Current status of robot-assisted total pelvic exenteration focusing on the field of urology: a clinical practice review
Introduction
Pelvic exenteration (PE) is performed to treat several types of locally advanced or recurrent pelvic cancers or multiple genitourinary and colorectal cancers (1). It was first reported in 1948 for the treatment of advanced recurrent gynecological malignancies and has since been applied to other advanced cancers (2,3). In primary rectal cancer, one of the major malignancies performed PE, approximately 30% of patients were diagnosed with rectal cancer in locally advanced state, and it was estimated that about 6–10% of patients received PE in order to achieve R0 resection (4). PE is divided into three types depending on the tumor location, extent, and involvement of the pelvic compartments (5). Total PE (TPE) refers to the resection of the urinary tract, rectum, and internal reproductive organs. Posterior PE was defined as resection of the rectum and female reproductive organs without resection of the bladder or ureter. Anterior PE was described as resection of the lower urinary tract and female reproductive organs without resection of the rectum. TPE involves multivisceral resection, including the rectum, sigmoid colon, bladder, prostate, uterus, vagina, or ovaries, and urologists normally perform radical cystectomy or radical prostatectomy and urinary diversion in collaboration with colorectal surgeons and gynecologists.
There have long been concerns about the high complication and mortality rates of open PE because of the technical difficulties in handling several organs in the narrow pelvic space, even though open PE has been shown to prolong survival (1). A systematic review of 23 studies on open PE showed that the perioperative mortality rate (within 30 days) was 0–25% (median, 2.2%), with a complication rate of 37–100% (median, 57%) (6). Minimally invasive techniques for pelvic surgery have several advantages in manipulating organs and vessels in the narrow and deep pelvis, with clear visualization; laparoscopic PE was first reported in 2003 for the treatment of locally advanced cervical cancer (7). Several studies have reported the safety and efficacy of laparoscopic PE, with low mortality and morbidity rates and high R0 resection rates compared to open PE (8-11). In contrast, laparoscopic manipulation to dissect pelvic vessels and multivisceral resections requires high skill. A robot-assisted approach is expected to overcome the problems of the laparoscopic approach with superior three-dimensional high-definition vision and a more ergonomically stable platform (12). The first report on robot-assisted PE for the treatment of locally advanced rectal cancer was published in 2014. Studies demonstrating the safety and usefulness of robot-assisted TPE for the treatment of several pelvic malignancies, including urological tumors, have been gradually increasing (12,13).
This review article provides the current status of robot-assisted TPE and surgical techniques for TPE, focusing on the association with urological malignancies and the manipulation of urological organs.
Current status of robot-assisted TPE
Patient selection
The most common indication for TPE is locally advanced or recurrent colorectal cancer (4,14). Locally advanced or recurrent cervical cancer was dominant for indication for TPE in non-rectal pelvic malignancy, although all gynecological neoplasms (cervical, endometrial, vulvar, or ovarian carcinoma) and lower urinary tract neoplasms (bladder or prostate cancer) are also candidates for TPE as reported in previous literatures (15,16). Moreover, TPE is indicated in patients with both urological and colorectal cancer occurring at the same time (8,17-19). Indication for TPE depends on various factors, including previous treatments and presence of unresectable metastasis and invasion of the pelvic wall, sciatic nerve, or sacral nerve plexus. Additionally, nutritional status or general health conditions tolerable to extended surgery and acceptance of reduced quality of life because of permanent stoma management or complications, including bladder bowel dysfunction, are crucial in identifying the indications for TPE.
The extent of the resected organs was determined based on the extent of the tumor lesion. In cases of preservation of sphincter function with colorectal or coloanal anastomosis, supralevator exenteration was performed, and the levator ani and anus were preserved. In cases with tumor invasion to the prostate but not to the bladder neck or trigone, bladder-sparing prostatectomy and vesicourethral anastomosis can be performed.
