IMR Press / CEOG / Volume 50 / Issue 6 / DOI: 10.31083/j.ceog5006123
Open Access Review
Robotic Pelvic Lymphadenectomy in Gynecological and Urological Malignancies
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1 Urology Department, Faculty of Medicine, Tanta University, 31527 Tanta, Egypt
2 Urology Department, ASST Santi Paolo e Carlo, University of Milan, 20142 Milan, Italy
3 Urology Department, University of Modena & Reggio Emilia, 41126 Modena, Italy
4 ORSI Academy, 9090 Melle, Belgium
5 Obstetrics and Gynecology Department, ASST Santi Paolo e Carlo, 20142 Milan, Italy
*Correspondence: ahmed.essa@med.tanta.edu.eg (Ahmed Eissa)
Clin. Exp. Obstet. Gynecol. 2023, 50(6), 123; https://doi.org/10.31083/j.ceog5006123
Submitted: 18 November 2022 | Revised: 10 January 2023 | Accepted: 19 January 2023 | Published: 30 May 2023
Copyright: © 2023 The Author(s). Published by IMR Press.
This is an open access article under the CC BY 4.0 license.
Abstract

Objectives: Pelvic lymphadenectomy is a crucial step in the management of different pelvic cancers for both prognostic and/or therapeutic goals. Robotic surgeries offered numerous benefits over open and/or laparoscopic surgeries such as better visualization, shorter hospital stay, less pain and better cosmoses. The aim of this narrative review is to evaluate the value and outcomes of robotic pelvic lymph node dissection (PLND). Mechanism: The PubMed database was searched using the following keywords “Robotic” AND “pelvic lymph node dissection” to identify all the relevant articles concerned with the role and outcomes of robotic PLND. We included only English articles published between 2010 and 2022. Data from the retrieved articles were then used to formulate this review that highlight the introduction, the outcomes of robotic pelvic lymph node dissection (PLND), and the mapping of sentinel lymph node (SLN) in cervical, endometrial, prostate, and bladder cancers. Findings in Brief: PLND is an integral part of gynecological and urological oncology for its role in tumor staging and planning of further treatment plan. Furthermore, it may play an important therapeutic role in bladder cancer. Robotic approach to PLND is safe and efficient and can be potentially used for cervical, endometrial, prostate, and bladder cancers. Conclusions: Robotic PLND could be an alternative to open and laparoscopic approaches as it may decrease the associated morbidities without compromising the quality of Lymph node dissection (LND).

Keywords
pelvic lymph node dissection
robotic surgery
bladder cancer
cervical cancer
endometrial cancer
prostate cancer
1. Introduction

The core concept of surgical oncology is the radicalness, which includes the resection of the primary tumor, the surrounding tissues, and loco-regional lymph nodes [1]. Loco-regional (20.5%) and distant (12.9%) lymph nodes (LN) represent the most common sites of metastasis, which justify the inclusion of lymph node dissection as an important step in the surgical management of different solid tumors [2]. Pelvic malignancies are not exception, where pelvic lymph node dissection (PLND) is considered an integral part of the management of several pelvic malignancies for prognostic and/or therapeutic purposes including cervical cancer [3], endometrial carcinoma [4], bladder cancer [5], and prostate cancer [6]. Despite the significance of PLND in pelvic oncological surgeries, it may be associated with increased morbidity and cost. Therefore, surgeons are obliged to weigh the potential benefits of PLND against its inherent drawbacks [7].

The advent of robotic technology to the surgical field offered several advantages to both surgeons and patients in the form of three-dimensional vision, 10× magnification, tremor filtration, endo-wrist instruments, shorter learning curve compared to laparoscopic approaches, better cosmetic outcomes, shorter hospital stay, less estimated blood loss, and less post-operative pain [8, 9, 10]. Thus, these technical advantages may theoretically enhance the outcomes of PLND especially in the narrow pelvic region [11]. In these settings, this narrative review aims at exploring the value and outcomes of robotic PLND.

2. Methodology

The PubMed database was searched using the following keywords “Robotic” AND “pelvic lymph node dissection” to identify all the relevant articles concerned with the role and outcomes of robotic PLND. Several search filters were applied to limit the search to only English articles published between 2010 and 2022. Data from the retrieved articles were then used for the formalization of the current narrative review.

3. Cervical Cancer
3.1 Introduction

Cervical cancer is the fourth most commonly diagnosed female cancer accounting for approximately 6.5% and 7.7% of all newly diagnosed female cancers and cancer specific-mortality in 2020, respectively [12]. Radical hysterectomy is the standard treatment option for early-stage cervical cancer (stage IA1-IB2), which was performed in an open approach for more than 100 years until minimally invasive approaches (laparoscopic and robotic-assisted laparoscopic) were adopted in the field of gynecological oncology [13]. However, it should be noted that the rate of minimally invasive radical hysterectomy has dramatically decreased over the last four years [14], following the publication of a phase three randomized controlled trial (RCTs) reporting that minimally invasive approaches to radical hysterectomy may be associated with worse disease-free survival (86.0% vs 96.5%) and overall survival (93.8% vs 99%) compared to open approaches [15]. Yet, it is worth mentioning that this trial was not devoid of limitations and concerns (mainly related to the difference in surgeon’s experience, centers’ volume, and only 15.6% of the patients undergone robotic-assisted approach) that might have affected the outcomes and thus minimally invasive approaches should not be completely abended [13]. Furthermore, a retrospective analysis of patients undergoing robotic-assisted laparoscopic radical hysterectomy (RALRH) for early-stage cervical cancer in Spain showed that centers with higher surgical volume, more participation in clinical trials, greater use of magnetic resonance imaging (MRI) for diagnosis, favorable learning curve, and higher use of sentinel lymph node biopsies usually report lower rates of recurrences and better oncological outcomes, highlighting the impact of surgical practice on the oncological outcomes of RALRH [16].

Radical trachelectomy is another option for the management of selected patients with small early-stage cervical carcinoma (<2 cm) wishing to preserve fertility. It consists of the resection of the cervix, upper vagina, and parametrium [17]. An international retrospective analysis of 646 patients undergoing radical trachelectomy (358 patients undergone open approach, and 288 patients undergone minimally invasive approach), reported comparable 4.5 years disease-free survival (94.3% vs 91.5%, p = 0.37) and overall survival (99.2% vs 99%, p = 0.49) among open and minimally invasive approaches, respectively [18].

Pelvic Lymph node metastasis is not rare in patients with early-stage cervical cancer, where it may range from 2% in patients with stage IA2 tumors to 14–36% in patients with stage IB tumors; while, para-aortic lymph node metastasis is less common (2–5% in patients with stage IB tumors) [19]. Thus, regardless the chosen treatment option (radical hysterectomy or radical trachelectomy), bilateral PLND remains an important step in the management plan of early-stage cervical cancer as the lymph node status is the most crucial prognostic factor and plays an essential role in guiding adjuvant protocols [20].

3.2 Robotic PLND in Cervical Cancer

Generally, minimally invasive approaches appear to be an attractive alternative to open pelvic lymphadenectomy with comparable surgical and oncological outcomes [21, 22]. Despite the controversy regarding the value of nodal yield on the survival of patients with negative lymph nodes, a more extensive lymph node dissection theoretically improves the pathological accuracy of lymph node status as a greater number of retrieved lymph nodes potentially increase the chance of detecting and resecting micro-metastasis [3]. Thus, the number of retrieved pelvic lymph nodes remains a surrogate marker of the extent and quality of surgery [23]. Table 1 (Ref. [15, 18, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38]) shows a summary of nodal yield in the included studies about different approaches to radical hysterectomy. Considering comparative trials, the majority of authors reported a comparable nodal yield among different surgical approaches (16–36 for robotic, 14–27 for laparoscopic, 17–25 for open) [21, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 39]. On the contrary, some studies demonstrated a significantly higher nodal yield for the open approach [36, 37], while others supported the superiority of minimally invasive approaches [22, 38].

