Technologic advances in robot-assisted nephron sparing surgery: a narrative review
Review Article

Technologic advances in robot-assisted nephron sparing surgery: a narrative review

Parth Udayan Thakker1,2, Timothy Kirk O’Rourke Jr1,2, Ashok Kumar Hemal1,2,3

1Department of Urology, Wake Forest University School of Medicine, Winston-Salem, NC, USA; 2Department of Urology, Atrium Health Wake Forest Baptist Medical Center, Winston-Salem, NC, USA; 3Wake Forest Institute for Regenerative Medicine, Winston-Salem, NC, USA

Contributions: (I) Concept and design: PU Thakker, AK Hemal; (II) Administrative support: AK Hemal; (III) Provision of study materials or patients: PU Thakker, AK Hemal; (IV) Collection and assembly of data: PU Thakker, AK Hemal; (V) Data analysis and interpretation: PU Thakker, AK Hemal; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

Correspondence to: Parth Udayan Thakker, MD. Department of Urology, Wake Forest University School of Medicine, Winston-Salem, NC, USA; Atrium Health Wake Forest Baptist Medical Center, 1 Medical Center Blvd., Winston-Salem, NC 27103, USA. Email: pthakker@wakehealth.edu.

Background and Objective: Nephron sparing surgery (NSS) is the preferred management for clinical stage T1 (cT1) renal masses. In recent years, indications have expanded to larger and more complex renal tumors. In an effort to provide optimal patient outcomes, urologists strive to achieve the pentafecta when performing partial nephrectomy. This has led to the continuous technologic advancement and technique refinement including the use of augmented reality, ultrasound techniques, changes in surgical approach and reconstruction, uses of novel fluorescence marker guided imaging, and implementation of early recovery after surgery (ERAS) protocols. The aim of this narrative review is to provide an overview of the recent advances in pre-, intra-, and post-operative management and approaches to managing patients with renal masses undergoing NSS.

Methods: We performed a non-systematic literature search of PubMed and MEDLINE for the most relevant articles pertaining to the outlined topics from 2010 to 2022 without limitation on study design. We included only full-text English articles published in peer-reviewed journals.

Key Content and Findings: Partial nephrectomy is currently prioritized for cT1a renal masses; however, indications have been expanding due to a greater understanding of anatomy and technologic advances. Recent studies have demonstrated that improvements in imaging techniques utilizing cross-sectional imaging with three-dimensional (3D) reconstruction, use of color doppler intraoperative ultrasound, and newer studies emerging using contrast enhanced ultrasound play important roles in certain subsets of patients. While indocyanine green administration is commonly used, novel fluorescence-guided imaging including folate receptor-targeting fluorescence molecules are being investigated to better delineate tumor-parenchyma margins. Augmented reality has a developing role in patient and surgical trainee education. While pre-and intra-operative imaging have shown to be promising, near infrared guided segmental and sub-segmental vessel clamping has yet to show significant benefit in patient outcomes. Studies regarding reconstructive techniques and replacement of reconstruction with sealing agents have a promising future. Finally, ERAS protocols have allowed earlier discharge of patients without increasing complications while improving cost burden.

Conclusions: Advances in NSS have ranged from pre-operative imaging techniques to ERAS protocols Further prospective investigations are required to determine the impact of novel imaging, in-vivo fluorescence biomarker use, and reconstructive techniques on achieving the pentafecta of NSS.

Keywords: Urologic surgery; partial nephrectomy; pentafecta; augmented reality (AR); contrast-enhanced ultrasound (CEUS)


Submitted Feb 19, 2023. Accepted for publication Jul 07, 2023. Published online Jul 17, 2023.

doi: 10.21037/tau-23-107


Introduction

In 2020, renal malignancies compromised 2.4% of cancer diagnoses with an incidence of over 431,000 cases, worldwide (1). The prevalence is highest in the United States and Western Europe; however, the incidence is projected to rise in Asia, Africa and Latin America as these countries continue to transition to a Western lifestyle. The management of renal masses has continued to evolve over time. Open partial nephrectomy (PN) was first performed in 1887 but since the advent of minimally invasive surgery in urology, this approach has been favored for many renal tumors (2,3). The first laparoscopic partial nephrectomy (LPN) was performed in 1990 with the robot-assisted approach following approximately a decade later (4-6). Currently, AUA guidelines recommend PN for cT1a tumors; however, with advances in the understanding of vascular anatomy and development of advanced techniques, PN has been performed on complex, unfavorably located, larger tumors, and in solitary kidneys (7-16).

The principles of robotic-assisted partial nephrectomy (RPN) have also changed over time. Initially, the concept of the “trifecta” was used to evaluate the success of RPN. However, as surgeons have progressively performed more complex RPN, an understanding of the functional ramifications of surgery have become better delineated. This ultimately resulted in the expansion of the trifecta to the so-called “pentafecta” (17). In order to achieve the RPN pentafecta while removing larger and more complex renal masses, a more detailed understanding of renal anatomy and its vasculature has been investigated. Through concepts such as selective vascular clamping, three-dimensional (3D) modeling, and intraoperative imaging techniques, great strides have been made in the oncologic outcomes and preservation of renal function in those with renal masses. In this narrative review, we discuss the many recent technological advances that have been implemented in the ever-changing landscape of RPN. We present this article in accordance with the Narrative Review reporting checklist (available at https://tau.amegroups.com/article/view/10.21037/tau-23-107/rc).


Methods

We performed a non-systematic literature search of PubMed and MEDLINE on November 1, 2022 to identify and select manuscripts from January 2010 to September 2022 (Table 1). The search keywords included “augmented reality”, “fluorescence markers”, “renorrhaphy”, “ultrasound”, “surgical approach”, “clamping” and “early recover after surgery” in combination with “partial nephrectomy” and “nephron sparing surgery”. We manually reviewed all resulting manuscripts relevant to the topic that were written in English. We also reviewed the references lists of review articles to include other papers relevant to the topic.

Table 1

Search strategy summary

Items Specification
Date of search November 01, 2022
Databases and other sources searched PubMed, MEDLINE
Search terms used Partial nephrectomy, nephron sparing surgery, augmented reality, fluorescence markers, renorrhaphy, ultrasound, surgical approach, clamping, early recovery after surgery
Timeframe January 2010–September 2022
Inclusion and exclusion criteria Exclusion: non-English text
Selection process Independent article selection

Striving for pentafecta achievement

In an attempt to standardize post-operative outcomes following RPN, the term “pentafecta” emerged from the initial concept of the “trifecta”. The “pentafecta” is now the gold standard when comparing long-term success of nephron sparing surgery (NSS). This concept includes achieving (I) negative surgical margins, (II) warm ischemia time (WIT) ≤25 minutes, (III) no major complications, (IV) >90% preservation of baseline estimated glomerular filtration rate (eGFR), and (V) no upgrading of chronic kidney disease (CKD) stage. During partial nephrectomy, optimized oncologic outcomes are sought while simultaneously minimizing reciprocal damage from surgery and preservation of renal function. Optimization of factors including pre-operative imaging to minimize the risk of surgery for benign lesions, decreasing WIT by implementing artery-only clamping or totally clampless RPN, utilizing intraoperative models, fluorescence markers, ultrasound to minimize excision of normal parenchyma, decreasing ischemic suturing techniques and utilization of percutaneous ablation have been published. Great strides have been made since the advent of RPN and their relative contributions towards pentafecta achievement will be explored in this narrative review (18).


