Edited by: Patrice Mathevet, Centre Hospitalier Universitaire Vaudois (CHUV), Switzerland
Reviewed by: Diego Raimondo, University of Bologna, Italy; Giulia Armano, University Hospital of Parma, Italy
This article was submitted to Obstetrics and Gynecology, a section of the journal Frontiers in Surgery
†These authors share first authorship
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Pelvic exenteration represents the last resort procedure for patients with advanced primary or recurrent gynecological malignancy. Pelvic exenteration can be divided into different subgroup based on anatomical extension of the procedures. The growing application of the minimally invasive surgical approach unlocked new perspectives for gynecologic oncology surgery. Minimally invasive surgery may offer significant advantages in terms of perioperative outcomes. Since 2009, several Robotic Assisted Laparoscopic Pelvic Exenteration experiences have been described in literature. The advent of robotic surgery resulted in a new spur to the worldwide spread of minimally invasive pelvic exenteration. We present a review of the literature on robotic-assisted pelvic exenteration. The search was conducted using electronic databases from inception of each database through June 2021. 13 articles including 53 patients were included in this review. Anterior exenteration was pursued in 42 patients (79.2%), 2 patients underwent posterior exenteration (3.8%), while 9 patients (17%) were subjected to total exenteration. The most common urinary reconstruction was non-continent urinary diversion (90.2%). Among the 11 women who underwent to total or posterior exenteration, 8 (72.7%) received a terminal colostomy. Conversion to laparotomy was required in two cases due to intraoperative vascular injury. Complications' report was available for 51 patients. Fifteen Dindo Grade 2 complications occurred in 11 patients (21.6%), and 14 grade 3 complications were registered in 13 patients (25.5%). Only grade 4 complications were reported (2%). In 88% of women, the resection margins were negative. Pelvic exenteration represents a salvage procedure in patients with recurrent or persistent gynecological cancers often after radiotherapy. A careful patient selection remains the milestone of such a mutilating surgery. The introduction of the minimally invasive approach has led to advantages in terms of perioperative outcomes compared to classic open surgery. This review shows the feasibility of robotic pelvic exenteration. An important step forward should be to investigate the potential equivalence between robotic approaches and the laparotomic one, in terms of long-term oncological outcomes.
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Pelvic exenteration represents the last resort procedure for patients with advanced primary or recurrent gynecological malignancy, particularly in those with irradiated pelvis and thus unsuitable for further radiotherapy (
Anterior pelvic exenteration includes partial or total excision of the vagina, removal of the genital organs and bladder and eventually partial or total excision of the urethra and is performed in patients with malignancies secondarily involving the bladder. Posterior pelvic exenteration includes partial or total excision of the vagina, removal of the genital organs and sigma rectum and is performed in patients with malignancies involving the rectum. Total pelvic exenteration comprises partial or total excision of the vagina, removal of the rectum, genital organs and bladder and eventually partial or total excision of the urethra. Therefore, three radical monovisceral surgical operations (resection of the rectum, hysterocolpectomy, and cystectomy) are combined in pelvic exenteration. Often, the recurrent disease infiltrates beyond the adjacent pelvic viscera involving different anatomical structures out of the “pelvic box”; such as bones, muscles and neurovascular components of pelvic lateral wall. Therefore, pelvic exenterative surgery must be tailored on tumor tridimensional topography. In view of this, a correct classification should consider not only anterior, posterior, or total extension but also resection of lateral pelvic side wall and levator ani muscle (
The growing application of the minimally invasive surgical approach, particularly in urologic and oncological colorectal surgery, unlocked new perspectives for gynecologic oncology surgery. Subsequently, the advent of robotic surgery resulted in a new spur to the worldwide spread of minimally invasive pelvic exenteration. The first case of robot-assisted laparoscopic pelvic exenteration was reported in 2009, when Lim (
Preliminary research was conducted using the PubMed and SCOPUS databases. The PRISMA based flow-diagram in
Study flow chart (
The search strategy applied in both databases included combinations of the keywords (“robot” OR “robotic”) AND “pelvic exenteration” AND “cervical cancer” AND “endometrial cancer” AND “ovarian cancer” AND “vulvar cancer.” The references for the relevant article were also hand-searched. Exclusion criteria included duplicate articles, papers non-pertinent with the current topic, particularly those regarding robotic pelvic exenteration for non-gynecological malignancies, commentary, letters to the editor. Two authors (MA and RG) screened each study independently and matched by title and abstract. Full texts of eligible studies were reviewed by two authors for data extraction. A third independent author (SC) supervised the research.