Table 1.Summary of included studies about the comparison of nodal yield, operative times, blood loss, and hospitalization in patients undergoing different approaches to radical hysterectomy for cervical cancer.
Article Approach Patients Nodal yield Operative time (min) Blood loss (mL) Hospital stay (days)
Salvo et al. [18] Open-RT 358 17 171 200 6
MIS-RT 288 18 262 50 2
Gao et al. [24] RSS-RH 32 21.37 223.56 217.25 7.5
LESS-RH 35 20.71 248.61 294.74 7.17
Ding et al. [28] 2D-LRH 54 21.7 151.6 233.5 10.4
3D-LRH 85 23 111.8 211.6 10.7
RALRH 100 22.4 171.6 317.5 10.9
Ramirez et al. [15] Open-RH 312 21 NA NA 5
MIS-RH 319 20 NA NA 3
Pellegrino et al. [29] RALRH 34 35.58 227.64 67.88 2.58
LRH 18 24.23 242.87 203.33 3.27
Nie et al. [30] RALRH 100 22.39 171.64 317.5 10.41
LRH 833 22.51 192.1 322.51 11.5
Wallin et al. [36] Open-RH 155 28.9 197 596 6.3
RALRH 149 22.7 206 80.9 2.4
Diver et al. [38] MIS-RH 101 19.4 NA 50 1.9
Open-RH 282 16 NA 500 4.9
Li et al. [31] 3D-LRH 24 18.08 222 325 15.54
RALRH 37 16.05 215.84 309.73 15.57
Corrado et al. [32] Open-RH 43 25 290 480 8
LRH 41 20 220 250 6
RALRH 41 23 180 150 4
Corrado et al. [33] Mini-LRH 30 17.5 180 50 2
RALRH 30 20 185 60 3
Yim et al. [34] RALRH 60 18 200.5 100 11
LRH 42 19.9 215.6 145 10
Vizza et al. [35] LRH 25 21 188 220 6
RALRH 25 23 190 160 4
Tinelli et al. [25] LRH 76 27.1 255 95 4
RALRH 23 24.7 323 157 3
Sert et al. [37] RALRH 35 19.5 263.8 82.8 3.8
LRH 7 15.4 364.2 164.2 8.4
Open-RH 26 26.1 163.4 595 9.2
Schreuder et al. [27] RALRH 13 29 434 300 4
Open-RH 14 26 225 2000 9
Nam et al. [26] RALRH 32 20.2 218.8 220.9 11.6
Open-RH 32 24.2 209.9 531.5 16.9

MIS, minimally invasive surgery; RH, radical hysterectomy; NA, not available; RT, radical trachelectomy; RSS, robotic single site surgery; LESS, laparoendoscopic single site surgery; LRH, laparoscopic radical hysterectomy; RALRH, robotic-assisted laparoscopic radical hysterectomy; 2D, two-dimensional; 3D, three-dimensional.

Noteworthy, the minimally invasive approaches offer several advantages in the form of less estimated blood loss (50–317.5 mL for robotic [18, 30, 37, 38], 50–325 mL for laparoscopic [31, 33], and 200–2000 mL for open approach [18, 27]) and shorter hospital stay [18, 27, 32, 36, 37, 38, 39]. However, minimally invasive approaches are usually associated with longer operative times [18, 27, 28, 37, 39].

3.3 Sentinel Lymph Node Mapping (SLN) in Cervical Cancer

The concept of SLNs was initially described by Gould et al. [40], in 1960 for patients with parotid carcinoma, subsequently this concept was introduced to different types of solid malignancies. Generally, SLN may provide the missing balance between the value of PLND and the associated lymphatic complications [41]. SLN mapping is based on the concept that a negative first lymph node group receiving lymphatic drainage from a primary tumor indicates a theoretically negative lymph nodes in the remainder of that basin [42]. In patients with cervical cancer, SLN may be used as an alternative to lymphadenectomy only in patients with early-stage cervical carcinoma and tumors <2 cm due to its low sensitivity and detection rates [43]. However, this recommendation was based mainly on studies that typically use radiocolloid tracer (99Technetium (99Tm)) either alone or in combination with blue dye [44]. Indocyanine Green (ICG) is another dye introduced for the use in cervical carcinoma few years ago. Several authors studied the value of ICG during RALRH reporting a SLN detection rate ranging from 86% to 100% and a rate of bilateral mapping ranging from 55% to 98.5% [41, 42, 45, 46]. Similarly, Luhrs et al. [41] indicated that ICG was associated with higher SLN detection rates compared to 99Tm. Furthermore, the authors reported that combining ICG with 99Tm did not improve the bilateral detection rates of SLNs [41]. On the same hand, Kim et al. [46], demonstrated that the sensitivity, specificity, negative predictive value (NPV), false negative rates (FNR), and accuracy, are generally affected by the tumor size supporting the previous recommendations, where they were 71.43%, 100%, 28.57%, 93.98%, and 94.76% when all tumor sizes (ranging from 0.1–8 cm) were considered, while they improved to 100%, 100%, 0%, 100%, and 100% when only patients with primary tumor <2 cm in size and no lymphadenopathy on imaging were considered. Yet, further studies are required to support the use of ICG guided SLNs as an alternative to lymphadenectomy in patients with cervical cancer.

4. Endometrial Cancer
4.1 Introduction

Endometrial cancer (ECa) is the fifth most commonly diagnosed malignancy in women. Unlike other solid tumors, ECa is showing an increasing incidence and mortality in developed and high-income countries [47]. Surgery remains the cornerstone management for patients with ECa. It includes the radical resection of cervix, uterus, fallopian tubes, and ovaries. Lymph node dissection (LND) is a fundamental part of this surgery as it may provide staging information and guide adjuvant therapy [48]. The decision and extent of LND in patients with ECa is still a matter of debate and is dependable on the preoperative findings (tumor grade, size, site, and myometrial invasion) together with the surgeon’s evaluation of all the peritoneal surfaces, pelvic and para-aortic lymph nodes because the lymphatic drainage of the uterus is not limited to the pelvic lymph nodes but it may have a direct lymphatic communication between the fundus of the uterus and the aortic lymph node chains [49]. Generally, this surgery can be performed either through an open, laparoscopic, or robotic approaches. Studies about the minimally invasive approaches (laparoscopic and robotic) in the management of early and advanced ECa supported the advantages of these approaches over laparotomy as regards blood loss, recovery, and hospital stay without compromising the complication rates and oncological outcomes [48]. However, similar to cervical cancer, some concerns were raised regarding the long-term oncological outcomes (recurrence-free survival, overall survival, and disease-specific survival) of robotic surgery compared to laparoscopic surgery [50]. Yet, the robotic approach is still an interesting option for the surgical treatment of patients with ECa.

As previously mentioned, the lymphatic drainage of the uterus includes both pelvic and para-aortic lymph nodes rendering lymph node metastasis in ECa patients a challenging situation as it greatly affects patients’ 5-years survival (94% for patients with negative lymph nodes, 75% for patients with positive pelvic nodes, and 38% for patients with positive para-aortic nodes) [51]. Pelvic lymph node metastasis ranges from 3.8–15.2%, 7.3–17.1%, and 6.9–35.3% in low-grade, intermediate-grade, and high-grade tumors, respectively. Similarly, aortic lymph node metastasis ranges from 0.8–9.4%, 5.3–20.5%, 0–25% in low-grade, intermediate-grade, and high-grade tumors, respectively [52]. Overall, the risk of paraaortic lymph node metastasis is 50% in case of positive pelvic lymph nodes, while isolated positive aortic lymph nodes are reported in only 2–3% of patients [49]. Tumor size is another predictor of lymph node metastasis in those patients; however, the cutoff size is controversial in the literature ranging from 2–5 cm. A recent systematic review and meta-analysis of 40 articles identified 2 cm as the ideal cutoff size for prediction of lymph node metastasis (odds ratio (OR) = 4.11, 95% confidence interval (CI) 3.36–4.66, p < 0.001).