Pre-operative planning

Imaging

Cross-sectional imaging

The incidence of localized renal masses continues to rise with almost 70% of renal tumors being identified incidentally as the use of cross-sectional imaging has increased (19,20). While traditionally, contrast-enhanced computed tomography (CT) has been used to characterize renal masses, other imaging modalities have been implemented in recent years to better characterize malignant renal lesions. Magnetic resonance imaging (MRI) has been utilized as an alternative to CT without associated patient irradiation. Diffusion-weighted imaging (DWI) had a sensitivity of 86% and a specificity of 78% in differentiating between malignant and non-malignant lesions in a recent meta-analysis, and was moderately accurate in distinguishing low- and high-grade lesions which was comparable to CT findings (21). Perfusion levels based on perfusion MRI and in particular, arterial spin labeling (ASL) has been shown to vary among renal mass histology type with oncocytoma having higher perfusion levels than renal cell carcinoma (RCC) (22). In additional to traditional MRI, positron emission tomography (PET)-CT based molecular and nuclear imaging have been developed and studied as biomarkers in RCC. 18F-fluorodeoxyglucose (FDG) PET/CT is the most common radiotracer used; however, its use in RCC is limited due to physiologic uptake in normal parenchyma (23). However, it may have use in determining the aggressiveness of renal masses. Higher 18F-FDG PET/CT activity has been correlated with a higher Fuhrman grade, tumor-node-metastasis (TNM) stage, and identifying sarcomatoid features and thus may have utility in predicting aggressiveness and risk of progression (24-27). Girentuximab is a carbonic anhydrase IX binding protein that has been evaluated in combination with PET/CT to evaluate indeterminant renal lesions. In the multicenter, phase III REDECT trial, imaging with contrast enhanced CT and girentuximab-PET/CT prior to surgical resection was conducted in 195 patients to identify clear-cell vs. non-clear-cell RCC. The imaging results were compared surgical pathology at time of excision. Girentuximab-PET/CT had a sensitivity and specificity of 86.2% and 85.9%, respectively and contrast-enhanced CT had a sensitivity and specificity of 75.5% and 46.8%, respectively (28). Currently, the ZIRCON trial is underway, investigating the ability of girentuximab PET/CT to distinguish clear-cell RCC from other renal lesions, and preliminary results have been promising (29). Other radiotracers including 11C-acetate PET/CT and prostate-specific membrane antigen (PSMA)-targeted PET/CT as well as imaging-based radiomics have been studied (30). Though some potential is evident in using novel markers to distinguish benign vs. malignant lesions and predict renal mass histopathology, there is insufficient evidence to suggest their use in clinical practice at this time. There is significant promise for these markers to guide patient counselling; however, further validation is required.

Contrast-enhanced ultrasound (CEUS)

Ultrasound remains a highly sensitive tool in detecting renal masses although it is limited in its characterization of anatomical factors related to surgery, including number and location of renal arteries and veins. Though traditionally not used for pre-operative surgical planning, it is particularly useful in those with pre-existing renal insufficiency or contrast allergy. Duplex ultrasound is readily available at most centers; however, the granular detail regarding malignant potential is not easily obtained using this modality. CEUS is an evolving imaging technique that maintains the cost-effectiveness, lack of radiation exposure, and reliability of duplex ultrasound while utilizing sonovue contrast to obtain enhancement patterns of indeterminant renal masses (31). The malignant potential of renal masses remains a difficult area to navigate for the urologist as 25% of resected renal masses have benign pathology (32). A recent study by Tufano et al. demonstrated that when using a combination of qualitative and quantitative parameters to distinguish between benign and malignant lesions, sensitivity was 93% and specificity was 100% (33). Another study has also demonstrated the ability of CEUS to distinguish between RCC and specific benign lesions including angiomyolipoma (AML) with one study correctly identifying lesions in 80% of patients, though 20% of patients with lipid poor AMLs had incorrectly identified lesions (34). When focusing on oncocytoma in particular, a study by Wei et al. incorrectly identified 100% of oncocytomas as malignant lesions resulting in surgical excision of these masses (35).

A variety of CEUS based characteristics have been investigated to delineate benign and malignant lesions including: heterogenous enhancement, late washout, fast wash-in, and rim-like enhancement; however, there is a significant degree of overlap between these characteristics in malignant and benign lesions. There remains a paucity of literature supporting the use of any given imaging characteristic, mandating further investigations before CEUS is widely implemented in the delineation of malignant lesions. Though CEUS is a promising imaging modality, contrast-enhanced cross-sectional imaging remains the imaging of choice for characterization of these masses without larger prospective studies (36).

3D models

3D models and their application to renal masses have been a critical development. The concept of individualized precision surgery is embodied by its use. Currently, the majority of pre-operative planning for RPN is based on conventional two-dimensional (2D) imaging. Intraoperative ultrasound is commonly used for the resection of renal masses. Issues with this method arise primarily when attempting selective clamping and teaching surgeons-in-training (37). A solution to this may be using 3D-printed models to guide surgeon decision-making and to augment trainee and patient understanding. The question of 3D-printed model accuracy continues to be investigated. Michiels et al. demonstrated an 87.5% validity of their 3D-printed model compared to CT imaging; however, this study did not evaluate upper urinary tract-tumor contact (38).

Selective or super-selective clamping is thought to decrease global renal ischemia by clamping only necessary vessels associated with the renal mass to be excised. This is a tedious process and is difficult with only 2D imaging. Though super-selective clamping has not shown benefit vs. main artery clamping alone, selective artery clamping has demonstrated improvements in post-operative renal function recovery (39,40). A recent study demonstrated that 3D-printed reconstruction of renal vasculature allows for improved surgeon confidence in selective clamping as well as occasional changes in surgical planning (41). Another study by Fan et al. demonstrated that the use of 3D models in LPN for T1-T2b renal masses with a R.E.N.A.L. (tumor radius, exophytic/endophytic properties, nearness to collecting system, anterior/posterior, location to polar line) score ≥8, reduced overall WIT and intraoperative blood loss though no short-term differences in renal function were noted (42).

Perhaps the most important role of 3D models is on trainee education and pre-operative patient education. As the prevalence of robotic surgery has increased, trainees have as a consequence become more involved in the surgical steps than in the past (43). Complex intra-renal anatomy particularly when combined with endophytic tumors makes pre-operative planning difficult for trainees to fully grasp. These models allow for trainees to understand this complex tumor-kidney interface and may improve confidence and procedural understanding. Monda et al. conducted a study including participants across all levels of urologic training and demonstrated significant usefulness of 3D models for pre-operative training (44). Furthermore, the use of 3D models has been shown to improve patient understanding in regards to the disease process and treatment plan as well as comfort level with surgery (45). Cost analysis of these models ranges between $1–1,000 USD based on the type of printer used and time required for printing and processing ranges from 1.5 hours to 4 days (46). Ultimately, the utility of these models lies primarily in patient education and surgical trainee education; however, the widespread use of 3D models will clearly be inhibited by cost and time. Acquisition of 3D printers with shorter printing and processing times may allow for the ubiquitous use of these models.


Intra-operative considerations

Surgical approach

Transperitoneal vs. retroperitoneal approach

The transperitoneal approach to RPN may be favored for anterior and medial tumors (47,48). For patients with hostile abdomens or with posterior or peri-hilar tumors, a retroperitoneal approach may be preferable. The advantages of the retroperitoneal approach also include direct hilar access and reduction in renal pedicle injury (49). Arora et al. demonstrated equivalent perioperative outcomes with the exception of longer length of stay and increased blood loss for the transperitoneal approach (50). A larger study by Porpiglia et al. demonstrated shorter operative time by 35 minutes in the transperitoneal group which came at a cost of a 3% increase in the overall complication rate (51). These results have been corroborated by several other groups, indicating the retroperitoneal approach may provide some benefits while maintaining oncologic outcomes in larger or completely endophytic masses (52-56). Furthermore, Ghani et al. demonstrated decreased time to normal diet, shorter catheter durations, and a reduction in post-operative opioid needs for those undergoing retroperitoneal RPN (57). The transperitoneal approach is widely considered the standard surgical technique and larger-scale adoption of retroperitoneal RPN is limited by lack of utilization and demonstration for surgical trainees across all programs.

While many surgeons are proponents of the retroperitoneal approach in the appropriately selected patient, many comparative studies have presented mixed results. A recent study by Choi et al. demonstrated that while retroperitoneal RPN resulted in shorter operative times, less blood loss, and less WIT, when comparing pentafecta rates for masses ≥4 cm, no differences were seen. Furthermore, they demonstrated that at 1 year, those who underwent a retroperitoneal approach were noted to have a greater reduction in eGFR than the transperitoneal approach. This was attributed to decreased working space resulting in excision of larger amounts of non-diseased parenchyma (58). Likewise, Mittakanti et al. demonstrated no differences in the trifecta categories of WIT, positive surgical margins (PSM), and complication rates between the two groups (59). Based on existing literature, retroperitoneal RPN may reduce hospital costs, catheter times, and opioid consumption at the cost of excision of greater non-diseased renal parenchyma and longer operative times. Ultimately, long-term outcomes are lacking and peri- and post-operative outcomes are likely highly dependent on surgeon comfort with the retroperitoneal approach, requiring up to 300 cases for the transperitoneal approach (57,60). Thus, surgical approach to RPN should be individually tailored to each patient and outcomes associated with retroperitoneal RPN will likely improve as surgeons become more facile with the technical aspects of the retroperitoneal approach.