After the first search, a total of 1,563 titles were extracted from the Pubmed and Scopus database, using the above mentioned keywords. After the first revision, 61 studies were extracted.
After matched revision, 21 articles were selected, of which 13 studies were ultimately eligible for the present review after full text evaluation. The selection diagram is reported in
At the time of the analysis (June 2021), 13 articles have been published on robotic pelvic exenterations, reporting a total of 53 patients.
The main findings of these studies are summarized in
General characteristics of the included studies.
1 | Lim ( |
1 | Cervix | Recurrence after RTCT | Total | Ileal conduit | End colostomy | 0 | 0 | 375 | 375 | 10 | 0 | 0 | NR | NR |
2 | Lambaudie et al. ( |
3 | Cervix | 2 Recurence after surgery + RT, 1 Rec after RT | Anterior | Miami Pouch | NA | 0 | 0 | 480 | 400 | 30 | pt.1: urocutaneous fistula (G3), pt.2: ureteral stenosis (G3) | 0 | 3 R0 | NR |
3 | Davis et al. ( |
2 | Cervix | 1 Recurrence after CTRT, 1 Rec after RT | Anterior | Ileal conduit | NA | 0 | 0 | 540 | 550 | 8 | NR | NR | 2 R0 | NR |
4 | Vasilescu et al. ( |
1 | Endometrium | Recurrence after surgery + RT | Total | Ureterostomy | End colostomy | 0 | 0 | 250 | 365 | 11 | 0 | 0 | NR | NR |
5 | Jauffret et al. ( |
2 | Cervix | Recurrence | Anterior | Miami Pouch | NA | 0 | 0 | 480 | 300 | NR | pt.1: wound dehiscence (G2), urocutaneous fistula (G3), pt.2: CVC sepsis (G2), urosespis (G2), 1 prerenal failure (G2), obstructive renal failure (G3) | 0 | 1 R0 1 R1 | 1. PFS 8 mo 23 mo OS, 2. 5 PFS, 22 OS |
6 | Lawande et al. ( |
1 | Cervix | Primary | Total | Wet colostomy | End Colostomy | 0 | 0 | 250 | 365 | 11 | 0 | 0 | NR | NR |
7 | Puntambekar et al. ( |
10 | Cervix | 6 Primary, 2 Recurrence, 2 Vescico-vaginal fistula | Anterior | Ileal conduit | NA | 0 | 0 | 180 | 110 | 5 | 0 | 0 | 10 R0 | 11 mo median FUP: 1 died 7 mo later for hepatic recurrence, 1 paraortic and hepatic recurrence after 6 mo, 8 NED |
8 | Kostantinidis et al. ( |
1 | Cervix | Recurrence after RTCT | Total | Ileal conduit | End colostomy | 0 | 0 | 641 | 400 | NR | NR | NR | 1 R0 | NR |
9 | Kim et al. ( |
1 | Melanoma | Recurrence after surgery + CT | Anterior | Ileal conduit | NA | 0 | 0 | 270 | NR | NR | 0 | 0 | 1 R0 | NED at 9 mo |
10 | Nguyen Xuan et al. ( |
5 | Cervix | 1 Recurrence after RTCT, 4 Recurrence after surgery + RTCT | 2 Anterior, 1 Total, 2 Posterior | 3 Bricker | 2 colorectal anastomoses 1 end colostomy | 0 | 0 | 402 | NR | 11.5 | pt.1: UTI (G2), wound dehiscence (G2), pt.2: sepsis (G2), anastomosis stenosis (G3), pt.3 UTI (G2), acute obstructive renal failure (G3), pt.4: TPE (G2), pt.5: UTI (G2) | 0 | 4 R0 1 R1 | 3 recurrences at 6, 7 and 7 mo |
11 | Yang et al. ( |
1 | Cervix | Recurrence after surgery + RTCT | Total | Bricker's ileal conduit | Colorectal anastomosis | 0 | 0 | 700 | 300 | 37 | Rectal anastomosi leak (G3) | 0 | 1 R0 | NED at 17 mo |
12 | Bizzarri et al. ( |
11 | 2 endometrium, 8 cervix, 1 urothelial | 8 Recurrence 2 Persistence 1 Primary | 8 Anterior 3 Total | Ileal conduit | End colostomy | 2 vascular lesion | 2 | 500 | 235 | 9 | 3 late G3 complications (NR complications < G3) | 0 | 7 R0 4 R1 | Not available for robotic surgery only |
13 | Jain et al. ( |
14 | Cervix | 10 Recurrence, |
Anterior | Ileal conduit | NA | 0 | 305 | 135 | 6.5 | pt.1: prolapsed stoma (G1), pt.2: urosepsis (G2), UTI (G2), pt.3: large bowel obstruction (G3); pt.4: subacute intestinal obstruction (G2); pt.5: sigma perforation and peritonitis (G4); pt.6: recto-vaginal fistula (G3); pt.7: uretero-ileal anastamotic leak (G3); pt.8: paralytic ileus (G2); pt.9: bleeding from ileal conduit (G2); pt.10: ureteral stenosis bilateral (G3) | 1 | 14 R0 | 5 pts died (4 for recurrence, 1 for postop complications). 7 NED. Median time to death: 12 months. 12-month DFS: 68.2% 12-month OS: 77.1%. |