4.2 Robotic PLND in Endometrial Cancer

Several studies assessed the value of robotic surgery during lymphadenectomy in ECa patients [53, 54]. Generally, compared to open and laparoscopic approaches, robotic surgery was associated with a comparable nodal yield (10.5–13 for open and 11–13 for robotic) [53, 54, 55, 56], even in obese patients (pelvic nodes 18 vs 14, aortic nodes 9 vs 3) [53]. On the contrary, Backes et al. [57] reported that robotic approach may be associated with significantly lower pelvic nodal yield compared to laparotomy (15 vs 18, p = 0.007), while the aortic nodal yield was not statistically different. Interestingly, minimally invasive surgeries were associated with higher rates of pelvic lymphadenectomy compared to open surgery [55, 57].

Robotic single site docking is a feasible option in patients undergoing robotic hysterectomy and lymphadenectomy (pelvic and/or para-aortic) for surgical staging of ECa with few reported complications including early postoperative complications (8%), lower limb lymphedema (14%), and pelvic lymphocysts (8%) [51, 56, 58]. Noteworthy, retrospective cohorts showed that patients with intermediate- or high-risk ECa should undergo combined pelvic and para-aortic lymphadenectomy as it is associated with better survival outcomes compared to pelvic lymphadenectomy only [59]. Table 2 (Ref. [53, 54, 55, 56, 57]) show a summary of included studies about different approaches to the management of endometrial cancer.

Table 2.Summary of included studies about the comparison of nodal yield, operative times, blood loss, and hospitalization in patients undergoing different approaches to radical hysterectomy for endometrial cancer.
Article Approach Patients Nodal yield Operative time (min) Blood loss (mL) Hospital stay (days)
Bernardini et al. [53] Open-RH 41 14 165 300 4
RALRH 45 18 270 200 2
Eklind et al. [54] RALRH 40 13 127 76 1.8
Open-RH 48 13 179 317 4.8
Pulman et al. [55] Open-RH 69 14 210 300 4
LRH 44 17 240 150 1
RALRH 63 18 240 150 1
Corrado et al. [56] RSS-RH 125 13 122 50 2
Backes et al. [57] Open-RH 93 18 NA 300 4
RALRH 89 15 NA 75 1

RH, Radical Hysterectomy; NA, not available; RSS, robotic single site surgery; LRH, laparoscopic radical hysterectomy; RALRH, Robotic-assisted Laparoscopic Radical Hysterectomy.

4.3 Sentinel Lymph Node Mapping in Endometrial Cancer

Sentinel lymph node biopsy is proposed as an alternative to lymphadenectomy in ECa. In this setting, a dye with/without a radiotracer is injected into the cervical (most common) or uterine stroma, subsequently, it will be accumulated in the corresponding lymph nodes to aid the recognition of SLNs using the robotic or laparoscopic camera [60]. In ECa, bilateral pelvic mapping is an integral part of the procedure of SLN to decrease the rate of pelvic lymphadenectomies without omitting the mapping of one side of the pelvis [61]. Initially, SLN in ECa was performed using a combination of 99Tm and a visible dye (such as Isosulfan blue dye) [62]; however, this practice was replaced by the use of ICG as it is superior to blue dye in detecting SLNs (64% vs 83%, p < 0.0001) [63].

The Fluorescence Imaging for Robotic Endometrial Sentinel lymph node biopsy (FIRES) trial is a prospective, multicenter, cohort study that aims to assess the value of ICG-SLN biopsy as an alternative to lymphadenectomy in 385 patients undergoing robotic surgery for stage I ECa. The authors reported that ICG-SLN biopsy can safely replace lymphadenectomy with a sensitivity of 97.2% and a NPV of 99.6%. Cusimano et al. [64], supported the same finding in 156 high-grade ECa patients undergoing minimally invasive surgery (laparoscopic or robotic) showing a detection of 97.4% per patient, 87.5% per hemipelvis, and 77.6% bilaterally. In this prospective cohort of patients, ICG-SLN biopsy showed a sensitivity of 96.3%, FNR of 3.7%, and a NPV of 99.2% [64]. Similar to SLNs in cervical cancer, the combination of ICG with 99Tm was not superior to ICG alone in the detection of SLN [61]. A recent systematic review and meta-analysis of 14 studies accounting for 2117 patients were in line with the pervious findings showing an overall and bilateral ICG-SLN detection rates of 95.6% and 76.5%, respectively. Furthermore, the authors showed a pooled NPV of 100% for patients with grade I & II ECa and 99.2% for patients with grade I, II, & III ECa [60]. Several other meta-analyses supported these findings [65, 66, 67]; however, their results should be interpreted with caution as the quality of these studies are doubtful [68].

5. Prostate Cancer
5.1 Introduction

According to the GLOBCAN study 2020, prostate cancer (PCa) is the second most common male malignancy worldwide with an incidence and mortality of 14.1% and 6.8%, respectively [12]. Nerve sparing radical prostatectomy (RP) is considered the current standard of care for patients with clinically localized prostate cancer and life expectancy of >10 years [8, 69]. Considering, the relatively significant incidence of lymph node metastasis (5–10%) in patients with PCa [70], the combination of PLND with RP is indicated in patients with risk of nodal metastasis 5% on validated nomograms [69]. Yet, the oncological value of PLND in the setting of RP remains one of the most controversial topics in the urological literature but its diagnostic and prognostic role should not be neglected [71].

The extent of LND is another point of debate, where the literature describes several templates extending from minimal or limited LND (including only the obturator fossa), standard dissection (obturator fossa and external iliac LNs), to extended dissection (extends to the common iliac up to the crossing of the ureter) [70]. Generally, the European Association of Urology (EAU) guidelines recommends the extended template of PLND [69].

Currently, the robotic approach to RP is the most commonly used approach for treating patients with PCa rendering robotic-assisted laparoscopic radical prostatectomy (RALP) the most commonly performed robotic procedure worldwide [10]. This may be attributed to the technical advantages of robotic surgery over laparoscopic and open surgeries [72]. Furthermore, there is some evidence that RALP may provide superior outcomes as regards the oncological and functional domains [73, 74, 75, 76]. In this setting, robotic PLND as a part of RP is common in the urological discipline [70].

5.2 Robotic PLND in Prostate Cancer

Over the last two decades, there was a decrease in the rate and indications of PLND during RP even among patients with intermediate and high risk PCa. Some surgeons related this finding to the wide adoption of the robotic approach to RP as surgeons wanted to avoid longer operative times, which may subsequently increase the risk of complications and the operative costs [7, 77]. Interestingly, Gandaglia et al. [77] used the Surveillance, Epidemiology, and End Results Program (SEER) database to assess the impact of robotic surgery on PLND during RP between October 2008 and December 2009, showing that patients undergoing open RP were more likely to undergo PLND compared to RALP (71.2% vs 48.6%, p < 0.001). This finding was consistent after stratifying the patients according to PCa risk [77]. On the contrary, a more recent study (including patients undergoing RP between 2004–2013) showed significant increase in the rate of PLND from 58.9% to 72.1%. Furthermore, this finding persists when patients were stratified according to the surgical approach (from 57.1% to 67.9%, 67.8% to 73.9%, and 77.6% to 81.3%, for robotic, laparoscopic, and open approaches, respectively). Yet, the rate of PLND during open and laparoscopic approaches was higher compared to robotic approach [78].

LN yield in PCa patients is an important predictor of lymph node positivity and surrogate marker of the quality of LND [79]. Two systematic reviews reported that the lymph node yield during robotic PLND ranges from 3.3 to 24 based on the template of dissection [7, 80]. Results from RCTs showed that that the nodal yield is comparable among robotic and laparoscopic approaches [81], while it was higher for RALP compared to open RP [82]. Noteworthy, these studies were not designed to compare the nodal yield among different approaches [81, 82].

5.3 Sentinel Lymph Node Mapping in Prostate Cancer

SLN biopsy in patients undergoing RALP aims to provide the balance between the potential value of PLND and its associated morbidities through identifying the patients who might benefit from PLND [83]. However, it is still considered an experimental procedure because of the complex lymphatic drainage of the prostate and the heterogeneous results of SLN biopsy in the medical literature [70]. Currently, ICG is the most commonly used dye for the SLN biopsy in PCa patients.