Single-port (SP) vs. multi-port (MP) approach

MP RPN has facilitated the widespread adoption of minimally invasive partial nephrectomy. The da Vinci SP robotic surgical system was more recently introduced in 2017 and continues to develop its place in the urologist’s armamentarium (61). Within urological surgery, the SP robot has been utilized for perineal prostatectomy, radical cystectomy, urinary diversion, ureteroneocystostomy, pyeloplasty, and partial as well as radical nephrectomy (62-67). While still in its youth, the use of the SP system for RPN has been studied, albeit mainly in single-center experiences, case series, and retrospective studies. A report of three patients by Kaouk et al. in 2019 initially demonstrated the feasibility SP RPN. All patients had negative surgical margins with an average WIT of 25 minutes though one patient required angioembolization in this study (68). While an SP system could theoretically reduce post-operative opioid consumption, a comparative, retrospective study from 2021 demonstrated similar short-term perioperative outcomes as well as similar inpatient and outpatient morphine equivalent consumption between the MP and SP study arms. Likewise, this study demonstrated no significant peri-operative differences between the SP and MP systems (69). Similarly, a recent prospective cohort study of 292 patients showed that the SP system resulted in longer WIT; however, all other peri-operative outcomes were similar between the groups (70). Ultimately, the SP system has not been widely investigated; however, retrospective and small cohort studies have demonstrated equivalent oncologic, peri-operative and pain-related outcomes to the MP system. Longer WIT may be attributed to surgeon comfort with the SP system and thus may be expected to improve over time. As outcome measures appear to be equivalent to MP, an SP system can be implemented if available and based on surgeon preference. There does not appear to be sufficient evidence to support the healthcare expenditure of acquiring an SP surgical system solely for RPN.

Fluorescence-guided therapy

Indocyanine green (ICG)

ICG is a fluorescent molecule that emits light when excited with near-infrared light (71). When injected intravenously, ICG binds to bilitranslocase and healthy, well-vascularized tissue appears isofluorescent (72). Applied to the surgical management of renal masses, tumors have lower expression of bilitranslocase and thus tumors appear hypofluorescent (73,74). This hypofluorescence has been demonstrated to have an 84% sensitivity and 87% of positive predictive value for malignant lesions in 100 cases, providing a reliable intraoperative method of identifying the oncologic potential of a renal mass (75). Furthermore, ICG is used to guide arterial clamping during RPN (76). The da Vinci platform has improved visualization and improved dexterity which has allowed for dissection of segmental and sub-segmental vasculature to ultimately decrease global renal ischemia (77). In combination with ICG these advances have allowed for super-selective arterial clamping which was initially demonstrated to reduce loss of post-operative eGFR 10-fold (74). Further studies have demonstrated a more modest reduction in eGFR post-operatively and at near 2 years follow-up (78-80). Conversely, a study by McClintock et al. demonstrated a reduced loss in eGFR with ICG-assisted segmental renal artery clamping in short-term follow-up, these results did not hold at 3 months (81). A more recent study by Takahara et al. comparing ICG-assisted full and selective clamping found increased blood loss with selective clamping with no benefit in eGFR at 6 and 12 months (82). While ICG-assisted RPN may not improve long-term compromise in renal function, it allows for rapid identification of the renal malignancy and may improve overall WIT and thus can be used to rapidly identify the tumor and normal renal parenchyma (83,84).

Folate receptor-targeting agents

The folate receptor is a widely abundant receptor with a difference in expression in normal and malignant renal tissue. Folate-linked ligands have previously been used as drug deliver agents into human cancer cells (85). Folate-receptor targeted near infrared (NIR) dye have been implemented in patients ovarian malignancy undergoing cytoreductive surgery, allowing surgeons to resect 29% greater malignant lesions than those not receiving dye (86). Since then, these dyes have been used for endometrial carcinoma, pulmonary adenocarcinoma, pituitary adenocarcinoma, metastatectomy for osteosarcoma, and for partial nephrectomy (87-91). While a paucity of literature is available for its application in RPN, a preliminary case report of three patients demonstrated tumor hypofluorescence with a good delineation between normal parenchyma and tumor. Furthermore, the authors were able to correlate patterns of intraoperative fluorescence to immunohistochemistry (92). A more recent study, similarly found excellent demarcation between normal parenchyma and tumor. Immunohistochemistry demonstrated staining limited to the proximal renal tubules which was significantly greater in normal parenchyma compared to tumor cells (93). While functional studies including a phase 2 clinical trial are underway, the benefits of folate receptor-targeted agents are not yet available.

Intra-operative imaging

Intra-operative ultrasound

The accurate identification and delineation between tumor and normal renal parenchyma is the primary goal when performing RPN. The tumor-parenchyma interface is difficult to precisely ascertain based on pre-operative 2D imaging and direct vision alone. Intraoperative ultrasound using a laparoscopic probe, when initially introduced, was cumbersome due to lack of surgeon (94). Drop-in ultrasound probes have since been introduced and controlled robotically by the surgeon to help identify this interface and depth of extension particularly for large, endophytic tumors or hilar tumors (95,96). Intraoperative ultrasound has also been used to identify renal vasculature for selective clamping and determine the distance between tumor and segmental vessels (97). In cases with renal vein and inferior vena cava thrombi, ultrasound can help localize the proximal extent of thrombus. Achieving negative surgical margins and preservation of as much normal parenchyma as possible are tenants of RPN; however, lower WIT have also been associated with decreased global kidney function, particularly in those with chronic pre-existing conditions (98-101). In an effort to reduce global ischemia and WIT, selective clamping in combination with CEUS has been used to reduce eGFR decrease after RPN (102-104). While intraoperative CEUS is not widely available, intraoperative drop-in ultrasound with assistance of TilePro technology will continue to play a critical role in all RPN cases.

Intra-operative use of augmented reality (AR)

While AR and 3D models have proven to be useful and trainee education and pre-operative patient education, its use intraoperatively as a replacement for ultrasound is emerging. This concept was first described by Porpiglia et al. (105). A retrospective study compared traditional intraoperative 2D ultrasound to AR-assisted RPN. These models developed pre-operatively were used intra-operatively during tumor resection and reconstruction phases. The use of intra-operative on-lay of pre-operative AR models resulted in lower rates of global ischemia and lower reduction in estimated renal plasma flow at 3 months (−12.38% in 3D AR group vs. −18.14% in 2D ultrasound group) by depicting detailed tumor, contact with collecting system, and vasculature (106,107). This study suffers from short-term follow-up; however, it provides promising support for the use intra-operative 3D on-lay technology.

Clamping technique

In an effort to eGFR after RPN, urologists have attempted to reduce WIT. Theorized to reduce ischemia to normal renal parenchyma distant from the tumor, selective clamping has been employed. These techniques have ranged from selective, super-selective, and clampless approaches to renal artery clamping alone (108,109). Clampless or “off-clamp” partial nephrectomy, as demonstrated by recent studies, have not been advantageous in preservation of renal function in patients with two functional renal units (109-111). There was also no difference in change in renal function at 9 months with those undergoing renal artery clamping alone vs. those undergoing renal artery and vein clamping (112). In combination with pre-operative CT imaging, segmental vessel clamping with ICG and near-infrared fluorescence (NIRF) was suggested to reduce the ischemic zone while reducing the risk of PSM and reduce the impact on eGFR after RPN (113). A retrospective study by Takahara et al. demonstrated that selective clamping resulted in greater blood loss with no benefit in preservation of eGFR (92.0% vs. 91.6% at 12 months) (82). Another study by Badani et al. demonstrated neither benefit nor harm in selective clamping, though this study had extremely short WIT (<15 minutes) (114). These findings have been corroborated by another retrospective cohort study (115).

The use of super-selective clamping strives to clamp tumor-specific vasculature in hopes to further reduce global ischemia. Super-selective clamping has been demonstrated to improve reductions in eGFR after partial nephrectomy at up to 6 months in follow-up compared to conventional RPN with early unclamping (116). Conversely, the recently published EMERALD trial demonstrated no benefit at 6 months in the conventional partial nephrectomy group compared to those undergoing super-selective clamping group. Though blood loss and complication rates were no different between the groups, this study was prematurely stopped due to lack of benefit for super-selective clamping (117). Combined, the current available data suggests that selective and super-selective clamping may lead to increased blood loss while providing limited benefit in preservation of renal function after NSS.