Anterior exenteration was pursued in 42 patients (79.2%), 2 patients underwent posterior exenteration (3.8%), while 9 patients (17%) were subjected to total exenteration.
Urinary reconstruction was performed with a continent urinary diversion in 5 patients (9.8%) and with a non-continent urinary diversion in 46 patients (90.2%), including 44 ileal conduit urinary diversions, 1 wet colostomy, and 1 ureterostomy.
Among the 11 women who underwent to total or posterior exenteration, 3 (27.3%) were primary re-anastomized, and 8 (72.7%) received a terminal colostomy.
Intraoperative complications occurred in 2 women (5%) due to vascular injury. Both cases required a conversion to laparotomy.
In two articles postoperative complications were not reported, so complications report was available for 51 patients.
Fifteen Dindo et al. (
A complete surgical cytoreduction with negative resection margins was achieved in 44 patients (88%) while a suboptimal cytoreduction was reached in 6 patients (12%). For three patients 5.7%), there was no pathologic report.
Data regarding follow up were available for 31 patients (from 6 out of 13 studies included).
As reported in these studies, 19 (61.3%) patients were disease free (NED), 8 (25.8%) were dead (7 death of disease, 1 death of postoperative complication), and 4 (12.9%) were alive with disease (AWD) at 12 months of median follow up.
The indication for pelvic evisceration is one of the most hotly debated topics and it must flow from the assessment of multiple factors to avoid inappropriate treatment.
In particular, previous treatments, presence of metastatic disease, infiltration of unresectable structures, general health conditions, nutritional status, and socioeconomic bedrock must be considered in order to address each patients toward the best therapeutic option (
Peritoneal carcinosis, distant metastases and invasion in the sciatic nerve and sacral plexus are considered as contraindications for pelvic exenteration (
The presence of lymph node involvement is still a controversial issue. Although some studies identify it as an adverse prognostic factor (
The first pelvic eviscerations were performed on recurrences of cervical carcinoma; then, the indication was extended to all gynecological neoplasms (endometrial, vulvar, ovarian carcinoma). However, as reported in the published literature (
As reported in this review, robotic pelvic exenteration was performed in most cases in patients who had undergone previous treatments (radiotherapy, surgery, chemotherapy, or combined treatments), only eight (15.1%) were naïve patients.
To achieve free surgical margins PE surgical steps must be tailored to the specific case, evaluating tumor localization, the involvement of pelvic organs and structures and previous treatment, including pelvic radiation. The surgeon adjusts the surgical procedures according to intraoperative findings but there are some essentials surgical steps. PE can be divided into three surgical phases: explorative; ablative; and reconstructive.
The first step is the exploration of the abdominal and pelvic cavity to exclude the presence of metastatic peritoneal disease or liver metastasis. Lateral resectability is assessed during this phase, and in case of massive pelvic wall involvement, the surgery could be aborted.