Hence, PCa is a multifocal neoplasm, it is not clearly known which lesion will metastasize or which one is the index lesion [84]. In this setting, the site of injection of the dye might have an impact on the outcomes of SLN biopsy. A recent RCT showed that ultrasound guided, transrectal, intratumoral injection of ICG-Technetium 99 m was associated with significantly higher percentage of positive SLNs compared to intraprostatic injection in the peripheral zone of the prostate [85].

Considering the outcomes of SLN biopsy, a systematic review and meta-analysis of 21 studies accounting for 2509 patients undergoing SLN biopsy through either transrectal or transperineal injection of tracers in the peripheral zone of the prostate or the whole prostate during RP (open, robotic, or laparoscopic), reported a pooled non-diagnostic ratio, sensitivity, specificity, positive predictive value (PPV), and NPV of 4.1%, 95.2%, 100%, 100%, and 98%, respectively [86]. Noteworthy, this meta-analysis included studies using different types of tracers [86]. In this setting, a more recent systematic review and meta-analysis assessed only the performance of ICG-SLN biopsy in patients undergoing RP concluded that the diagnostic performance of this procedure is relatively low (sensitivity = 0.75, and specificity = 0.66) rendering it a suboptimal alternative to PLND [87]. However, the combination of prostate specific membrane antigen positron emission tomography and computed tomography (PSMA PET/CT) and SLN biopsy is capable of improving the detection rate of positive lymph nodes by 26% [88]. Generally, a consensus meeting in Germany considered that extended PLND remains the standard of care for lymph node staging, while SLN biopsy can be considered in conjunction with PLND in intermediate- and high-risk PCa patients [89].

6. Bladder Cancer
6.1 Introduction

Bladder cancer (BCa) is one of the most common urological neoplasms [12]. Approximately, 75% of bladder cancers are confined to the mucosa without invasion of the detrusor muscle. The treatment those patients with non-muscle invasive BCa consists of complete endoscopic resection of the mass followed by intravesical chemo- or immune-therapy [90]. Unfortunately, the remaining 25% are muscle invasive BCa, which is a more aggressive form of the disease that requires a more radical intervention in the form of radical cystectomy (RC) with bilateral PLND [70]. Generally, the extent of LND in patients with BCa is debatable as the lymphatic drainage of the bladder is complex as it mainly includes the obturator, external and internal iliac, and presacral lymph nodes. However, it may also extend to the common iliac, paraaortic, interaortocaval, and paracaval LNs [91]. Unlike PCa, the advantage of PLND in patients with BCa is not limited to its prognostic value but it extends to include also a survival benefit [92]. In this setting, an extended PLND template is recommended as a standard template may underestimate the presence of LN metastasis by 11% [93], and is generally associated with significantly higher all-cause and cancer-specific mortalities [94]. In these settings, PLND is considered an integral part of the treatment of patients with BCa.

Robotic approach to RC started to gain popularity among urologists due to the high complexity of open approach with its associated morbidity and mortality together with the steep learning curve of pure laparoscopic RC [95]. Despite the lack of high-level evidence, robotic assisted laparoscopic radical cystectomy (RARC) continues to expand at the expenses of open and laparoscopic approaches. Noteworthy, results from RCTs comparing RARC to open and laparoscopic approaches showed that RARC is associated with significantly longer operative times, lower estimated blood loss, lower postoperative pain and shorter hospitalization. Yet, there was no significance difference as regards the post-operative complication rates and the oncological outcomes. It should be mentioned that most of the RCTs comparing the robotic approach to other approaches was limited to patients undergoing RARC with extracorporeal urinary diversion, which may limit the benefits of minimally invasive surgery [96]. In this setting, the most recent RCT comparing open radical cystectomy to RARC with intracorporeal urinary diversion showed significantly higher rates of perioperative blood transfusion in patients undergoing open RC (41% vs 22%, p = 0.047) [97].

6.2 Robotic PLND in Bladder Cancer

Theoretically, minimally invasive approaches to RC are associated with better quality of LND in the form of higher Lymph node yield and lower density compared to open approach because minimally invasive approaches allow enbloc resection of lymphatic tissue with a 10× magnified view of the surgical field [98, 99]. A recent analysis of 1425 BCa patients from the Italian Radical Cystectomy Registry showed that robotic and laparoscopic approaches were associated with higher rates of PLND compared to open approach (97.1%, 93.5%, and 85.6%, respectively, p < 0.001). Furthermore, the authors reported that the rate of limited template of PLND was comparable among the three approaches, while RARC was associated with 2-folds higher rates of using extended PLND template compared to the other approaches [100]. Similar to the previously discussed tumors, LNs yield is an important indicator of the quality of LND and it may have an impact on the patients’ survival [101]. In this setting, an analysis of 16,505 muscle invasive BCa patients undergoing RC with PLND reported that the oncological outcomes (in patients not receiving neoadjuvant chemotherapy) were significantly superior in patients who had adequate LND (10 nodes) compared to those with inadequate LND (<10 nodes) [102].

Some authors demonstrated that RARC may be associated with higher LN yield compared to other approaches (16–20 nodes vs 11–14 nodes based on the extent of dissection, respectively) [103, 104]. However, when considering the results from RCTs, the lymph node yield in patients undergoing RARC seems to be comparable to open and laparoscopic approaches [97, 105, 106, 107, 108].

LN density was proposed as an alternative to LN yield in the assessment of the quality of LND as LN yield is related to several factors that may affect its assessment including the method of submission (enbloc or separate packets), the surgeon’s experience and technique, and the pathologists’ experience [70]. Lymph node density refers to the number of positive LNs to the total number of nodes retrieved. A density of >20% is associated with a 10% reduction of survival. However, there is still no consensus on the ideal way of assessment of the quality of PLND [109].

6.3 Sentinel Lymph Node Mapping in Bladder Cancer

The concept of SLN biopsy in patients with BCa is less commonly utilized as it is still experimental [110]. In this setting, Schaafsma et al. [111] injected ICG bound to human serum albumin (an experimental material not available in market) cystoscopically around the bladder tumor after bladder distention demonstrating the feasibility of this technique in identifying of SLNs in BCa patients. In line with this study, Rietbergen et al. [112] demonstrated the feasibility of ICG-99mTc-nanocolloid injected one day before surgery in identifying SLN in 63% of patients. Furthermore, the authors demonstrated that preoperative imaging in the form of lymphoscintigraphy and SPECT/CT was capable of identifying 83% of patients who showed any SN on intra-operative guidance, thus highlighting the value of preoperative imaging in patients undergoing SLN-biopsy [112]. Despite being a promising tool for intraoperative guidance, SLN biopsy in BCa patients requires further assessment and no recommendations can be built based on the currently available evidence [110].

7. Conclusions

PLND is an integral part of gynecological and urological oncology for its role in tumor staging and planning of further treatment plan. Furthermore, it may play an important therapeutic role in bladder cancer. Robotic approach to PLND seems to be an interesting alternative to open and laparoscopic approaches as it may decrease the associated morbidities without compromising the quality of LND (nodal yield). SLN-biopsy can be applied during minimally invasive surgery to improve the quality of LND, while reducing the associated morbidity.

Abbreviations

BCa, Bladder cancer; ECa, Endometrial cancer; EAU, European Association of Urology; FNR, False negative rate; ICG, Indocyanine green; LND, Lymph node dissection; LN, Lymph nodes; MRI, Magnetic resonance imaging; NPV, Negative predictive value; PCa, Prostate cancer; PPV, Positive predictive value; PSMA PET/CT, Prostate specific membrane antigen positron emission tomography and computed tomography; PLND, Pelvic lymph node dissection; RP, Radical prostatectomy; RALP, Robotic-assisted laparoscopic radical prostatectomy; RCTs, Randomized controlled trials; RALRH, Robotic-assisted laparoscopic radical hysterectomy; RC, Radical cystectomy; RARC, Robotic-assisted laparoscopic radical cystectomy; SLN, Sentinel lymph node; SPECT/CT, single-photon emission computerized tomography and computed Tomography; 99Tm, 99Technetium.