Reconstruction following tumor excision

Renorrhaphy technique

As a tenant of the pentafecta for RPN, urologists strive to minimize complications and preserve renal function. After tumor excision, reconstructive techniques have been postulated to impact eGFR and the risk of complications such as urine leak (118,119). Renorrhaphy techniques include single vs. a double layer closure and running vs. interrupted closure. While few studies existing comparing long-term eGFR as a function of reconstruction method, some studies have reported short-term results. When comparing running vs. interrupted renorrhaphy, a recent systematic review conducted by Bertolo et al. found no differences in peri-operative or functional outcomes. While WIT was higher in the interrupted group due to longer suturing time, this was though to be offset by greater tissue necrosis resulting from the running technique (120,121). Ultimately, WIT does not appear to impact eGFR in the short term, underlying the developing understanding of the relationship between renal ischemia and function (118).

Convention dictates closure of the renal defect in distinct medullary and cortical layers. However, in recent years this dogma has been challenged insofar as single-layer closure has been reported to have decreased reduction in eGFR at the risk of a small increase in urinary fistula rate (120). A study by Bahler et al. investigated the possibility of an isolated, medullary closure alone and found no differences in post-operative outcomes and a decreased loss in ipsilateral renal mass with exclusion of the cortical layer (122). Williams et al. excluded the collecting system closure and closed only the cortical layer using a sliding-clip technique and found no differences in perioperative outcomes or differences in eGFR at 2-year follow-up (123). A more novel study in this regard by Hidas et al. omitted the defect altogether and implemented tissue sealant (CoSeal or BioGlue) in a subset of patients and found improved functional outcomes measured by quantitative dimercaptosuccinic acid (DMSA) scanning (124). A recent meta-analysis of this technique which incorporated six studies demonstrated a reduction in WIT, operative time, and blood loss for those patients in whom suture closure of the defect was substituted by hemostatic agents without any increase in complication rates (125). As such, implementing single-layer renorrhaphy or substituting closure with tissue sealing agents may help to achieve the pentafecta of NSS. Ultimately, reconstruction technique will vary by surgeon; however, many options are available to minimize collateral damage during RPN.

Post-operative drain placement

Partial nephrectomy has a high risk of complications due to its technical complexity (126). As such, many surgeons performing RPN elect to leave a post-operative, closed suction drain as a surgical principle, especially in cases where there is entry into the collecting system, though little evidence to support this is present in the literature. While drains potentially increase patient discomfort and pain, they may allow for earlier detection of post operative hemorrhage and urine leak (127). Contrary to surgeon dogma regarding post-operative drains, a retrospective study of 636 patients from 8 academic centers showed similar complication rates between patients with and without a drain (128). These findings were supported by Beksac et al. who found that reserving drain placement to non-routine cases only, was better than routinely placing drains (129).

While drain placement appears to be unnecessary, many consider drains to have relatively few consequences. Several reports from other surgical fields have reported drain-related complications including retained drain fragments, patient discomfort, and post-operative small bowel obstruction due to drain placement (130,131). Drain placement has also been demonstrated to reduce post-operative length of stay after RPN. Therefore, given the body of evidence it appears routine drain placement can be omitted in routine RPN to prevent patient discomfort and minimize risk of drain related complications while potentially reducing patient length of stay.


Post-operative management

Early recovery after surgery (ERAS)

Advancements in perioperative protocols, including ERAS protocols, have been designed to improve patient outcomes, reduce hospital stays, and reduce post-operative complications. While commonly implemented for major abdominal operations, recently ERAS protocols have been developed for minimally invasive partial nephrectomy. An early study investigated fast-track programs for patients undergoing laparoscopic nephrectomy. The authors found a reduction in length of stay, pain and nausea scores, inpatient morphine equivalent consumption, and improved patient satisfaction scores (132). A recent prospective randomized trial in patients undergoing laparoscopic partial nephrectomy focused on improving pre-operative education, reducing pre-operative fasting, omitting bowel preparation, decreasing intraoperative fluid resuscitation, and early catheter removal as well as early ambulation and feeding. This study demonstrated that patients on an ERAS protocol had fewer complications, earlier return of bowel function, and shorter length of stay compared to controls (133). This has been demonstrated by Sentell et al. in a multi-institutional study which showed single overnight stay did not lead to increased complication rates compared to >1 day stay (134). While ERAS protocols are typically applied to major abdominal cases where longer length of stay and higher post-operative complication rates are expected, the importance of ERAS principals to robotic surgery cannot be overstated. For RPN, practice patterns vary widely; however, the general principals of ERAS seem to improve patient outcomes and increase patient satisfaction. Thus, in patients undergoing RPN, surgeons should focus on minimizing pre-operative fasting, limiting intra-operative fluid resuscitation, utilization of local anesthetics and nerve blocks, and early discontinuation of surgical drains and urethral catheters.


Complications following robotic partial nephrectomy

Robotic partial nephrectomy has advantages over the open approach in several categories; however, many of the same complications are seen with an incidence of up to 33%. Potential complications include injury to other visceral organs, diaphragm injury, small bowel obstruction, fistulae, development of arteriovenous malformation and the more common complications including urinary leak and hemorrhage. Urinary leakage after minimally invasive partial nephrectomy has been reported in up to 1% of patients which is four-fold lower than in open nephrectomy. With increasing experience and use of sliding clip renorrhaphy, urine leakage after RPN can be minimized though the index of suspicion must remain high in patients with persistently elevated surgical drain output or delayed ileus. Post-operative hemorrhage, seen in up to 10% of patients, may be seen acutely or in a delayed fashion associated with pseudoaneurysms. These can be managed with re-exploration or selective angioembolization if needed. Ultimately, these complications can be avoided with meticulous robotic port placement, visualization of instruments during the operation, careful dissection in initial phases of the operation, and optimally placed sliding-clip renorrhaphy sutures (135).


Impact of PSM

As surgeons have successfully performed RPN on T1b and T2 renal masses, the evaluation of PSM rate is critical to examine. While PSM after RPN is relatively uncommon, their presence poses a risk of recurrence. A recent study by Rothberg et al. demonstrated 6.7% of patients in a cohort of 432 patients had PSM after RPN and only 0.6% of patients had disease recurrence after upfront RPN. Survival analysis between those with PSM and negative surgical margins showed no difference in recurrence free survival (136). A multi-institutional analysis demonstrated a similarly low PSM rate of 5.1% and no association between PSM and overall survival (137). As such, PSM after RPN in and of itself does not appear to warrant adjuvant therapy; however, attentive post-operative surveillance should be pursued in lieu of these findings.


Conclusions

Partial nephrectomy remains one of the most commonly performed robotic surgeries and is the recommended management for cT1 renal masses where technically feasible. Technical innovations within urological surgery have led to progressive expansion of the indications for RPN including more hilar and T1b renal masses. In order to perform partial nephrectomy and strive for pentafecta achievement, a variety of pre- and intra-operative imaging techniques including fluorescence marker implementation, and post-operative patient management protocols have been implemented. CEUS has emerged as a promising technique for pre-operative imaging; however, its ability to distinguish many benign from malignant tumors remains uncertain. AR and 3D reconstructions have not been demonstrated to improve reductions in eGFR; however, their usefulness for surgical trainee education cannot be overstated. Intra-operative imaging with ICG and drop-in ultrasound with TilePro technology allow for rapid tumor-parenchyma identification and reductions in WIT leading to shorter operative times and higher rates of negative surgical margins. Newer fluorescence techniques are emerging including folate receptor targeting agents to allow for better tumor-parenchyma delineation; however, head-to-head comparisons are lacking. Optimized renorrhaphy technique and, in particular, substitution of renorrhaphy with sealing agents, may represent the future of renal defect reconstruction after partial nephrectomy. Furthermore, development in post-operative management has led to earlier patient discharge with decreased post-operative complications. While head-to-head studies and randomized controlled trials (RCTs) are lacking, advancements in partial nephrectomy have allowed urologists to decrease WIT, operative time, and time to discharge while achieving the pentafecta of partial nephrectomy. The need for RCTs and cost analysis of these technique merit further investigation.


Acknowledgments

Funding: None.