The goals of the demolition phase are to obtain free margins and to decrease the surgery-associated morbidity. This phase starts with paravescial and Latzko and Okabayashi pararectal spaces development to identify and to dissect the pelvic neurovascular structure and the ureter. Umbilical and uterine artery are dissected and closed at their origin. The dissection is continued caudally in the paravesical space to reach the levator ani muscle. During total or anterior PE, Retzius space is opened ventrally, and the bladder was dissected off the anterior abdominal wall. In case of posterior PE the bladder is dissected completely from the cervix and from the proximal part of the vagina. After colon mobilization, the presacral space is opened (posterior and total PE) while during anterior PE, the rectovaginal space is developed, and the rectum is dissected from the vagina. Subsequently, the surgeon performs the parametrial resection. After section of the umbilical and uterine artery and isolation and section of the deep uterine vein, lateral parametria are resected at the lateral pelvic attachments. In a total or anterior PE, the ureters are resected above their involvement in the tumor, often with an intraoperative assessment of margins. Ventral parametria are transected at the posterior bladder wall (posterior PE) or at the attachment to the inferior portion of the pubic bones (total or anterior PE). The surgeon resects the dorsal parametria at the level of the rectum (anterior PE) or on the presacral space at the level of sacral bone (total or posterior PE). After the resection of the parametria, the exenteration specimen is mobilized centrally in the pelvis. The sigmoid is then resect caudally (posterior or total PE). At this point, steps diverge depending on whether supralevator or infralevator exenteration is planned. Supralevator exenteration finishes with removal of the specimen above the levator muscles. The rectum is resected caudally at the level of the pelvic floor (total and posterior PE); urethra is transected (total and anterior PE) and the vagina are resected below the level of the tumor with adequate margins. These completes detachment of the specimen, which includes bladder, uterus, rectum, and surrounding tissue.
In case of infralevator PE (types II and III), the pelvic floor is resected. A total vaginectomy may be part of infralevator PE. A total vaginectomy and urethrectomy (total or anterior PE) is obtained through a circumferential incision inside the vulva; if necessary, resection of the anus is also made. The vagina is dissected off the elevator muscles unless they have tumor involvement. In this case, the muscle is excised to obtain free margin. In case of total or posterior PE, the rectum is resected caudally at the level of the middle vagina (if a complete perineal resection is not necessary), and the specimen is removed en-block.
The preservation of a distal part of the vagina and the urogenital diaphragm improves the quality of sexual life and decreases the risk of empty pelvis syndrome. In case of vulva or distal part of the vagina or rectovaginal septum involvement, distal colpectomy or vulvectomy, or both are performed from a perineal approach. During type I PE, the specimen is removed abdominally while after infralevator exenteration it can be removed either vaginally or abdominally (
The last phase is the reconstructive one. If the anal sphincter cannot be spared in cases of type II-III PE, the feces are diverted trough permanent end colostomy. During type I PE with anal sphincter sparing, bowel continuity could be restored by a deep colorectal or coloanal anastomosis, if technically feasible. However, the risk of anastomosis breakdown is high in irradiated pelvis.
To restore or substitute urethrovesical function after cystectomy, the surgeon has different possibility: an orthotopic neobladder, supravesical urinary diversion with either continent pouches or incontinent conduits (
In the minimally invasive pelvic exenteration, the surgeon must operate in narrow pelvic spaces, often performing dissection on fibrotic and fragile retroperitoneal tissues, previously subjected to radiation therapy or surgery. Robotic technology can help the surgeon to face these challenging conditions, particularly thanks to the 3-D vision, articulated motion, improved ergonomics, and tremor stabilization. The magnified 3D vision and articulating wristed robotic instruments may allow more accurate dissection (
Moreover, the robotic approach provides minimal fatigue of the operating surgeon and facilitates complex procedures such as intracorporeal suturing (
A 2018 meta-analysis by the Pelvex Collaborative (
When the laparoscopic and robotic approaches were compared, the only difference in perioperative parameters was operative time, with a longer duration of laparoscopic surgery (
Also Puntambekar et al. (
However, the analysis of the operative time in robotics has a significant bias: some authors calculated it as the time from skin incision to the end of the surgery (docking included), others considered only the console time.
Regarding blood loss and hospital stay, our review reports a median blood loss of 365 ml (110-150) and a median hospital stay of 10.5 days 5-37)
Our review showed an estimated median blood loss that was substantially lower than those reported in the laparotomic approach by Martinez et al., ranging from 875 to 6,300 ml (
Hospital stays length was highly variable among the different studies, ranging from 17 to 33 days for the laparotomic group, and from 3.5 to 27 days in the laparoscopic one.