Author Contributions

Conceptualization—AEis, MCS, GG, AZ, BR, SM, AHE; Methodology—GH, IE, AEls, AM, MAE; Database Search & Data Extraction—GH, IE, SP, AEls, AZ, ME, MR; Original Drafting—AEis, MCS, SP, MR, MAE, GG; Article Writing—ME, AEis, AM, MR; Review & Supervision—MAE, ME, AHE, SM, BR. All authors contributed to editorial changes in the manuscript. All authors read and approved the final manuscript. All authors have participated sufficiently in the work to take public responsibility for appropriate portions of the content and agreed to be accountable for all aspects of the work in ensuring that questions related to its accuracy or integrity.

Ethics Approval and Consent to Participate

Not applicable.

Acknowledgment

We would like to express our gratitude to all those who helped us during the writing of this manuscript. Thanks to all the peer reviewers for their opinions and suggestions.

Funding

This research received no external funding.

Conflict of Interest

The authors declare no conflict of interest. Giorgia Gaia is serving as one of the Guest editors of this journal. We declare that Giorgia Gaia had no involvement in the peer review of this article and has no access to information regarding its peer review. Full responsibility for the editorial process for this article was delegated to Ugo Indraccolo.

References
[1]
Emons G. Significance of lymph node dissection in gynecological oncology. Oncology Research and Treatment. 2014; 37: 500–504.
[2]
Disibio G, French SW. Metastatic patterns of cancers: results from a large autopsy study. Archives of Pathology & Laboratory Medicine. 2008; 132: 931–939.
[3]
Roque DR, Wysham WZ, Soper JT. The surgical management of cervical cancer: an overview and literature review. Obstetrical & Gynecological Survey. 2014; 69: 426–441.
[4]
Guo W, Cai J, Li M, Wang H, Shen Y. Survival benefits of pelvic lymphadenectomy versus pelvic and para-aortic lymphadenectomy in patients with endometrial cancer: A meta-analysis. Medicine. 2018; 97: e9520.
[5]
Li R, Petros FG, Davis JW. Extended Pelvic Lymph Node Dissection in Bladder Cancer. Journal of Endourology. 2018; 32: S49–S54.
[6]
Onol FF, Bhat S, Moschovas M, Rogers T, Albala D, Patel V. The ongoing dilemma in pelvic lymph node dissection during radical prostatectomy: who should decide and in which patients? Journal of Robotic Surgery. 2020; 14: 549–558.
[7]
Ploussard G, Briganti A, de la Taille A, Haese A, Heidenreich A, Menon M, et al. Pelvic lymph node dissection during robot-assisted radical prostatectomy: efficacy, limitations, and complications-a systematic review of the literature. European Urology. 2014; 65: 7–16.
[8]
Puliatti S, Elsherbiny A, Eissa A, Pirola G, Morini E, Squecco D, et al. Effect of puboprostatic ligament reconstruction on continence recovery after robot-assisted laparoscopic prostatectomy: our initial experience. Minerva Urologica e Nefrologica. 2019; 71: 230–239.
[9]
Hussain A, Malik A, Halim MU, Ali AM. The use of robotics in surgery: a review. International Journal of Clinical Practice. 2014; 68: 1376–1382.
[10]
El Sherbiny A, Eissa A, Ghaith A, Morini E, Marzotta L, Sighinolfi MC, et al. Training in urological robotic surgery. Future perspectives. Archivos Espanoles de Urologia. 2018; 71: 97–107.
[11]
Watanabe T, Hata K. Robotic surgery for rectal cancer with lateral lymph node dissection. The British Journal of Surgery. 2016; 103: 1755–1757.
[12]
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA: A Cancer Journal for Clinicians. 2021; 71: 209–249.
[13]
Brandt B, Levin G, Leitao MM Jr. Radical Hysterectomy for Cervical Cancer: the Right Surgical Approach. Current Treatment Options in Oncology. 2022; 23: 1–14.
[14]
Charo LM, Vaida F, Eskander RN, Binder P, Saenz C, McHale M, et al. Rapid dissemination of practice-changing information: A longitudinal analysis of real-world rates of minimally invasive radical hysterectomy before and after presentation of the LACC trial. Gynecologic Oncology. 2020; 157: 494–499.
[15]
Ramirez PT, Frumovitz M, Pareja R, Lopez A, Vieira M, Ribeiro R, et al. Minimally Invasive versus Abdominal Radical Hysterectomy for Cervical Cancer. The New England Journal of Medicine. 2018; 379: 1895–1904.
[16]
Fernandez-Gonzalez S, Ponce J, Martínez-Maestre MÁ, Barahona M, Gómez-Hidalgo NR, Díaz-Feijoo B, et al. The Impact of Surgical Practice on Oncological Outcomes in Robot-Assisted Radical Hysterectomy for Early-Stage Cervical Cancer, Spanish National Registry. Cancers. 2022; 14: 698.
[17]
Saito T, Matsuura M, Tamate M, Iwasaki M, Mariya T. Radical Vaginal Trachelectomy. Surgery Journal. 2021; 7: S103–S107.
[18]
Salvo G, Ramirez PT, Leitao MM, Cibula D, Wu X, Falconer H, et al. Open vs minimally invasive radical trachelectomy in early-stage cervical cancer: International Radical Trachelectomy Assessment Study. American Journal of Obstetrics and Gynecology. 2022; 226: 97.e1–97.e16.
[19]
Olthof EP, van der Aa MA, Adam JA, Stalpers LJA, Wenzel HHB, van der Velden J, et al. The role of lymph nodes in cervical cancer: incidence and identification of lymph node metastases-a literature review. International Journal of Clinical Oncology. 2021; 26: 1600–1610.
[20]
Lührs O, Ekdahl L, Geppert B, Lönnerfors C, Persson J. Resection of the upper paracervical lymphovascular tissue should be an integral part of a pelvic sentinel lymph node algorithm in early stage cervical cancer. Gynecologic Oncology. 2021; 163: 289–293.
[21]
Uwins C, Patel H, Prakash Bhandoria G, Butler-Manuel S, Tailor A, Ellis P, et al. Laparoscopic and Robotic Surgery for Endometrial and Cervical Cancer. Clinical Oncology. 2021; 33: e372–e382.
[22]
Rizou N, Moris D, Pikoulis E, Dimitrokallis N, Mpaili E, Felekouras E, et al. Minimally Invasive Lymphadenectomy in Uterine Cervical Cancer: A Systematic Review. Anticancer Research. 2017; 37: 335–342.
[23]
Van Gorp T, Kruse AJ, Slangen BF, Kruitwagen RF. Lymph node density as a surrogate marker for positive lymph nodes. British Journal of Cancer. 2011; 104: 221–222; author reply 223.
[24]
Gao J, Dang J, Chu J, Liu X, Wang J, You J, et al. A Comparative Analysis of Robotic Single-Site Surgery and Laparoendoscopic Single-Site Surgery as Therapeutic Options for Stage IB1 Cervical Squamous Carcinoma. Cancer Management and Research. 2021; 13: 3485–3492.
[25]
Tinelli R, Malzoni M, Cosentino F, Perone C, Fusco A, Cicinelli E, et al. Robotics versus laparoscopic radical hysterectomy with lymphadenectomy in patients with early cervical cancer: a multicenter study. Annals of Surgical Oncology. 2011; 18: 2622–2628.
[26]
Nam EJ, Kim SW, Kim S, Kim JH, Jung YW, Paek JH, et al. A case-control study of robotic radical hysterectomy and pelvic lymphadenectomy using 3 robotic arms compared with abdominal radical hysterectomy in cervical cancer. International Journal of Gynecological Cancer. 2010; 20: 1284–1289.
[27]