Current status of robot-assisted TPE for patients involving urological malignancies
Previous reports on TPE for locally advanced or recurrent urological malignancies are fewer than on those for locally advanced or recurrent colorectal or gynecological malignancies, and information about the surgical outcomes of TPE for urological malignancies is limited (14,16,20). Table 1 shows a summary of previous reports of robot-assisted TPE involving urological malignancies (17-19,21-24). Many cases receiving robot-assisted TPE for urological malignancies had synchronous rectal and prostate cancer, and cases with locally advanced or recurrent bladder or prostate cancer are few (21-24). It may be important to note that the concept of R0 resection or en bloc extended resection including urinary diversion and decision of the extent of resection can be different between Robot-assisted TPE for synchronous localized rectal and prostate cancer and those for locally advanced urological malignancies or colorectal or gynecological malignancies.
Table 1
Authors, year | Cases | Primary urological tumor | Simultaneous tumor | Type of surgery | Mean operating time [range] | Mean blood loss [range] | Intraoperative complication | Postoperative complications (Clavien-Dindo classification) | Perioperative mortality | Margin of resection | Recurrence |
---|---|---|---|---|---|---|---|---|---|---|---|
Castillo et al., 2015, (21) | 1 | Locally recurrent prostate cancer | None | APR + radical cystectomy | 249 | 600 | None | None | None | Negative | Biochemical recurrence |
Winters et al., 2015, (22) | 2 (with another case of primary rectal cancer) | Locally recurrent prostate cancer (n=1), locally advanced bladder cancer (n=1) | None | APR + RCP (n=1), APR + RP (n=1) | 597 [530–660] | 550 [350–800] | None | Pelvic abscess and pyelonephritis (II, n=1) | None | Negative (n=2) | Negative (n=2) |
Kamiyama et al., 2016, (17)† | 1 | Prostate cancer | Rectal cancer | APR + RP (n=1) | 545 | 170 | None | None | None | Negative | N/A |
Peng et al., 2020, (23) | 1 (with 4 other cases of primary rectal cancer) | Locally advanced prostate cancer | None | APR + RCP | N/A | N/A | N/A | N/A | None | Negative | N/A |
Maeda et al., 2022, (19) | 1 (with 4 other cases of primary rectal cancer) | Prostate cancer | Rectal cancer | ISR + RP | N/A | N/A | N/A | N/A | None | Negative | N/A |
Williams et al., 2021, (24) | 5 (with other 2 cases with primary rectal cancer) | Prostate cancer (n=5) (including 2 cases with cT4 cancer) | Primary rectal cancer (n=2), recurrent rectal cancer (n=1), none (n=2) | APR + RCP (n=2), ultra-low anterior resection + RP (n=2), APR + RP (n=1) | 485 [200–670] | 563 [150–1,000] | None | Vesicourethral anastomotic leak and sepsis (IIIa, n=1), ileus and perineal wound infection (II, n=1), urinary tract infection (I, n=1), ileus (I, n=1) | None | Negative (n=5) | Negative (n=3), internal iliac node and thoracic vertebrae (n=1), pelvic, ling, femoral neck (n=1) |
Fukata et al., 2022, (18) | 5 | Prostate cancer (n=5) | Rectal cancer (n=5) | APR + RP (n=2), ISR + RP (n=2), high anterior resection + RP (n=1) | 505 [431–764] | 139 [20–345] | N/A | Colorectal anastomotic leakage (IIIb, n=1), vesicourethral anastomotic leakage (IIIa, n=2) | None | Negative (n=5) | Negative (n=4), bone metastasis of prostate cancer (n=1) |
†, abdominoperineal resection performed laparoscopically. TPE, total pelvic exenteration; APR, abdominoperineal resection; RCP, radical cystoprostatectomy; RP, radical prostatectomy; N/A, not available; ISR, intersphincteric resection.
The long-term oncological outcomes of robot-assisted TPE for locally advanced bladder or prostate cancer remain unclear; however, the reduced risk of perioperative complications from minimally invasive surgery (MIS) and improvement of perioperative adjuvant chemotherapies for urological cancers these days may expand the indications for extended surgery for urological malignancies in the near future.