This variability may be explained by the differences in health care systems across different countries in which the studies were performed and by the gradual evolution of perioperative care, given that, over time, we observed a gradual shift from the laparotomic to the laparoscopic approach.
Blood loss, shorter hospital stays, and faster restoration of bowel function are the main benefits of minimally invasive surgery, although the complication rate is superimposable with the open abdominal approach (
Although the Laparoscopic Approach to Cervical Cancer (LACC) Trial showed a difference in survival, depending on the surgical route applied in early-stage cervical cancer (
There are also some drawbacks of robotic technology that should be considered while planning a robotic pelvic exenteration. The first is the high cost of purchasing the robot, which must be added to the costs related to the use of disposable robotic instruments. In addition to the initial cost of the robotic system, the expense for each robotic instrument, which can be used only 10 times, adds significant increase to the total cost. The overall cost of robot-assisted practice is variable, depending on the requirements for each different procedure and on surgeon experience (
An additional problem in robotic surgery may be the conflict between the robotic arms due to suboptimal triangulation, if not placed at an adequate distance between each other, particularly in patients with small abdominal diameters and low BMI.
Furthermore, this should be a criterion in selecting the patients eligible for robotic pelvic exenteration.
In pelvic exenteration, the most critical elements affecting survival outcomes are the lymph node status and the achievement of a free-margin resection (
As described by Bizzarri et al. in a series of 23 patients subjected to pelvic exenteration, the free-margin resection rate of minimally invasive pelvic exenterations was 92.9% (
In the present review, focusing on the robotic approach, we registered a free-margin status in 88% of cases; no patient had macroscopically infiltrated margins while 6 out of 50 patients (12%) demonstrated microscopic infiltration of resection margins. In three patients the histopathological evaluation was not reported.
Also, data regarding long term follow-up are scant. Only 6 of the 13 selected studies had an available follow-up for a total of 31 patients. 19 (61.3%) patients were disease free (NED), 8 (25.8%) were dead (7 death of disease, 1 death of postoperative complication), and 4 (12.9%) were alive with disease (AWD) at 12 months of median follow up. These findings are difficult to interpret because of the small number of patients, the heterogeneity of follow-up duration and the different biology of the analyzed tumors.
Therefore, it is crucial to supplement these data with future studies, enrolling a larger number of patients with a detailed follow-up.
In the reported series of robotic pelvic exenterations, grade 2 postoperative complications occurred in 11 out of 51 patients (21.6%) while grade 3 were recorded in 13 women (25.5%). Only one grade 4 complications were reported (2%). Interestingly the robotic complication rate is overlapping to that reported in the laparotomic approach, ranging from 22 to 32% (
The probability of post-surgical complications is directly impacted by two factors: the specific type of urinary diversion and the primary bowel reanastomosis. In particular, complications related to urinary derivation were more frequent after Miami Pouch diversion. On the other hand, all major complications related to bowel resection occurred in patients who were subjected to direct colorectal reanastomosis.
Therefore, in patients with previous pelvic radiotherapy or systemic chemotherapy, probably bowel anastomosis and continent urinary reconstruction should be avoided. However, this hypothesis must be proved.
Pelvic exenteration represents the very last surgical resort for diseases unresponsive to chemotherapy and already treated with pelvic radiation therapy.
In this context, a careful patient selection remains the milestone of such a mutilating surgery.
Although the introduction of the minimally invasive approach has led to advantages in terms of less blood loss and faster hospitalization time compared to the classic open surgery.
An important step forward should be to investigate the potential equivalence between minimally invasive approaches and the laparotomic one, in terms of long-term oncological outcomes.
Prospective randomized trials in this field will probably never be possible, so we still have to rely on small case series.
In this scenario, multicenter studies with larger numbers of patients and detailed follow-up information will be needed to justify such a surgical effort.
The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author/s.
SC, MA, AF, AE, and GS: writing and data interpretation. MA, RG, ML, and GV: data analysis. MA, SC, and RG: study design and literature search. SC, MA, RG, ML, AF, FF, GV, and GS: data collection. All authors reviewing of the final manuscript.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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