Schreuder HWR, Zweemer RP, van Baal WM, van de Lande J, Dijkstra JC, Verheijen RHM. From open radical hysterectomy to robot-assisted laparoscopic radical hysterectomy for early stage cervical cancer: aspects of a single institution learning curve. Gynecological Surgery. 2010; 7: 253–258.
[28]
Ding D, Jiang H, Nie J, Liu X, Guo SW. Concurrent Learning Curves of 3-Dimensional and Robotic-Assisted Laparoscopic Radical Hysterectomy for Early-Stage Cervical Cancer Using 2-Dimensional Laparoscopic Radical Hysterectomy as a Benchmark: A Single Surgeon’s Experience. Medical Science Monitor. 2019; 25: 5903–5919.
[29]
Pellegrino A, Damiani GR, Loverro M, Pirovano C, Fachechi G, Corso S, et al. Comparison of Robotic and laparoscopic Radical type-B and C hysterectomy for cervical cancer: Long term-outcomes. Acta Bio-medica: Atenei Parmensis. 2017; 88: 289–296.
[30]
Nie JC, Yan AQ, Liu XS. Robotic-Assisted Radical Hysterectomy Results in Better Surgical Outcomes Compared With the Traditional Laparoscopic Radical Hysterectomy for the Treatment of Cervical Cancer. International Journal of Gynecological Cancer. 2017; 27: 1990–1999.
[31]
Li XL, Du DF, Jiang H. The learning curves of robotic and three-dimensional laparoscopic surgery in cervical cancer. Journal of Cancer. 2016; 7: 2304–2308.
[32]
Corrado G, Cutillo G, Saltari M, Mancini E, Sindico S, Vici P, et al. Surgical and Oncological Outcome of Robotic Surgery Compared With Laparoscopic and Abdominal Surgery in the Management of Locally Advanced Cervical Cancer After Neoadjuvant Chemotherapy. International Journal of Gynecological Cancer. 2016; 26: 539–546.
[33]
Corrado G, Fanfani F, Ghezzi F, Fagotti A, Uccella S, Mancini E, et al. Mini-laparoscopic versus robotic radical hysterectomy plus systematic pelvic lymphadenectomy in early cervical cancer patients. A multi-institutional study. European Journal of Surgical Oncology. 2015; 41: 136–141.
[34]
Yim GW, Kim SW, Nam EJ, Kim S, Kim HJ, Kim YT. Surgical outcomes of robotic radical hysterectomy using three robotic arms versus conventional multiport laparoscopy in patients with cervical cancer. Yonsei Medical Journal. 2014; 55: 1222–1230.
[35]
Vizza E, Corrado G, Mancini E, Vici P, Sergi D, Baiocco E, et al. Laparoscopic versus robotic radical hysterectomy after neoadjuvant chemotherapy in locally advanced cervical cancer: a case control study. European Journal of Surgical Oncology. 2015; 41: 142–147.
[36]
Wallin E, Flöter Rådestad A, Falconer H. Introduction of robot-assisted radical hysterectomy for early stage cervical cancer: impact on complications, costs and oncologic outcome. Acta Obstetricia et Gynecologica Scandinavica. 2017; 96: 536–542.
[37]
Sert MB, Abeler V. Robot-assisted laparoscopic radical hysterectomy: comparison with total laparoscopic hysterectomy and abdominal radical hysterectomy; one surgeon’s experience at the Norwegian Radium Hospital. Gynecologic Oncology. 2011; 121: 600–604.
[38]
Diver E, Hinchcliff E, Gockley A, Melamed A, Contrino L, Feldman S, et al. Minimally Invasive Radical Hysterectomy for Cervical Cancer Is Associated With Reduced Morbidity and Similar Survival Outcomes Compared With Laparotomy. Journal of Minimally Invasive Gynecology. 2017; 24: 402–406.
[39]
Soliman PT, Iglesias D, Munsell MF, Frumovitz M, Westin SN, Nick AM, et al. Successful incorporation of robotic surgery into gynecologic oncology fellowship training. Gynecologic Oncology. 2013; 131: 730–733.
[40]
Gould EA, Winship T, Philbin PH, Kerr HH. Observations on a “sentinel node” in cancer of the parotid. Cancer. 1960; 13: 77–78.
[41]
Lührs O, Ekdahl L, Lönnerfors C, Geppert B, Persson J. Combining Indocyanine Green and Tc99-nanocolloid does not increase the detection rate of sentinel lymph nodes in early stage cervical cancer compared to Indocyanine Green alone. Gynecologic Oncology. 2020; 156: 335–340.
[42]
Beavis AL, Salazar-Marioni S, Sinno AK, Stone RL, Fader AN, Santillan-Gomez A, et al. Sentinel lymph node detection rates using indocyanine green in women with early-stage cervical cancer. Gynecologic Oncology. 2016; 143: 302–306.
[43]
Holman LL, Levenback CF, Frumovitz M. Sentinel lymph node evaluation in women with cervical cancer. Journal of Minimally Invasive Gynecology. 2014; 21: 540–545.
[44]
Lukas R, Helena R, Jiri HM, Martin H, Petr S. Current status of sentinel lymph node mapping in the management of cervical cancer. Expert Review of Anticancer Therapy. 2013; 13: 861–870.
[45]
Salvo G, Ramirez PT, Levenback CF, Munsell MF, Euscher ED, Soliman PT, et al. Sensitivity and negative predictive value for sentinel lymph node biopsy in women with early-stage cervical cancer. Gynecologic Oncology. 2017; 145: 96–101.
[46]
Kim JH, Kim DY, Suh DS, Kim JH, Kim YM, Kim YT, et al. The efficacy of sentinel lymph node mapping with indocyanine green in cervical cancer. World Journal of Surgical Oncology. 2018; 16: 52.
[47]
Crosbie EJ, Kitson SJ, McAlpine JN, Mukhopadhyay A, Powell ME, Singh N. Endometrial cancer. The Lancet. 2022; 399: 1412–1428.
[48]
Kalampokas E, Giannis G, Kalampokas T, Papathanasiou AA, Mitsopoulou D, Tsironi E, et al. Current Approaches to the Management of Patients with Endometrial Cancer. Cancers. 2022; 14: 4500.
[49]
Clark LH, Soper JT. Endometrial Cancer and the Role of Lymphadenectomy. Obstetrical & Gynecological Survey. 2016; 71: 353–360.
[50]
Argenta PA, Mattson J, Rivard CL, Luther E, Schefter A, Vogel RI. Robot-assisted versus laparoscopic minimally invasive surgery for the treatment of stage I endometrial cancer. Gynecologic Oncology. 2022; 165: 347–352.
[51]
Geppert B, Persson J. Robotic infrarenal paraaortic and pelvic nodal staging for endometrial cancer: feasibility and lymphatic complications. Acta Obstetricia et Gynecologica Scandinavica. 2015; 94: 1074–1081.
[52]
Bogani G, Dowdy SC, Cliby WA, Ghezzi F, Rossetti D, Frigerio L, et al. Management of endometrial cancer: issues and controversies. European Journal of Gynaecological Oncology. 2016; 37: 6–12.
[53]
Bernardini MQ, Gien LT, Tipping H, Murphy J, Rosen BP. Surgical outcome of robotic surgery in morbidly obese patient with endometrial cancer compared to laparotomy. International Journal of Gynecological Cancer. 2012; 22: 76–81.
[54]
Eklind S, Lindfors A, Sjöli P, Dahm-Kähler P. A prospective, comparative study on robotic versus open-surgery hysterectomy and pelvic lymphadenectomy for endometrial carcinoma. International Journal of Gynecological Cancer. 2015; 25: 250–256.
[55]
Pulman KJ, Dason ES, Philp L, Bernardini MQ, Ferguson SE, Laframboise S, et al. Comparison of three surgical approaches for staging lymphadenectomy in high-risk endometrial cancer. International Journal of Gynaecology and Obstetrics. 2017; 136: 315–319.
[56]
Corrado G, Mereu L, Bogliolo S, Cela V, Freschi L, Carlin R, et al. Robotic single site staging in endometrial cancer: A multi-institution study. European Journal of Surgical Oncology. 2016; 42: 1506–1511.