Footnote

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://tau.amegroups.com/article/view/10.21037/tau-23-107/rc

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References

  1. World Cancer Research Fund International. Available online: https://www.wcrf.org/
  2. Herr HW. A history of partial nephrectomy for renal tumors. J Urol 2005;173:705-8. [Crossref] [PubMed]
  3. Hennessey DB, Wei G, Moon D, et al. Strategies for success: a multi-institutional study on robot-assisted partial nephrectomy for complex renal lesions. BJU Int 2018;121:40-7. [Crossref] [PubMed]
  4. Kerbl DC, McDougall EM, Clayman RV, et al. A history and evolution of laparoscopic nephrectomy: perspectives from the past and future directions in the surgical management of renal tumors. J Urol 2011;185:1150-4. [Crossref] [PubMed]
  5. Gettman MT, Blute ML, Chow GK, et al. Robotic-assisted laparoscopic partial nephrectomy: technique and initial clinical experience with DaVinci robotic system. Urology 2004;64:914-8. [Crossref] [PubMed]
  6. Patel TH, Babbar P, Hemal AK. The emergence of surgeon-controlled robotic surgery in urologic oncology. Indian J Surg Oncol 2012;3:77-84. [Crossref] [PubMed]
  7. Hung AJ, Cai J, Simmons MN, et al. "Trifecta" in partial nephrectomy. J Urol 2013;189:36-42. [Crossref] [PubMed]
  8. Cerrato C, Patel D, Autorino R, et al. Partial or radical nephrectomy for complex renal mass: a comparative analysis of oncological outcomes and complications from the ROSULA (Robotic Surgery for Large Renal Mass) Collaborative Group. World J Urol 2023;41:747-55. [Crossref] [PubMed]
  9. Delto JC, Paulucci D, Helbig MW, et al. Robot-assisted partial nephrectomy for large renal masses: a multi-institutional series. BJU Int 2018;121:908-15. [Crossref] [PubMed]
  10. Sunaryo PL, Paulucci DJ, Okhawere K, et al. A multi-institutional analysis of 263 hilar tumors during robot-assisted partial nephrectomy. J Robot Surg 2020;14:585-91. [Crossref] [PubMed]
  11. Reynolds CR, Delto JC, Paulucci DJ, et al. Comparison of perioperative and functional outcomes of robotic partial nephrectomy for cT1a vs cT1b renal masses. BJU Int 2017;120:842-7. [Crossref] [PubMed]
  12. Beksac AT, Carbonara U, Abou Zeinab M, et al. Redo Robotic Partial Nephrectomy for Recurrent Renal Tumors: A Multi-Institutional Analysis. J Endourol 2022;36:1296-301. [Crossref] [PubMed]
  13. Sharma G, Shah M, Ahluwalia P, et al. Perioperative outcomes following robot-assisted partial nephrectomy for complex renal masses: A Vattikuti Collective Quality Initiative database study. Indian J Urol 2022;38:288-95. [Crossref] [PubMed]
  14. Martini A, Turri F, Barod R, et al. Salvage Robot-assisted Renal Surgery for Local Recurrence After Surgical Resection or Renal Mass Ablation: Classification, Techniques, and Clinical Outcomes. Eur Urol 2021;80:730-7. [Crossref] [PubMed]
  15. Beksac AT, Okhawere KE, Elbakry AA, et al. Management of high complexity renal masses in partial nephrectomy: A multicenter analysis. Urol Oncol 2019;37:437-44. [Crossref] [PubMed]
  16. Gul Z, Blum KA, Paulucci DJ, et al. A multi-institutional report of peri-operative and functional outcomes after robot-assisted partial nephrectomy in patients with a solitary kidney. J Robot Surg 2019;13:423-8. [Crossref] [PubMed]
  17. Zargar H, Allaf ME, Bhayani S, et al. Trifecta and optimal perioperative outcomes of robotic and laparoscopic partial nephrectomy in surgical treatment of small renal masses: a multi-institutional study. BJU Int 2015;116:407-14. [Crossref] [PubMed]
  18. Pandolfo SD, Beksac AT, Derweesh I, et al. Percutaneous Ablation vs Robot-Assisted Partial Nephrectomy for Completely Endophytic Renal Masses: A Multicenter Trifecta Analysis with a Minimum 3-Year Follow-Up. J Endourol 2023;37:279-85. [Crossref] [PubMed]
  19. Capitanio U, Bensalah K, Bex A, et al. Epidemiology of Renal Cell Carcinoma. Eur Urol 2019;75:74-84. [Crossref] [PubMed]
  20. Partin AW, Dmochowski RR, Kavoussi LR, et al. Chapter 57: Campbell-Walsh-Wein Urology. 12th ed. Amsterdam, The Netherlands: Elsevier; 2020.
  21. Kang SK, Zhang A, Pandharipande PV, et al. DWI for Renal Mass Characterization: Systematic Review and Meta-Analysis of Diagnostic Test Performance. AJR Am J Roentgenol 2015;205:317-24. [Crossref] [PubMed]
  22. Lanzman RS, Robson PM, Sun MR, et al. Arterial spin-labeling MR imaging of renal masses: correlation with histopathologic findings. Radiology 2012;265:799-808. [Crossref] [PubMed]
  23. Roussel E, Capitanio U, Kutikov A, et al. Novel Imaging Methods for Renal Mass Characterization: A Collaborative Review. Eur Urol 2022;81:476-88. [Crossref] [PubMed]
  24. Singh H, Arora G, Nayak B, et al. Semi-quantitative F-18-FDG PET/computed tomography parameters for prediction of grade in patients with renal cell carcinoma and the incremental value of diuretics. Nucl Med Commun 2020;41:485-93. [Crossref] [PubMed]
  25. Zhu H, Zhao S, Zuo C, et al. FDG PET/CT and CT Findings of Renal Cell Carcinoma With Sarcomatoid Differentiation. AJR Am J Roentgenol 2020;215:645-51. [Crossref] [PubMed]
  26. Zhao Y, Wu C, Li W, et al. 2-[18F]FDG PET/CT parameters associated with WHO/ISUP grade in clear cell renal cell carcinoma. Eur J Nucl Med Mol Imaging 2021;48:570-9. [Crossref] [PubMed]
  27. Nakajima R, Abe K, Kondo T, et al. Clinical role of early dynamic FDG-PET/CT for the evaluation of renal cell carcinoma. Eur Radiol 2016;26:1852-62. [Crossref] [PubMed]
  28. Divgi CR, Uzzo RG, Gatsonis C, et al. Positron emission tomography/computed tomography identification of clear cell renal cell carcinoma: results from the REDECT trial. J Clin Oncol 2013;31:187-94. [Crossref] [PubMed]
  29. Conroy R. 89Zr-DFO-Girentuximab PET Agent Meets Specificity and Sensitivity End Points in Clear Cell RCC. [accessed 2 January 2023]. Available online: https://www.cancernetwork.com/view/89zr-dfo-girentuximab-pet-agent-meets-specificity-and-sensitivity-end-points-in-clear-cell-rcc
  30. Posada Calderon L, Eismann L, Reese SW, et al. Advances in Imaging-Based Biomarkers in Renal Cell Carcinoma: A Critical Analysis of the Current Literature. Cancers (Basel) 2023;15:354. [Crossref] [PubMed]
  31. Correas JM, Claudon M, Tranquart F, et al. The kidney: imaging with microbubble contrast agents. Ultrasound Q 2006;22:53-66. [PubMed]
  32. Russo P, Uzzo RG, Lowrance WT, et al. Incidence of benign versus malignant renal tumors in selected studies. J Clin Oncol 2012;30:abstr 357.
  33. Tufano A, Drudi FM, Angelini F, et al. Contrast-Enhanced Ultrasound (CEUS) in the Evaluation of Renal Masses with Histopathological Validation-Results from a Prospective Single-Center Study. Diagnostics (Basel) 2022;12:1209. [Crossref] [PubMed]
  34. Xu ZF, Xu HX, Xie XY, et al. Renal cell carcinoma and renal angiomyolipoma: differential diagnosis with real-time contrast-enhanced ultrasonography. J Ultrasound Med 2010;29:709-17. [Crossref] [PubMed]
  35. Wei SP, Xu CL, Zhang Q, et al. Contrast-enhanced ultrasound for differentiating benign from malignant solid small renal masses: comparison with contrast-enhanced CT. Abdom Radiol (NY) 2017;42:2135-45. [Crossref] [PubMed]
