Robotic‐assisted approaches to urachal carcinoma: A comprehensive systematic review of the safety and efficacy outcomes

Abstract Introduction Surgical intervention is the treatment of choice in patients with urachal carcinoma. Due to complications and to reduce hospital stay from open surgery, minimally invasive approaches are desirable. Nowadays, robotic‐assisted surgery has become increasingly popular, and robot‐assisted cystectomy can be performed in patients with urachal carcinoma with low complication rates. Methods We performed a systematic review to search for studies that evaluated patients who underwent robotic‐assisted surgery for urachal carcinoma. The outcomes of interest were the type of cystectomy performed, whether there was umbilicus resection, total operative time, console time, intraoperative complications, estimated blood loss, postoperative complications, time of hospitalisation, positive surgical margins and the presence of documented tumour recurrence. Results In this study, we evaluated three cohorts comprising a total of 21 patients. The median follow‐up period ranged from 8 to 40 months. Medium age was between 51 and 54 years, with a majority (63.1%) being male. One patient (5.2%) underwent a radical cystectomy, and 19 patients (94.7%) underwent to partial cystectomy. Umbilical resections were performed in all cases, and pelvic lymphadenectomy in 14 cases (73.6%). Recurrence occurred in three patients at a median of 17 months postoperation, two cases in the trocar insertion site. Additionally, there was one death, which was attributed to postoperative cardiovascular complications. Conclusion Robotic‐assisted partial cystectomy has a low incidence of adverse outcomes in patients with urachal carcinoma. Controlled studies, ideally randomised, are warranted to establish the comparative efficacy and safety of the robotic‐assisted cystectomy approach relative to open surgery.


| INTRODUCTION
Urachal carcinoma (UrC) is an uncommon neoplasm originating from the urachal remnant and represents less than 0.5% of all bladder neoplasms, 1 with an incidence of less than one in 100.000 per year.
The urachus, an embryonic remnant between the bladder dome and umbilicus, is the origin of UrC. 2 The disease often presents a diagnostic and therapeutic challenge due to its rarity, leading to a dearth of extensive epidemiological studies and dedicated treatment protocols.
Despite its infrequent occurrence, UrC demands attention owing to its aggressive nature and the distinct therapeutic approach it necessitates, diverging from typical urothelial cancers. 3storically, the surgical management of UrC has predominantly involved open partial or radical cystectomy, often extending to the umbilicus or even further, as dictated by tumour extent. 4,5Such procedures invariably involve a sizeable midline incision, carrying the associated morbidities of considerable blood loss, prolonged hospital stays and an extended recovery period. 6The search for improved surgical modalities, offering better postoperative outcomes without compromising oncological efficacy, has been perpetual. 7 this surgical landscape, robotic surgery has heralded a new era of promise. 8,9Over the past two decades, robotic-assisted techniques have revolutionised many aspects of urologic surgery, boasting potential advantages of enhanced precision, reduced morbidity and expedited recovery. 9Yet, the niche application of this technology in the realm of UrC is still nascent, with fragmented evidence and anecdotal experiences forming the bulk of our current understanding.
Recognising this knowledge gap, the present systematic review endeavours to amalgamate the scattered pieces of evidence.Our aim is to offer a comprehensive overview of the current state of robotic treatment for UrC, critically examining its efficacy, safety and outcomes.

| Literature search
The study was conducted in strict compliance with the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) 10  We searched the following databases up to October 2023:

| Study screening and selection
Two independent authors (Caio Vinicius SUARTZ, CVS, and Lucas Motta Martinez, LMM) screened all retrieved records.Discrepancies were resolved by discussion.The full text of the screened papers was selected if found relevant to the present review.

| Selection criteria
We selected articles written in English describing research and studies in humans.There were no other restrictions based on study design or time of publication.Meeting abstracts, case reports, letters to the editor and editorials were excluded.When finding studies from the same institution with overlapping patients and outcomes, we considered only the most recent data.We also excluded previous literature reviews and studies mixing the data of different approaches (open, laparoscopic, and robotic) without specifying the robotic surgery outcomes.