[57]
Backes FJ, ElNaggar AC, Farrell MR, Brudie LA, Ahmad S, Salani R, et al. Perioperative Outcomes for Laparotomy Compared to Robotic Surgical Staging of Endometrial Cancer in the Elderly: A Retrospective Cohort. International Journal of Gynecological Cancer. 2016; 26: 1717–1721.
[58]
Göçmen A, Sanlıkan F, Uçar MG. Robotic-assisted infrarenal aortic lymphadenectomy and pelvic lymphadenectomy for endometrial staging using a single docking procedure. Gynecologic Oncology Case Reports. 2012; 2: 44–46.
[59]
Petousis S, Christidis P, Margioula-Siarkou C, Papanikolaou A, Dinas K, Mavromatidis G, et al. Combined pelvic and para-aortic is superior to only pelvic lymphadenectomy in intermediate and high-risk endometrial cancer: a systematic review and meta-analysis. Archives of Gynecology and Obstetrics. 2020; 302: 249–263.
[60]
Burg LC, Verheijen S, Bekkers RLM, IntHout J, Holloway RW, Taskin S, et al. The added value of SLN mapping with indocyanine green in low- and intermediate-risk endometrial cancer management: a systematic review and meta-analysis. Journal of Gynecologic Oncology. 2022; 33: e66.
[61]
Cabrera S, Barahona-Orpinell M, Almansa-González C, Padilla-Iserte P, Bebia V, Martí L, et al. Combined use of ICG and technetium does not improve sentinel lymph node detection in endometrial cancer: Results of the COMBITEC study. Gynecologic Oncology. 2021; 162: 32–37.
[62]
Rossi EC. Current state of sentinel lymph nodes for women with endometrial cancer. International Journal of Gynecological Cancer. 2019; 29: 613–621.
[63]
Backes FJ, Cohen D, Salani R, Cohn DE, O’Malley DM, Fanning E, et al. Prospective clinical trial of robotic sentinel lymph node assessment with isosulfane blue (ISB) and indocyanine green (ICG) in endometrial cancer and the impact of ultrastaging (NCT01818739). Gynecologic Oncology. 2019; 153: 496–499.
[64]
Cusimano MC, Vicus D, Pulman K, Maganti M, Bernardini MQ, Bouchard-Fortier G, et al. Assessment of Sentinel Lymph Node Biopsy vs Lymphadenectomy for Intermediate- and High-Grade Endometrial Cancer Staging. JAMA Surgery. 2021; 156: 157–164.
[65]
Marchocki Z, Cusimano MC, Clarfield L, Kim SR, Fazelzad R, Espin-Garcia O, et al. Sentinel lymph node biopsy in high-grade endometrial cancer: a systematic review and meta-analysis of performance characteristics. American Journal of Obstetrics and Gynecology. 2021; 225: 367.e1–367.e39.
[66]
Wang L, Liu F. Meta-analysis of laparoscopy sentinel lymph node mapping in endometrial cancer. Archives of Gynecology and Obstetrics. 2018; 298: 505–510.
[67]
Lin H, Ding Z, Kota VG, Zhang X, Zhou J. Sentinel lymph node mapping in endometrial cancer: a systematic review and meta-analysis. Oncotarget. 2017; 8: 46601–46610.
[68]
Mariño MAG. Sentinel Lymph Node Biopsy in Endometrial Cancer - A Systematic Review and Quality Assessment of Meta-Analyses. Revista Brasileira de Ginecologia e Obstetricia. 2022; 44: 785–789.
[69]
Mottet N, van den Bergh RCN, Briers E, Van den Broeck T, Cumberbatch MG, De Santis M, et al. EAU-EANM-ESTRO-ESUR-SIOG Guidelines on Prostate Cancer-2020 Update. Part 1: Screening, Diagnosis, and Local Treatment with Curative Intent. European Urology. 2021; 79: 243–262.
[70]
Rocco B, Eissa A, Gaia G, Assumma S, Sarchi L, Bozzini G, et al. Pelvic lymph node dissection in prostate and bladder cancers. Minerva Urology and Nephrology. 2022; 74: 680–694.
[71]
Winter A, Harzmann R, Wendler JJ, Roloff C, Weikert S, Weissbach L. Is the Recommendation of a Pelvic Lymphadenectomy in Conjunction with Radical Prostatectomy in Prostate Cancer Patients Justified? Report from a Multidisciplinary Expert Panel Meeting. Advances in Therapy. 2020; 37: 213–224.
[72]
Ploussard G. Robotic surgery in urology: facts and reality. What are the real advantages of robotic approaches for prostate cancer patients? Current Opinion in Urology. 2018; 28: 153–158.
[73]
Eissa A, Zoeir A, Sighinolfi MC, Puliatti S, Bevilacqua L, Del Prete C, et al. “Real-time” Assessment of Surgical Margins During Radical Prostatectomy: State-of-the-Art. Clinical Genitourinary Cancer. 2020; 18: 95–104.
[74]
Tang K, Jiang K, Chen H, Chen Z, Xu H, Ye Z. Robotic vs. Retropubic radical prostatectomy in prostate cancer: A systematic review and an meta-analysis update. Oncotarget. 2017; 8: 32237–32257.
[75]
Seo HJ, Lee NR, Son SK, Kim DK, Rha KH, Lee SH. Comparison of Robot-Assisted Radical Prostatectomy and Open Radical Prostatectomy Outcomes: A Systematic Review and Meta-Analysis. Yonsei Medical Journal. 2016; 57: 1165–1177.
[76]
Leitao MM, Jr, Kreaden US, Laudone V, Park BJ, Pappou EP, Davis JW, et al. The RECOURSE Study: Long-term Oncologic Outcomes Associated With Robotically Assisted Minimally Invasive Procedures for Endometrial, Cervical, Colorectal, Lung, or Prostate Cancer: A Systematic Review and Meta-analysis. Annals of Surgery. 2023; 277: 387–396.
[77]
Gandaglia G, Trinh QD, Hu JC, Schiffmann J, Becker A, Roghmann F, et al. The impact of robot-assisted radical prostatectomy on the use and extent of pelvic lymph node dissection in the “post-dissemination” period. European Journal of Surgical Oncology. 2014; 40: 1080–1086.
[78]
Nocera L, Sood A, Dalela D, Gild P, Rogers CG, Peabody JO, et al. Rate and Extent of Pelvic Lymph Node Dissection in the US Prostate Cancer Patients Treated With Radical Prostatectomy. Clinical Genitourinary Cancer. 2018; 16: e451–e467.
[79]
Mandel P, Kriegmair MC, Bogdan K, Boehm K, Budäus L, Graefen M, et al. Association between Lymph Node Counts and Oncological Outcomes in Lymph Node Positive Prostate Cancer. European Urology Focus. 2017; 3: 248–255.
[80]
Novara G, Ficarra V, Mocellin S, Ahlering TE, Carroll PR, Graefen M, et al. Systematic review and meta-analysis of studies reporting oncologic outcome after robot-assisted radical prostatectomy. European Urology. 2012; 62: 382–404.
[81]
Porpiglia F, Fiori C, Bertolo R, Manfredi M, Mele F, Checcucci E, et al. Five-year Outcomes for a Prospective Randomised Controlled Trial Comparing Laparoscopic and Robot-assisted Radical Prostatectomy. European Urology Focus. 2018; 4: 80–86.
[82]
Yaxley JW, Coughlin GD, Chambers SK, Occhipinti S, Samaratunga H, Zajdlewicz L, et al. Robot-assisted laparoscopic prostatectomy versus open radical retropubic prostatectomy: early outcomes from a randomised controlled phase 3 study. The Lancet. 2016; 388: 1057–1066.
[83]
Narayanan R, Wilson TG. Sentinel node evaluation in prostate cancer. Clinical & Experimental Metastasis. 2018; 35: 471–485.
[84]
Mehralivand S, van der Poel H, Winter A, Choyke PL, Pinto PA, Turkbey B. Sentinel lymph node imaging in urologic oncology. Translational Andrology and Urology. 2018; 7: 887–902.
[85]