Surgical technique of robot-assisted TPE focusing on the manipulation of urological organs
The patients were placed in the lithotomy position, and the robot was docked in the Trendelenburg position after four robot ports and two assistant ports were placed. Representative port placements for robot-assisted TPE using the Da Vinci Xi surgical system have been described in the literature (18,19). The same robot ports can be used in rectal and urologic surgery using the Da Vinci Xi surgical system; however, robot or assistant ports can be replaced or added for colorectal surgeons and urologists to operate with the port placement to which they are usually accustomed. Further, combining laparoscopic and robotic surgery was allowed, depending on the type of MIS in which the colorectal surgeons or urologists specialized in each institute (17).
Generally, rectal resection is performed first, followed by radical cystectomy or prostatectomy (Figure 1). Initially, after dividing the inferior mesenteric artery and vein, colorectal surgeons mobilize the rectum by dissecting its dorsal side. After dividing the sigmoid colon, radical prostatectomy or cystectomy was performed. To obtain en bloc specimens, prostatectomy in robot-assisted TPE differed from ordinal robot-assisted radical prostatectomy (RARP) in not dissecting the Denonvilliers’ fascia or ligating the lateral pedicles (Figure 1A). It should be noted that the dorsal tissue moved more easily when dissecting the bladder neck compared to standard RARP because the rectum was already dissected (Figure 1B). During cystectomy in robot-assisted TPE, retrovesical dissection, developing the rectovesical space, and lateral dissection were not performed to resect the bladder with rectal specimen (Figure 1C).
After urethral resection, the rectum was dissected, and en bloc specimen was obtained (Figure 2). Finally, urinary diversion or vesicourethral anastomosis and sigmoid-end colostomy or coloanal anastomosis were performed.
In cases of large rectal tumors in narrow pelvic spaces, dissection of the dorsal side of the rectum is sometimes difficult, and it would be better to perform radical cystectomy procedure earlier in order to increase the range of motion of the bladder and rectum (Figure 1D).
Complications and oncological outcomes of robot-assisted TPE for urological malignancies
In the field of urological surgery, several robotic surgeries, including radical prostatectomy, radical cystectomy, and partial nephrectomy, have revealed the superiority of perioperative outcomes and postoperative complications over open surgeries (25,26). In addition, several studies have reported that the oncological outcomes of RARP are equivalent or superior to those of open or laparoscopic radical prostatectomy, with superior perioperative safety, continence, and erectile dysfunction recovery (27-31). The oncological outcomes of robot-assisted radical cystectomy for invasive bladder cancer are also equivalent to those of open or laparoscopic radical cystectomies (32-34). In contrast, the safeties and treatment efficacy of robot-assisted TPE for urological malignancies with large cohort have not yet been reported in the literature, and information about the perioperative or oncological outcomes of robot-assisted TPE compared with open or laparoscopic TPE is scarce.
Limited information for previous reports suggested that perioperative complications of robot-assisted TPE for urological malignancies have been tolerable and oncological outcomes have also been well preserved (Table 1) (17-19,21-24). A recent case series has summarized fourteen cases of robot-assisted TPE for locally advanced rectal and/or prostate cancers, including three literature reviews, and compared the perioperative and oncological outcomes to those in the literature of a large cohort or meta-analysis data of open TPE (21,22,24,35-37). The study reported higher rates of Clavien-Dindo grade III–IV complications, return to the operating room and intensive care unit (ICU) in open TPE than in robot-assisted TPE, and the tendency of less blood loss and prolonged median operating time in robot-assisted TPE (not statistically analyzed). Therefore, the perioperative complications about urinary tract and the oncological outcomes of urological cancer in robot-assisted TPE for synchronous rectal and urological malignancies or locally advanced urological malignancies are expected to be better or at least equivalent than in open TPE. Further studies with large cohort studies will be needed.