| Variables
We included the number of patients undergoing cystectomy in the study, the type of cystectomy performed, whether there was umbilicus resection, total operative time, console time, intraoperative complications, estimated blood loss, postoperative complications, time of hospitalisation, positive surgical margins, presence of documented tumour recurrence and median follow-up.The primary outcome of our review is to assess and report complication rates, as well as oncological outcomes after robotic cystectomy to UrC.
Given the single-arm nature of this study, without a comparison group, we utilised the Joanna Briggs Institute Critical Appraisal Checklist for Case Series to perform risk of bias assessment 11 The Joanna Briggs Institute (JBI) is an international, membership-based research and development organisation within the Faculty of Health Sciences at the University of Adelaide.The purpose of this appraisal is to assess the methodological quality of a study and to determine the extent to which a study has addressed the possibility of bias in its design, conduct, and analysis.The checklist consists of 10 questions ranging from criteria for inclusion, selections of participants, reported about demographic, clinical and follow-up information and statistical analysis.The answers can be yes, no, unclear or not applicable.A response of 'no' to any of the questions negatively impacts the quality of the study.

| Literature screening
The literature search retrieved 90 papers.Thirty-six duplicate studies were automatically excluded.After the title and abstract screening of the remaining 54 unique references, 30 records were excluded because they were irrelevant to the study's aim.The full texts of the remaining 27 studies were assessed for eligibility.Finally, three studies were selected and included.Figure 1 shows the PRISMA flowchart of the literature search.We summarised in Table 1 information about the selected articles, such as institution, year of publication, country, patient gender, total number of patients and surgical technique utilised.

| Quality assessment
The quality assessment of individual studies is reported in Table 2.All studies had a clear outline of the inclusion criteria for patient selection.

| Clinical and epidemiological characteristics
In a comparative series from the Netherlands, Stokkel (2022) evaluated the outcomes of robot-assisted versus open partial cystectomy for UrC. 14The study spanned from 1994 to 2020, with eight patients undergoing the procedure, seven of whom had adenocarcinoma.
Patients who underwent robotic surgery presented a median age of 60 years, with a range from 42 to 79 years, 5 men and 3 women. 14e Madeb study conducted between January 2005 and All patients presented with hematuria, dysuria or urinary mucus.Preoperative evaluation included MRI and CT scans with mass in the dome or anterior bladder wall.Cystoscopy with biopsy and colon preparation were utilised in all patients. 13

| Surgical technique
In the methodology proposed by the authors, [12][13][14] , the patient was placed in the Trendelenburg position to enhance the surgical exposure of the pelvic region.Flexible intraoperative cystoscopy was used to assist in resection for all patients, and just James mentioned the robotic platform utilized (Da Vinci S and SI robotic systems).All studies located the camera port between 2 and 5 cm cephalad to the umbilicus to facilitate both the umbilectomy, which was performed by a circumferential incision at a distance of 2 cm from the umbilicus, and the closure of the incision with the umbilicoplasty described by Schaeffer 15 preserving the aesthetic aspect.Strategic placement of the camera port incision was prioritized to allow its subsequent incorporation into an umbilectomy incision, thereby reducing the necessity for additional incisions and associated surgical trauma.After the camera port placement, two 8-mm robotic ports and one 12-mm assistant port were inserted into the right iliac fossa.In certain instances, an additional trocar was employed to assist the procedure.
The configuration of the port sites was planned to promote the ergonomic handling of instruments, ensure optimal articulation of the robotic arms, and facilitate surgical access to urachus with minimal aesthetic impact.