Wit EMK, van Beurden F, Kleinjan GH, Grivas N, de Korne CM, Buckle T, et al. The impact of drainage pathways on the detection of nodal metastases in prostate cancer: a phase II randomized comparison of intratumoral vs intraprostatic tracer injection for sentinel node detection. European Journal of Nuclear Medicine and Molecular Imaging. 2022; 49: 1743–1753.
[86]
Wit EMK, Acar C, Grivas N, Yuan C, Horenblas S, Liedberg F, et al. Sentinel Node Procedure in Prostate Cancer: A Systematic Review to Assess Diagnostic Accuracy. European Urology. 2017; 71: 596–605.
[87]
Urabe F, Kimura S, Yasue K, Yanagisawa T, Tsuzuki S, Kimura T, et al. Performance of Indocyanine Green Fluorescence for Detecting Lymph Node Metastasis in Prostate Cancer: A Systematic Review and Meta-analysis. Clinical Genitourinary Cancer. 2021; 19: 466.e1–466.e9.
[88]
Hinsenveld FJ, Wit EMK, van Leeuwen PJ, Brouwer OR, Donswijk ML, Tillier CN, et al. Prostate-Specific Membrane Antigen PET/CT Combined with Sentinel Node Biopsy for Primary Lymph Node Staging in Prostate Cancer. Journal of Nuclear Medicine. 2020; 61: 540–545.
[89]
van der Poel HG, Wit EM, Acar C, van den Berg NS, van Leeuwen FWB, Valdes Olmos RA, et al. Sentinel node biopsy for prostate cancer: report from a consensus panel meeting. BJU International. 2017; 120: 204–211.
[90]
Eissa A, Zoeir A, Ciarlariello S, Sarchi L, Sighinolfi MC, Ghaith A, et al. En-bloc resection of bladder tumors for pathological staging: the value of lateral margins analysis. Minerva Urologica e Nefrologica. 2020; 72: 763–769.
[91]
Cattaneo F, Motterle G, Zattoni F, Morlacco A, Dal Moro F. The Role of Lymph Node Dissection in the Treatment of Bladder Cancer. Frontiers in Surgery. 2018; 5: 62.
[92]
Grabbert M, Grimm T, Buchner A, Kretschmer A, Apfelbeck M, Schulz G, et al. Risks and benefits of pelvic lymphadenectomy in octogenarians undergoing radical cystectomy due to urothelial carcinoma of the bladder. International Urology and Nephrology. 2017; 49: 2137–2142.
[93]
Hugen CM, Daneshmand S. Lymph node dissection in bladder cancer: Where do we stand? World Journal of Urology. 2017; 35: 527–533.
[94]
Hwang EC, Sathianathen NJ, Imamura M, Kuntz GM, Risk MC, Dahm P. Extended versus standard lymph node dissection for urothelial carcinoma of the bladder in patients undergoing radical cystectomy. The Cochrane Database of Systematic Reviews. 2019; 5: CD013336.
[95]
Sighinolfi MC, Micali S, Eissa A, Picozzi SCM, Puliatti S, Rocco B. Robotic assisted radical cystectomy: insights on long term oncological outcomes from the International Robotic Cystectomy Consortium. Translational Andrology and Urology. 2019; 8: S521–S523.
[96]
Gul ZG, Katims AB, Winoker JS, Wiklund P, Waingankar N, Mehrazin R. Robotic assisted radical cystectomy versus open radical cystectomy: a review of what we do and don’t know. Translational Andrology and Urology. 2021; 10: 2209–2215.
[97]
Mastroianni R, Ferriero M, Tuderti G, Anceschi U, Bove AM, Brassetti A, et al. Open Radical Cystectomy versus Robot-Assisted Radical Cystectomy with Intracorporeal Urinary Diversion: Early Outcomes of a Single-Center Randomized Controlled Trial. The Journal of Urology. 2022; 207: 982–992.
[98]
Chlosta P, Drewa T, Siekiera J, Jaskulski J, Petrus A, Kamecki K, et al. Lymph node dissection during laparoscopic (LRC) and open (ORC) radical cystectomy due to muscle invasive bladder urothelial cancer (pT2-3, TCC). Videosurgery and other Miniinvasive Techniques. 2011; 6: 127–131.
[99]
Tyritzis SI, Wiklund NP. Is the open cystectomy era over? An update on the available evidence. International Journal of Urology. 2018; 25: 187–195.
[100]
Porreca A, Di Gianfrancesco L, Artibani W, Busetto GM, Carrieri G, Antonelli A, et al. Robotic-assisted, laparoscopic, and open radical cystectomy: surgical data of 1400 patients from The Italian Radical Cystectomy Registry on intraoperative outcomes. Central European Journal of Urology. 2022; 75: 135–144.
[101]
Khanna A, Miest T, Sharma V, Campbell R, Hensley P, Thapa P, et al. Role of Lymphadenectomy during Radical Cystectomy for Nonmuscle-Invasive Bladder Cancer: Results from a Multi-Institutional Experience. The Journal of Urology. 2022; 207: 551–558.
[102]
von Landenberg N, Speed JM, Cole AP, Seisen T, Lipsitz SR, Gild P, et al. Impact of adequate pelvic lymph node dissection on overall survival after radical cystectomy: A stratified analysis by clinical stage and receipt of neoadjuvant chemotherapy. Urologic Oncology. 2018; 36: 78.e13–78.e19.
[103]
Arora A, Pugliesi F, Zugail AS, Moschini M, Pazeto C, Macek P, et al. Higher nodal yield with robot-assisted pelvic lymph node dissection for bladder cancer compared to laparoscopic dissection: implications for more accurate staging. Arab Journal of Urology. 2021; 19: 92–97.
[104]
Mortezavi A, Crippa A, Kotopouli MI, Akre O, Wiklund P, Hosseini A. Association of Open vs Robot-Assisted Radical Cystectomy With Mortality and Perioperative Outcomes Among Patients With Bladder Cancer in Sweden. JAMA Network Open. 2022; 5: e228959.
[105]
Ghazi A, Zimmermann R, Al-Bodour A, Shefler A, Janetschek G. Optimizing the approach for lymph node dissection during laparoscopic radical cystectomy. European Urology. 2010; 57: 71–78.
[106]
Khan MS, Gan C, Ahmed K, Ismail AF, Watkins J, Summers JA, et al. A Single-centre Early Phase Randomised Controlled Three-arm Trial of Open, Robotic, and Laparoscopic Radical Cystectomy (CORAL). European Urology. 2016; 69: 613–621.
[107]
Bochner BH, Dalbagni G, Sjoberg DD, Silberstein J, Keren Paz GE, Donat SM, et al. Comparing Open Radical Cystectomy and Robot-assisted Laparoscopic Radical Cystectomy: A Randomized Clinical Trial. European Urology. 2015; 67: 1042–1050.
[108]
Parekh DJ, Reis IM, Castle EP, Gonzalgo ML, Woods ME, Svatek RS, et al. Robot-assisted radical cystectomy versus open radical cystectomy in patients with bladder cancer (RAZOR): an open-label, randomised, phase 3, non-inferiority trial. The Lancet. 2018; 391: 2525–2536.
[109]
Jena R, Shrivastava N, Sharma AP, Choudhary GR, Srivastava A. The Adequacy of Pelvic Lymphadenectomy During Radical Cystectomy for Carcinoma Urinary Bladder: A Narrative Review of Literature. Frontiers in Surgery. 2021; 8: 687636.
[110]
Liss MA, Noguchi J, Lee HJ, Vera DR, Kader AK. Sentinel lymph node biopsy in bladder cancer: Systematic review and technology update. Indian Journal of Urology. 2015; 31: 170–175.
[111]
Schaafsma BE, Verbeek FPR, Elzevier HW, Tummers QRJG, van der Vorst JR, Frangioni JV, et al. Optimization of sentinel lymph node mapping in bladder cancer using near-infrared fluorescence imaging. Journal of Surgical Oncology. 2014; 110: 845–850.
[112]
Rietbergen DDD, van Gennep EJ, KleinJan GH, Donswijk M, Valdés Olmos RA, van Rhijn BW, et al. Evaluation of the Hybrid Tracer Indocyanine Green- 99m Tc-Nanocolloid for Sentinel Node Biopsy in Bladder Cancer-A Prospective Pilot Study. Clinical Nuclear Medicine. 2022; 47: 774–780.

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