at rate of 20 PN/year [77]. Similarly, a stabilization of operating time and trifecta rate after 77 cases was reported [78]. Other have found continuous improvement of WI times and complications Clavien-Dindo ≥ 2 during 50–100 cases with subsequent plateau after 150 interventions [79]. And finally, Larcher et al. described continuing improvement of WI time, blood loss decrease, and trifecta achievement event after 300 cases [80].
According to an analysis of Dagenais et al., quantifiable surgeon factors explained 10–40% of variability in intraoperative outcomes and over 90% of variability in PSM and patient morbidity. Non-measurable surgeon factors affected the variability of operative time in 27%, EBL in only 6%, and ischemia time in 31% [68].
Conclusion
Robot-assisted partial nephrectomy is a well-established technique for treatment of cT1 and selected cT2 renal masses. It is continuously evolving technique with further extension to complex renal tumors and patients with impaired renal function. Functional results depend on non-modifiable factors such as quality of renal parenchyma and modifiable factors, primarily extent and duration of warm ischemia during resection and reconstruction. They may be affected on multiple levels. Besides tumor complexity, functional and oncological results are influence by an individual surgeon´s technique and experience. Besides appropriate training ideally supported by a fellowship, the hospital and surgeon case load have important role in achievement of favorable results.
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Macek, P., Cathelineau, X., Barbe, Y. et al. Robotic-Assisted Partial Nephrectomy: Techniques to Improve Clinical Outcomes. Curr Urol Rep 22, 51 (2021). https://doi.org/10.1007/s11934-021-01068-4
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DOI: https://doi.org/10.1007/s11934-021-01068-4