| Perioperative considerations
In the series reported by Stokkel et al., 14 , the established therapeutic approach for UrC involved partial cystectomy with En-bloc excision of the urachal remnant and the umbilicus.All cases were performed with flexible cystoscope assistance, and the bladder was distended with 300 mL of saline to improve the visualization of robotic excision.
The urachus was sectioned at the umbilical junction and pelvic lym- Madeb's study emphasised that the positioning and placement of portals are fundamental to optimising the range of motion for the robotic arms, facilitating the complete resection of the urachus. 12e bladder was distended with 250-300 mL of saline to improve the visualisation to bladder resection and the urachus was sectioned at the umbilical junction.The dissection of the Retzius space revealed the anterior pelvic fascia, allowing bilateral pelvic lymphadenectomy and urachal excision with the umbilicus.The radical cystectomy procedure included the dissection of the ureters, ovarian and uterine arteries, and the block removal of the anterior vaginal wall and urethra.
Average blood loss was reported as 118 m, with a range of 25-300 mL.The duration of the operative time was observed to vary from 120 to 300 min. 12e total exenteration of the anterior pelvis was completed in 480 min, followed by a six-day postoperative hospitalisation.For those submitted to partial cystectomy, the discharge time varied from 36 to 48 h.Routine cystography was performed within 10 days after partial cystectomy, confirming the absence of urinary leaks. 12e study by James et al. utilised the Hason pneumoperitoneum method, utilising a six-port array comparable to that in radical prostatectomy, which was modified by elevating the port sites by 3 cm to guarantee unobstructed access to the urachal region.The umbilicus was excised, aligning with the camera port positioned 2 cm above it.To enhance the surgical field, the bladder was inflated with 200 mL of air.A dual-lens camera system, with zero and 30 angles, afforded clear visualisation for the bladder dissection and cystotomy, maintaining a 2-cm margin from the identified bladder mass via integrated flexible cystoscopy.Bladder closure and drain insertion were performed in all selected studies with a double-layered Vicryl 2-0 suture and a Jackson-Pratt drain into the Retzius space. 13mes et al. referred to an operative time average of 184 min, with a range of 130 to 240 min, and the mean duration of console operation of 120 min, ranging from 70 to 170 min. 13The estimated blood loss was minimal, averaging 50 mL, with no cases requiring conversion to open surgery.The average hospital stay was 4 days, with a range of 3 to 7 days.Drains were typically removed after 2.5 days.
The cystography conducted at the 10-day mark postoperatively confirmed the absence of leaks.The postoperative course was uncomplicated, with no instances of positive surgical margins. 13

| Oncological outcomes
In the Stokkel series, patients had a median follow-up of 40 months and a median overall survival of 28 months. 14Local recurrence was observed in 15% of the cohort.The median time to recurrence was 21 months.One patient died of postoperative complications related to past medical history of cardiovascular disease that included an abdominal aortic prosthetic grafting.Anticoagulant therapy was discontinued prior to surgery, and a prophylactic dose of heparin was administered.After the surgery, the patient received brachytherapy with strict immobilisation for 3 days and ended up developing an acute arterial infrarenal occlusion of the aortic prosthetic graft 4 days after the surgery and died.There was only one case of persistent urinary leak for which the indwelling catheter was successfully left in place for a more extended time. 14okkel et al. described two port sites recurrences post robotassisted partial cystectomy.The author utilized positron emission tomography-computed tomography (PET-CT) with fluorodeoxyglucose (FDG) to identify an umbilical lesion at the anterior port site of the robotic trocar, which biopsy confirmed as a metastatic UrC tract. 14 the first case, subsequent to the FDG-PET-CT imaging, the patient underwent a secondary diagnostic laparoscopy.This revealed multiple peritoneal lesions proximal to the excised umbilicus, the site of UrC mobilisation during the initial surgery.The patient was treated with cytoreductive surgery and hyperthermic intraperitoneal chemotherapy (HIPEC).Seven months postsurgery, additional lesions were identified bilaterally at the lower abdomen anterior to the robotic-assisted partial cystectomy trocar sites and at the median laparotomy site.Despite resection of all abdominal wall lesions, disease progression ensued, culminating in patient death after 10 months.
In the second case, the patient received adjuvant brachytherapy along the bladder suture lines.Although the initial resection was complete (R0), the patient experienced a local recurrence 2 years postoperatively.The recurrence was managed with external beam radiotherapy, local resection, and brachytherapy.A subsequent metastasis at the trocar site led to its local excision and further investigative diagnostic laparoscopy, which revealed advanced peritoneal carcinomatosis.Owing to the significant tumor load, additional cytoreductive surgery with HIPEC was deemed infeasible.The patient was administered palliative chemotherapy and died approximately 1 year following the diagnosis of peritoneal disease.
Kaplan-Meier analysis revealed no significant difference in recurrence-free survival between patients undergoing robot-assisted surgery and open partial cystectomy.Tumour sizes were predominantly under 4 cm, with most patients achieving negative surgical margins (88%).Lymphovascular invasion was identified in a single case.Similarly, James et al. reported no recurrences within an average follow-up of 32 months without deaths. 13