  36. Tufano A, Antonelli L, Di Pierro GB, et al. Diagnostic Performance of Contrast-Enhanced Ultrasound in the Evaluation of Small Renal Masses: A Systematic Review and Meta-Analysis. Diagnostics (Basel) 2022;12:2310. [Crossref] [PubMed]
  37. Borghesi M, Brunocilla E, Volpe A, et al. Active surveillance for clinically localized renal tumors: An updated review of current indications and clinical outcomes. Int J Urol 2015;22:432-8. [Crossref] [PubMed]
  38. Michiels C, Jambon E, Bernhard JC. Measurement of the Accuracy of 3D-Printed Medical Models to Be Used for Robot-Assisted Partial Nephrectomy. AJR Am J Roentgenol 2019;213:626-31. [Crossref] [PubMed]
  39. Cacciamani GE, Medina LG, Gill TS, et al. Impact of Renal Hilar Control on Outcomes of Robotic Partial Nephrectomy: Systematic Review and Cumulative Meta-analysis. Eur Urol Focus 2019;5:619-35. [Crossref] [PubMed]
  40. Xu J, Xu S, Yao B, et al. Segmental artery clamping versus main renal artery clamping in nephron-sparing surgery: updated meta-analysis. World J Surg Oncol 2020;18:210. [Crossref] [PubMed]
  41. Scott ER, Singh A, Quinn AM, et al. The use of individualized 3D-printed models on trainee and patient education, and surgical planning for robotic partial nephrectomies. J Robot Surg 2023;17:465-72. [Crossref] [PubMed]
  42. Fan G, Meng Y, Zhu S, et al. Three-dimensional printing for laparoscopic partial nephrectomy in patients with renal tumors. J Int Med Res 2019;47:4324-32. [Crossref] [PubMed]
  43. Carrion DM, Rodriguez-Socarrás ME, Mantica G, et al. Current status of urology surgical training in Europe: an ESRU-ESU-ESUT collaborative study. World J Urol 2020;38:239-46. [Crossref] [PubMed]
  44. Monda SM, Weese JR, Anderson BG, et al. Development and Validity of a Silicone Renal Tumor Model for Robotic Partial Nephrectomy Training. Urology 2018;114:114-20. [Crossref] [PubMed]
  45. Wake N, Rosenkrantz AB, Huang R, et al. Patient-specific 3D printed and augmented reality kidney and prostate cancer models: impact on patient education. 3D Print Med 2019;5:4.
  46. Lupulescu C, Sun Z. A Systematic Review of the Clinical Value and Applications of Three-Dimensional Printing in Renal Surgery. J Clin Med 2019;8:990. [Crossref] [PubMed]
  47. Carbonara U, Crocerossa F, Campi R, et al. Retroperitoneal Robot-assisted Partial Nephrectomy: A Systematic Review and Pooled Analysis of Comparative Outcomes. Eur Urol Open Sci 2022;40:27-37. [Crossref] [PubMed]
  48. Ali S, Ahn T, Papa N, et al. Changing trends in surgical management of renal tumours from 2000 to 2016: a nationwide study of Medicare claims data. ANZ J Surg 2020;90:48-52. [Crossref] [PubMed]
  49. Pavan N, Derweesh I, Hampton LJ, et al. Retroperitoneal Robotic Partial Nephrectomy: Systematic Review and Cumulative Analysis of Comparative Outcomes. J Endourol 2018;32:591-6. [Crossref] [PubMed]
  50. Arora S, Heulitt G, Menon M, et al. Retroperitoneal vs Transperitoneal Robot-assisted Partial Nephrectomy: Comparison in a Multi-institutional Setting. Urology 2018;120:131-7. [Crossref] [PubMed]
  51. Porpiglia F, Mari A, Amparore D, et al. Transperitoneal vs retroperitoneal minimally invasive partial nephrectomy: comparison of perioperative outcomes and functional follow-up in a large multi-institutional cohort (The RECORD 2 Project). Surg Endosc 2021;35:4295-304. [Crossref] [PubMed]
  52. Fan X, Xu K, Lin T, et al. Comparison of transperitoneal and retroperitoneal laparoscopic nephrectomy for renal cell carcinoma: a systematic review and meta-analysis. BJU Int 2013;111:611-21. [Crossref] [PubMed]
  53. Ren T, Liu Y, Zhao X, et al. Transperitoneal approach versus retroperitoneal approach: a meta-analysis of laparoscopic partial nephrectomy for renal cell carcinoma. PLoS One 2014;9:e91978. [Crossref] [PubMed]
  54. Xia L, Zhang X, Wang X, et al. Transperitoneal versus retroperitoneal robot-assisted partial nephrectomy: A systematic review and meta-analysis. Int J Surg 2016;30:109-15. [Crossref] [PubMed]
  55. Okhawere KE, Rich JM, Ucpinar B, et al. A comparison of outcomes between transperitoneal and retroperitoneal robotic assisted partial nephrectomy in patients with completely endophytic kidney tumors. Urol Oncol 2023;41:111.e1-6. [Crossref] [PubMed]
  56. Paulucci DJ, Beksac AT, Porter J, et al. A Multi-Institutional Propensity Score Matched Comparison of Transperitoneal and Retroperitoneal Partial Nephrectomy for cT1 Posterior Tumors. J Laparoendosc Adv Surg Tech A 2019;29:29-34. [Crossref] [PubMed]
  57. Ghani KR, Porter J, Menon M, et al. Robotic retroperitoneal partial nephrectomy: a step-by-step guide. BJU Int 2014;114:311-3. [Crossref] [PubMed]
  58. Choi CI, Kang M, Sung HH, et al. Comparison by Pentafecta Criteria of Transperitoneal and Retroperitoneal Robotic Partial Nephrectomy for Large Renal Tumors. J Endourol 2020;34:175-83. [Crossref] [PubMed]
  59. Mittakanti HR, Heulitt G, Li HF, et al. Transperitoneal vs. retroperitoneal robotic partial nephrectomy: a matched-paired analysis. World J Urol 2020;38:1093-9. [Crossref] [PubMed]
  60. Paulucci DJ, Abaza R, Eun DD, et al. Robot-assisted partial nephrectomy: continued refinement of outcomes beyond the initial learning curve. BJU Int 2017;119:748-54. [Crossref] [PubMed]
  61. Pathak RA, Patel M, Hemal AK. Comprehensive Approach to Port Placement Templates for Robot-Assisted Laparoscopic Urologic Surgeries. J Endourol 2017;31:1269-76. [Crossref] [PubMed]
  62. Garisto J, Bertolo R, Wilson CA, et al. The evolution and resurgence of perineal prostatectomy in the robotic surgical era. World J Urol 2020;38:821-8. [Crossref] [PubMed]
  63. Kaouk J, Garisto J, Eltemamy M, et al. Step-by-step technique for single-port robot-assisted radical cystectomy and pelvic lymph nodes dissection using the da Vinci(®) SP™ surgical system. BJU Int 2019;124:707-12. [Crossref] [PubMed]
  64. Kaouk J, Garisto J, Eltemamy M, et al. Single-port Robotic Intracorporeal Ileal Conduit Urinary Diversion During Radical Cystectomy Using the SP Surgical System: Step-by-step Technique. Urology 2019;130:196-200. [Crossref] [PubMed]
  65. Hebert KJ, Joseph J, Gettman M, et al. Technical Considerations of Single Port Ureteroneocystostomy Utilizing da Vinci SP Platform. Urology 2019;129:236. [Crossref] [PubMed]
  66. Kang SK, Jang WS, Kim SW, et al. Robot-assisted laparoscopic single-port pyeloplasty using the da Vinci SP® system: initial experience with a pediatric patient. J Pediatr Urol 2019;15:576-7. [Crossref] [PubMed]
  67. Fang AM, Saidian A, Magi-Galluzzi C, et al. Single-port robotic partial and radical nephrectomies for renal cortical tumors: initial clinical experience. J Robot Surg 2020;14:773-80. [Crossref] [PubMed]
  68. Kaouk J, Garisto J, Eltemamy M, et al. Pure Single-Site Robot-Assisted Partial Nephrectomy Using the SP Surgical System: Initial Clinical Experience. Urology 2019;124:282-5. [Crossref] [PubMed]
  69. Glaser ZA, Burns ZR, Fang AM, et al. Single- versus multi-port robotic partial nephrectomy: a comparative analysis of perioperative outcomes and analgesic requirements. J Robot Surg 2022;16:695-703. [Crossref] [PubMed]
  70. Okhawere KE, Beksac AT, Wilson MP, et al. A Propensity-Matched Comparison of the Perioperative Outcomes Between Single-Port and Multi-Port Robotic Assisted Partial Nephrectomy: A Report from the Single Port Advanced Research Consortium (SPARC). J Endourol 2022;36:1526-31. [Crossref] [PubMed]