Complications and oncological outcomes of robot-assisted TPE for colorectal and gynecological malignancies (Table 2)
Table 2
Authors, year | Design | Sample size | Primary malignancies | Median operating time (min) | Median blood loss (mL) | 30-day morbidity (%) | Median ICU stay (days) | Mean length of stay (days) | R0 resection (%) | Recurrence (%) |
---|---|---|---|---|---|---|---|---|---|---|
Kumar et al., 2020, (38) | MIS vs. open | 95 (23 vs. 72) | Primary colorectal cancer | 640 vs. 432 (P<0.01) | 900 vs. 1,550 (P<0.01) | 60 vs. 49 (P=0.306) | N.E. | 11 vs. 12 (P=0.63) | 87 vs. 89 (P=0.67) | N.E. |
Kazi et al., 2021, (39) | MIS vs. open | 158 (61 vs. 97) | Locally advanced rectal cancer | 640 vs. 450 (P<0.0001) | 900 vs. 1,600 (P<0.0001) | 39 vs. 46 (P=0.15) | N.E. | 11 vs. 12 (P=0.62) | 89 vs. 92 (P=0.49) | 51.9 vs. 47.8 (3 years recurrence-free survival; P=0.922) |
PelvEx Collaborative, 2018, (40) | MIS vs. open, meta-analysis | 170 (37 vs. 133) | Mixed | Prolonged 83 min in MIS (median) | 550 vs. 2,300 (P<0.001) | 56.7 vs. 88.5 (P=0.17) | N.E. | 22 vs. 28 (P=0.04) | 21.7 vs. 23.0 (P=0.96) | N.E. |
Winters et al., 2015, (22) | Robotic vs. open | 12 (3 vs. 9) | Robotic: recurrent prostate 1, locally advanced bladder 1, locally advanced rectal 1. Open: mixed | 600 vs. 690 (P=0.18) | 575 vs. 2,300 (P=0.01) | 33.3 vs. 44 (P=0.74) | 1 vs. 3 (P=0.01) | 7 vs. 13 (P=0.01) | N.E. | N.E. |
Bizzarri et al., 2019, (41) | Robotic vs. laparoscopic | 23 (11 vs. 12) | Cervical 10, endometrial 9, vaginal 3, urothelial 1 | 500 vs. 660 (P=0.04) | 235 vs. 250 (P=0.298) | 0 vs. 16.7 (P=0.47) | N.E. | 9 vs. 11.5 (P=0.10) | 63.6 vs. 83.3 (P=0.37) | N.E. |
TPE, total pelvic exenteration; ICU, intensive care unit; MIS, minimally invasive surgery (laparoscopic or robot-assisted surgery); N.E., not evaluated.
The PelvEx Collaborative summarized a meta-analysis comparing minimally invasive (robotic or laparoscopic) and open PE, concluding that MIS reduced intraoperative blood loss (550 vs. 2,300 mL, P<0.001), prolonged the median operation time by 83 minutes (P<0.001), and shortened hospital stay (22 vs. 28 days, P=0.04) compared to open PE. The overall morbidity rate in the MIS group showed reduced tendency (56.7% vs. 88.5%) but not statistically significant [relative risk rate, 1.17 (95% confidence interval, 0.93–1.48, P=0.172)] (40). Moreover, another retrospective study comparing perioperative outcomes between MIS and open PE for primary colorectal cancer has shown longer operative time (630 vs. 432 minutes, P<0.01) and less blood loss (900 vs. 1,550 mL, P<0.01) in MIS; however, the overall morbidity was not significantly reduced (60% vs. 49%, P=0.306) in the MIS group (38).