| DISCUSSION
3][14][15][16] However, it is essential to manage the tumours carefully and to be cautious when removing the specimens, thus avoiding the implantation of tumour cells in the trocar sites, as evidenced by Stokkel. 14ntica et al. (2020) highlight the potential underreporting of such recurrences, suggesting a publication bias that may skew data to centres reporting favourable results. 18This challenges the accuracy of reported incidence rates and raises concerns about the generalisation of results, reinforcing the importance of works such as that of Stokkel et al. when reporting in detail cases of recurrence in port sites. 14ogress in surgical proficiency, technique refinement, careful manipulation of the tumour and the containment of the urine leak in the moment of partial cystectomy need to be paramount in preserving tumour integrity and preventing the spillage of tumour cells in the abdominal cavity.Adopting techniques such as replacing saline solution to insufflation with air to facilitate bladder filling, as suggested by Peak and Hemal (2020), exemplifies some strategies that aim to minimise the chance of tumour recurrences. 19wever, despite these advances, recurrences at the port site remain a nonnegligible risk.These cases, highlighted by the literature cited, reinforce the need for postoperative surveillance and establishing robust protocols for local control.[16][17][18][19] Madeb (2006) and James (2015) have documented the evolution of robot-assisted surgical techniques, with a notable decrease in positive surgical margins as surgeons move up the learning curve.This indicates improved surgical accuracy and suggests a potential for better oncological results. 12,13wever, a comparison between open, laparoscopic and robotic techniques is hampered by the need for more scientific research describing the outcomes in a comparative approach to patients with UrC.Currently, there is an absence of research on the robotic surgical technique employed relating it to clinical outcomes since most studies are case reports without technical details, perioperative and/or oncological outcomes.There are innumerable series of UrC that did not stratify patients by the surgical technique employed, analysing patients operated with open, laparoscopic and robotic approaches as a single group.
All studies used the Intuitive ® robotic platform (da Vinci Si, X, or Xi), which reinforces the need for scientific validation of the new multiports and single ports robotic platforms to treat this specific group of patients.
The limited number of cases in these three series restricts the generalizability of the results.New studies individualising patients in the analysis by surgical technique are necessary to ensure the surgical safety and oncological efficacy of treatment with robotic assistance.

| CONCLUSION
Robotic surgery represents a paradigm shift in the management of UrC potentially offering superior results.Robotic partial cystectomy in this clinical condition has a low incidence of adverse outcomes and can be done safely and effectively, but controlled studies, ideally randomised, are justified to establish the comparative efficacy and safety of the robotic-assisted approach in relation to open surgery.
statement on October 01, 2023.A research question was established based on the Patient-Index test-Comparator-Outcome-Study design (PICOS) criteria, which is as follows 8 : What is the current paradigm of robotic surgery for UrC?The search strategy was as follows: (UrC OR urachal adenocarcinoma OR urachal cancer) AND (cystectomy OR cystoprostatectomy OR bladder resection OR partial cystectomy) AND (robotic OR da Vinci OR robotic-assisted OR robotic-assisted).

February
2006 included five patients with a median age of 51 years, ranging from 24 to 68 years.Two men and one woman with the anatomopathological revealing two well-differentiated and one moderately adenocarcinoma of the urachus colonic subtype with margins and negative lymph nodes.Another two cases presented anatomopathological leiomyoma and squamous metaplasia in the urachus.The clinical presentations varied between gross hematuria and a normal physical examination.The computerised tomography revealed, in all cases, bladder mass in dome topography extending to the anterior wall without lymph node involvement. 12F I G U R E 1 Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) flowchart of the literature search.The James study, conducted from 2009 to 2014, consisted of five men and three women with a mean age of 53.5 years (±10.3years).
Abbreviations: IQR, interquartile range; SD, standard deviation. 14 T A B L E 2 Quality assessment of individual studies.