  71. Landsman ML, Kwant G, Mook GA, et al. Light-absorbing properties, stability, and spectral stabilization of indocyanine green. J Appl Physiol 1976;40:575-83. [Crossref] [PubMed]
  72. Golijanin DJ, Marshall J, Cardin A, et al. Bilitranslocase (BTL) is immunolocalised in proximal and distal renal tubules and absent in renal cortical tumors accurately corresponding to intraoperative near infrared fluorescence (NIRF) expression of renal cortical tumors using intravenous indocyanine green (ICG). J Urol 2008;179:137. [Crossref]
  73. Tobis S, Knopf J, Silvers C, et al. Near infrared fluorescence imaging with robotic assisted laparoscopic partial nephrectomy: initial clinical experience for renal cortical tumors. J Urol 2011;186:47-52. [Crossref] [PubMed]
  74. Borofsky MS, Gill IS, Hemal AK, et al. Near-infrared fluorescence imaging to facilitate super-selective arterial clamping during zero-ischaemia robotic partial nephrectomy. BJU Int 2013;111:604-10. [Crossref] [PubMed]
  75. Manny TB, Krane LS, Hemal AK. Indocyanine green cannot predict malignancy in partial nephrectomy: histopathologic correlation with fluorescence pattern in 100 patients. J Endourol 2013;27:918-21. [Crossref] [PubMed]
  76. Veccia A, Antonelli A, Hampton LJ, et al. Near-infrared Fluorescence Imaging with Indocyanine Green in Robot-assisted Partial Nephrectomy: Pooled Analysis of Comparative Studies. Eur Urol Focus 2020;6:505-12. [Crossref] [PubMed]
  77. Cacciamani GE, Shakir A, Tafuri A, et al. Best practices in near-infrared fluorescence imaging with indocyanine green (NIRF/ICG)-guided robotic urologic surgery: a systematic review-based expert consensus. World J Urol 2020;38:883-96. [Crossref] [PubMed]
  78. Krane LS, Hemal AK. Surgery: Is indocyanine green dye useful in robotic surgery? Nat Rev Urol 2014;11:12-4. [Crossref] [PubMed]
  79. Bjurlin MA, Gan M, McClintock TR, et al. Near-infrared fluorescence imaging: emerging applications in robotic upper urinary tract surgery. Eur Urol 2014;65:793-801. [Crossref] [PubMed]
  80. Harke N, Schoen G, Schiefelbein F, et al. Selective clamping under the usage of near-infrared fluorescence imaging with indocyanine green in robot-assisted partial nephrectomy: a single-surgeon matched-pair study. World J Urol 2014;32:1259-65. [Crossref] [PubMed]
  81. McClintock TR, Bjurlin MA, Wysock JS, et al. Can selective arterial clamping with fluorescence imaging preserve kidney function during robotic partial nephrectomy? Urology 2014;84:327-32. [Crossref] [PubMed]
  82. Takahara K, Kusaka M, Nukaya T, et al. Functional Outcomes after Selective Clamping in Robot-Assisted Partial Nephrectomy. J Clin Med 2022;11:5648. [Crossref] [PubMed]
  83. Krane LS, Manny TB, Hemal AK. Is near infrared fluorescence imaging using indocyanine green dye useful in robotic partial nephrectomy: a prospective comparative study of 94 patients. Urology 2012;80:110-6. [Crossref] [PubMed]
  84. Hemal AK, Golijanin D. Does infrared imaging improve partial nephrectomy for renal cell carcinoma? J Urol 2012;188:1078-80. [Crossref] [PubMed]
  85. Low PS, Kularatne SA. Folate-targeted therapeutic and imaging agents for cancer. Curr Opin Chem Biol 2009;13:256-62. [Crossref] [PubMed]
  86. Hoogstins CE, Tummers QR, Gaarenstroom KN, et al. A Novel Tumor-Specific Agent for Intraoperative Near-Infrared Fluorescence Imaging: A Translational Study in Healthy Volunteers and Patients with Ovarian Cancer. Clin Cancer Res 2016;22:2929-38. [Crossref] [PubMed]
  87. Boogerd LSF, Hoogstins CES, Gaarenstroom KN, et al. Folate receptor-α targeted near-infrared fluorescence imaging in high-risk endometrial cancer patients: a tissue microarray and clinical feasibility study. Oncotarget 2017;9:791-801. [Crossref] [PubMed]
  88. Predina JD, Newton AD, Keating J, et al. A Phase I Clinical Trial of Targeted Intraoperative Molecular Imaging for Pulmonary Adenocarcinomas. Ann Thorac Surg 2018;105:901-8. [Crossref] [PubMed]
  89. Predina JD, Newton AD, Connolly C, et al. Identification of a Folate Receptor-Targeted Near-Infrared Molecular Contrast Agent to Localize Pulmonary Adenocarcinomas. Mol Ther 2018;26:390-403. [Crossref] [PubMed]
  90. Lee JYK, Cho SS, Zeh R, et al. Folate receptor overexpression can be visualized in real time during pituitary adenoma endoscopic transsphenoidal surgery with near-infrared imaging. J Neurosurg 2018;129:390-403. [Crossref] [PubMed]
  91. Predina JD, Newton A, Deshpande C, et al. Utilization of targeted near-infrared molecular imaging to improve pulmonary metastasectomy of osteosarcomas. J Biomed Opt 2018;23:1-4. [Crossref] [PubMed]
  92. Shum CF, Bahler CD, Low PS, et al. Novel Use of Folate-Targeted Intraoperative Fluorescence, OTL38, in Robot-Assisted Laparoscopic Partial Nephrectomy: Report of the First Three Cases. J Endourol Case Rep 2016;2:189-97. [Crossref] [PubMed]
  93. Sulek JE, Steward JE, Bahler CD, et al. Folate-targeted intraoperative fluorescence, OTL38, in robotic-assisted laparoscopic partial nephrectomy. Scand J Urol 2021;55:331-6. [Crossref] [PubMed]
  94. Kaczmarek BF, Sukumar S, Kumar RK, et al. Comparison of robotic and laparoscopic ultrasound probes for robotic partial nephrectomy. J Endourol 2013;27:1137-40. [Crossref] [PubMed]
  95. Zhang Y, Ouyang W, Wu B, et al. Robot-assisted partial nephrectomy with a standard laparoscopic ultrasound probe in treating endophytic renal tumor. Asian J Surg 2020;43:423-7. [Crossref] [PubMed]
  96. Hyams ES, Perlmutter M, Stifelman MD. A prospective evaluation of the utility of laparoscopic Doppler technology during minimally invasive partial nephrectomy. Urology 2011;77:617-20. [Crossref] [PubMed]
  97. Li QL, Guan HW, Wang FP, et al. Significance of margin in nephron sparing surgery for renal cell carcinoma of 4 cm or less. Chin Med J (Engl) 2008;121:1662-5. [Crossref] [PubMed]
  98. Lam JS, Bergman J, Breda A, et al. Importance of surgical margins in the management of renal cell carcinoma. Nat Clin Pract Urol 2008;5:308-17. [Crossref] [PubMed]
  99. Clark MA, Shikanov S, Raman JD, et al. Chronic kidney disease before and after partial nephrectomy. J Urol 2011;185:43-8. [Crossref] [PubMed]
  100. Thompson RH, Lane BR, Lohse CM, et al. Every minute counts when the renal hilum is clamped during partial nephrectomy. Eur Urol 2010;58:340-5. [Crossref] [PubMed]
  101. Campbell SC, Novick AC, Belldegrun A, et al. Guideline for management of the clinical T1 renal mass. J Urol 2009;182:1271-9. [Crossref] [PubMed]
  102. Rosen DC, Kannappan M, Paulucci DJ, et al. Reevaluating Warm Ischemia Time as a Predictor of Renal Function Outcomes After Robotic Partial Nephrectomy. Urology 2018;120:156-61. [Crossref] [PubMed]
  103. Di Cosmo G, Verzotti E, Silvestri T, et al. Intraoperative ultrasound in robot-assisted partial nephrectomy: State of the art. Arch Ital Urol Androl 2018;90:195-8. [Crossref] [PubMed]
  104. Alenezi A, Motiwala A, Eves S, et al. Robotic assisted laparoscopic partial nephrectomy using contrast-enhanced ultrasound scan to map renal blood flow. Int J Med Robot 2017;13:e1738. [Crossref] [PubMed]