A retrospective single-center study comparing perioperative outcomes between laparoscopic and robot-assisted PE in gynecological malignancies has reported that robot-assisted PE significantly shortened operative time (500 vs. 660 minutes, P=0.04), with equivalent outcomes of blood loss (235 vs. 250 mL, P=0.298), major postoperative complications (0 vs. 16.7%, P=0.47), and hospital stay (9 vs. 11.5 days, P=0.10) (41). A meta-analysis in colorectal surgeries has reported that the perioperative outcomes and postoperative complications in robotic surgeries were similar to those in laparoscopic surgeries, although there was little evidence of the safety of robot-assisted TPE in colorectal cancers compared with laparoscopic TPE (42).
In addition to safety and perioperative outcomes, there is little evidence of the superiority of oncological outcomes of robot-assisted TPE over open or laparoscopic TPE in a large cohort not only in urological malignancies but also in colorectal or gynecological malignancies.
Robot-assisted rectal cancer surgery has shown similar oncological outcomes to those of open surgery or laparoscopic surgery for colorectal cancer (43-45). Therefore, the oncological outcomes of robot-assisted TPE are expected to be equivalent or superior to those of open or laparoscopic TPE for colorectal malignancies; however, limited evidence has been established regarding the difference in oncological outcomes, especially long-term outcomes. A recent retrospective study at a single institute has revealed that recurrence-free survival and 3-year overall survival for locally advanced rectal cancer in minimally invasive (robotic or laparoscopic) TPE were not statistically different from those in open TPE (51.9% vs. 47.8%, P=0.922, 79.4% vs. 60.2%, P=0.251, respectively) (39). In gynecological malignancies, the rate of negative resection margins (R0) in robot-assisted PE was similar to that in laparoscopic PE (63.6% vs. 83.3%, P=0.37) (41). To clarify the superiority of the oncological outcomes of robot-assisted TPE, large multicenter cohort studies with long-term observations are required.
Limitations and further prospective
Currently, most reports on robot-assisted TPE are case reports or studies with small cohorts, and no previous studies have compared the treatment outcomes of robot-assisted TPE to open or laparoscopic TPE in large cohorts or randomized control trials. In addition, information on the long-term oncological outcomes, late complications, and cost-effectiveness of robot-assisted TPE is insufficient. In contrast, several robotic pelvic surgeries in the urological, gynecological, and colorectal fields have demonstrated superior or at least similar safety and oncological outcomes compared to open and laparoscopic surgeries, and robot-assisted pelvic surgeries could replace open or laparoscopic surgeries as the primary technique. Robot-assisted TPE may be a favorable standard MIS for locally invasive or recurrent pelvic malignancies requiring multivisceral resection, and cumulative evidence is warranted.
Conclusions
Robot-assisted TPE is a feasible, safe, and minimally invasive surgical procedure for the treatment of locally invasive or recurrent pelvic malignancies. More high-quality evidence revealing the superiority of robot-assisted TPE in perioperative and long-term oncological outcomes is required to establish robot-assisted TPE as a standard procedure.
Acknowledgments
The authors would like to thank Editage (https://www.editage.com/) for English language editing.
Funding: None.
Footnote
Provenance and Peer Review: This article was commissioned by the Guest Editor (Takuya Koie) for the series “Current Status of Robotic Surgery for Genitourinary Diseases in Japan” published in Translational Cancer Research. The article has undergone external peer review.
Peer Review File: Available at https://tcr.amegroups.com/article/view/10.21037/tcr-23-1039/prf
Conflicts of Interest: Both authors have completed the ICMJE uniform disclosure form (available at https://tcr.amegroups.com/article/view/10.21037/tcr-23-1039/coif). The series “Current Status of Robotic Surgery for Genitourinary Diseases in Japan” was commissioned by the editorial office without any funding or sponsorship. The authors have no other conflicts of interest to declare.
Ethical Statement: The authors are accountable for all aspects of the work and ensure that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. All clinical procedures described in this study were performed in accordance with the ethical standards of the institutional research committee of the Jichi Medical University (No. A19-199) and with the Helsinki Declaration (as revised in 2013). Written informed consent was obtained from the patient for the publication of this article and accompanying images.
Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.
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