  105. Porpiglia F, Amparore D, Checcucci E, et al. Current Use of Three-dimensional Model Technology in Urology: A Road Map for Personalised Surgical Planning. Eur Urol Focus 2018;4:652-6. [Crossref] [PubMed]
  106. Veneziano D, Amparore D, Cacciamani G, et al. Climbing over the Barriers of Current Imaging Technology in Urology. Eur Urol 2020;77:142-3. [Crossref] [PubMed]
  107. Piramide F, Amparore D, Pecararo A. Augmented reality 3D robotic assisted partial nephrectomy: tips and tricks to improve surgical strategies and outcomes. Urology Video Journal 2022;13:100137. [Crossref]
  108. Greco F, Autorino R, Altieri V, et al. Ischemia Techniques in Nephron-sparing Surgery: A Systematic Review and Meta-Analysis of Surgical, Oncological, and Functional Outcomes. Eur Urol 2019;75:477-91. [Crossref] [PubMed]
  109. Antonelli A, Cindolo L, Sandri M, et al. Safety of on- vs off-clamp robotic partial nephrectomy: per-protocol analysis from the data of the CLOCK randomized trial. World J Urol 2020;38:1101-8. [Crossref] [PubMed]
  110. Krane LS, Mufarrij PW, Manny TB, et al. Comparison of clamping technique in robotic partial nephrectomy: does unclamped partial nephrectomy improve perioperative outcomes and renal function? Can J Urol 2013;20:6662-7. [PubMed]
  111. Rosen DC, Paulucci DJ, Abaza R, et al. Is Off Clamp Always Beneficial During Robotic Partial Nephrectomy? A Propensity Score-Matched Comparison of Clamp Technique in Patients with Two Kidneys. J Endourol 2017;31:1176-82. [Crossref] [PubMed]
  112. Blum KA, Paulucci DJ, Abaza R, et al. Main Renal Artery Clamping With or Without Renal Vein Clamping During Robotic Partial Nephrectomy for Clinical T1 Renal Masses: Perioperative and Long-term Functional Outcomes. Urology 2016;97:118-23. [Crossref] [PubMed]
  113. Diana P, Buffi NM, Lughezzani G, et al. The Role of Intraoperative Indocyanine Green in Robot-assisted Partial Nephrectomy: Results from a Large, Multi-institutional Series. Eur Urol 2020;78:743-9. [Crossref] [PubMed]
  114. Badani KK, Kothari PD, Okhawere KE, et al. Selective clamping during robot-assisted partial nephrectomy in patients with a solitary kidney: is it safe and does it help? BJU Int 2020;125:893-7. [Crossref] [PubMed]
  115. Paulucci DJ, Rosen DC, Sfakianos JP, et al. Selective arterial clamping does not improve outcomes in robot-assisted partial nephrectomy: a propensity-score analysis of patients without impaired renal function. BJU Int 2017;119:430-5. [Crossref] [PubMed]
  116. Lanchon C, Arnoux V, Fiard G, et al. Super-selective robot-assisted partial nephrectomy using near-infrared flurorescence versus early-unclamping of the renal artery: results of a prospective matched-pair analysis. Int Braz J Urol 2018;44:53-62. [Crossref] [PubMed]
  117. Long JA, Fiard G, Giai J, et al. Superselective Ischemia in Robotic Partial Nephrectomy Does Not Provide Better Long-term Renal Function than Renal Artery Clamping in a Randomized Controlled Trial (EMERALD): Should We Take the Risk? Eur Urol Focus 2022;8:769-76. [Crossref] [PubMed]
  118. Volpe A, Blute ML, Ficarra V, et al. Renal Ischemia and Function After Partial Nephrectomy: A Collaborative Review of the Literature. Eur Urol 2015;68:61-74. [Crossref] [PubMed]
  119. Dagenais J, Maurice MJ, Mouracade P, et al. Excisional Precision Matters: Understanding the Influence of Excisional Volume Loss on Renal Function After Partial Nephrectomy. Eur Urol 2017;72:168-70. [Crossref] [PubMed]
  120. Bertolo R, Campi R, Mir MC, et al. Systematic Review and Pooled Analysis of the Impact of Renorrhaphy Techniques on Renal Functional Outcome After Partial Nephrectomy. Eur Urol Oncol 2019;2:572-5. [Crossref] [PubMed]
  121. Bertolo R, Campi R, Klatte T, et al. Suture techniques during laparoscopic and robot-assisted partial nephrectomy: a systematic review and quantitative synthesis of peri-operative outcomes. BJU Int 2019;123:923-46. [Crossref] [PubMed]
  122. Bahler CD, Dube HT, Flynn KJ, et al. Feasibility of omitting cortical renorrhaphy during robot-assisted partial nephrectomy: a matched analysis. J Endourol 2015;29:548-55. [Crossref] [PubMed]
  123. Williams RD, Snowden C, Frank R, et al. Has Sliding-Clip Renorrhaphy Eliminated the Need for Collecting System Repair During Robot-Assisted Partial Nephrectomy? J Endourol 2017;31:289-94. [Crossref] [PubMed]
  124. Hidas G, Lupinsky L, Kastin A, et al. Functional significance of using tissue adhesive substance in nephron-sparing surgery: assessment by quantitative SPECT of 99m Tc-Dimercaptosuccinic acid scintigraphy. Eur Urol 2007;52:785-9. [Crossref] [PubMed]
  125. Guo Q, Lin Y, Zhang C, et al. Hemostatic Agent May Improve Perioperative Outcomes in Partial Nephrectomy: A Systematic Review and Meta-Analysis. Urol Int 2022;106:352-9. [Crossref] [PubMed]
  126. Stephenson AJ, Hakimi AA, Snyder ME, et al. Complications of radical and partial nephrectomy in a large contemporary cohort. J Urol 2004;171:130-4. [Crossref] [PubMed]
  127. Nora PF, Vanecko RM, Bransfield JJ. Prophylactic abdominal drains. Arch Surg 1972;105:173-6. [Crossref] [PubMed]
  128. Peyronnet B, Pradère B, De La Taille A, et al. Postoperative drainage does not prevent complications after robotic partial nephrectomy. World J Urol 2016;34:933-8. [Crossref] [PubMed]
  129. Beksac AT, Okhawere KE, Meilika K, et al. Should a Drain Be Routinely Required After Transperitoneal Robotic Partial Nephrectomy? J Endourol 2020;34:964-8. [Crossref] [PubMed]
  130. Poon CM, Leong HT. Abdominal drain causing early small bowel obstruction after laparoscopic colectomy. JSLS 2009;13:625-7. [PubMed]
  131. Stawicki SP, Evans DC, Cipolla J, et al. Retained surgical foreign bodies: a comprehensive review of risks and preventive strategies. Scand J Surg 2009;98:8-17. [Crossref] [PubMed]
  132. Recart A, Duchene D, White PF, et al. Efficacy and safety of fast-track recovery strategy for patients undergoing laparoscopic nephrectomy. J Endourol 2005;19:1165-9. [Crossref] [PubMed]
  133. Miao C, Yu A, Yuan H, et al. Effect of Enhanced Recovery After Surgery on Postoperative Recovery and Quality of Life in Patients Undergoing Laparoscopic Partial Nephrectomy. Front Oncol 2020;10:513874. [Crossref] [PubMed]
  134. Sentell KT, Badani KK, Paulucci DJ, et al. A Single Overnight Stay After Robotic Partial Nephrectomy Does Not Increase Complications. J Endourol 2019;33:1003-8. [Crossref] [PubMed]
  135. Gabrielson AT, Faisal FA, Pierorazio PM. Management of acute post-operative hemorrhage following partial nephrectomy with renal artery embolization. Urol Case Rep 2020;32:101252. [Crossref] [PubMed]
  136. Rothberg MB, Peak TC, Reynolds CR, et al. Long-term oncologic outcomes of positive surgical margins following robot-assisted partial nephrectomy. Transl Androl Urol 2020;9:879-86. [Crossref] [PubMed]
  137. Rothberg MB, Paulucci DJ, Okhawere KE, et al. A Multi-Institutional Analysis of the Effect of Positive Surgical Margins Following Robot-Assisted Partial Nephrectomy on Oncologic Outcomes. J Endourol 2020;34:304-11. [Crossref] [PubMed]
Cite this article as: Thakker PU, O’Rourke TK Jr, Hemal AK. Technologic advances in robot-assisted nephron sparing surgery: a narrative review. Transl Androl Urol 2023;12(7):1184-1198. doi: 10.21037/tau-23-107

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