Robot-Assisted Reconstructive Surgery for Ureteral Malignancy: Analysis of Efficacy and Oncologic Outcomes

Introduction

I n the past three decades, there has been a slight increase in the incidence of urothelial cancer, with upper urinary tract urothelial-cell carcinoma comprising 5% of all urothelial malignancies. ^1,2 The gold standard for the management of upper urinary tract transitional-cell carcinoma is open nephroureterectomy. ^3,4 Eventually, open segmental ureterectomy emerged as a surgical alternative to open nephroureterectomy, and studies suggested that, in cases of low-grade, noninvasive transitional-cell carcinoma, segmental ureterectomy provided equivalent outcomes to the gold standard of care with the added benefit of conserving renal functional mass. ^5,6

With the inception of minimally invasive surgery, however, laparoscopic techniques began to supersede open surgery in the treatment of patients with urological neoplasms because of decreased morbidity and superior cosmetic outcomes, while maintaining oncologic control. ⁷ Roupret and associates ⁸ demonstrated the safety and feasibility of laparoscopic distal ureterectomy for upper urinary tract transitional cell carcinoma in six patients. These authors reported two cases of recurrence during a follow-up. In addition, laparoscopic nephroureterectomy for patients with upper urinary tract transitional-cell carcinoma has become a widely accepted practice. ⁹ These laparoscopic achievements helped to stimulate the use of robot-assisted surgery for the same procedures. It was hoped that robotic technology, which had already gained widespread popularity in the treatment of patients with prostate cancer, may also provide an alternative minimally invasive management approach for upper urinary tract neoplasms.

Despite these technologic surgical advancements, analyses regarding perioperative outcomes and long-term oncologic follow-up are needed to evaluate the practical utility of robot-assisted techniques for malignant ureteral surgery. Another challenge is the low incidence of upper tract transitional-cell carcinoma, which makes powerful studies difficult to conduct, especially in a prospective manner. We consequently present our experience of six cases of mid and distal ureteral malignancy treated using surgeon-controlled robotic techniques with analysis of perioperative and oncologic outcomes.

Patients and Methods

We retrospectively examined our Institutional Review Board-approved, prospectively maintained robotic surgical database to isolate cases of ureteral malignancy managed using robotic technology, excluding any patients treated with nephroureterectomy.

We identified six patients who underwent robotic surgical treatment of ureteral neoplasia since 2008. Each patient demonstrated a mid or distal ureteral lesion and obstruction of the ipsilateral renal moiety on cross-sectional functional imaging with CT urography or MR urography. All patients subsequently underwent cystoscopy and ureteroscopic biopsy of their lesion, which in all cases demonstrated low-grade, superficial disease. No patient was found to have bladder lesions on preoperative cystoscopy. Patients were offered various treatments, including nephroureterectomy, and all elected for robotic segmental excision with reconstruction. No patient received chemotherapy or radiotherapy at any time.

All robot-assisted surgeries were performed at our medical institution by the senior author (AKH) using the da Vinci S system. Patients underwent standard preoperative assessment, including laboratory blood work, cross-sectional functional imaging, and anesthesia evaluation. All patients received bowel preparation 1 day before surgery and prophylactic antibiotics before induction of anesthesia. Demographic and perioperative data were chronicled prospectively, with special emphasis on oncologic and functional outcomes.

Our operative techniques for robotic ureteral surgery with reconstruction have previously been described in detail. ¹⁰ Furthermore, our video of this robotic technique recently became available for review. ¹¹ Intraoperative frozen sections were routinely sent to assess appropriateness of surgical margins, and stent placement in each case was performed intracorporeally using robotic assistance, as previously reported. ^12,13 In cases necessitating excision of the bladder cuff, this was performed extravesically, and the subsequent cystostomy was closed in two layers using 3-0 polyglecaprone suture. ^14,15 In these patients, the bladder catheter was maintained for 7 to 10 days before removal.

Patients underwent stent removal 4 to 8 weeks postoperatively in addition to a standard oncologic and functional surveillance protocol to evaluate for recurrence of malignancy or obstruction as follows: Standard laboratory basic metabolic panel analysis postoperatively at follow-up clinic visits, CT urography performed approximately 12 weeks after surgery, and cystoscopy and retrograde ureteropyelography with bladder and selective cytologic assessments at 6 months postoperatively. Patients would then follow-up with cystoscopy and cytologic assessment and alternate between CT urography and cystoscopy with retrograde ureteropyelography every 6 months for the first 2 years, and 12 months thereafter if results were normal. The single patient found to have B cell lymphoma on final pathology results underwent a positron emission tomography scan and CT scan of the chest, abdomen, and pelvis at 4 weeks postoperatively, in addition to the above.

Results

Patient characteristics and perioperative data are summarized in Table 1. Preoperative, baseline creatinine in all patients was normal and thus did not influence our decision to perform nephron-sparing surgery.

The mean total operative time including cystoscopy was 268.5 minutes (188–400), mean estimated blood loss was 72.5 mL (<30–150 mL), and the mean postoperative length of stay was 1.8 days (1–2). There were no intraoperative complications or conversion to pure laparoscopic or open surgery, and no patient received a blood transfusion.

Four patients underwent robotic distal ureteral excision, excision of a bladder cuff, and ureteroneocystostomy. In three of these patients, a bladder psoas hitch was necessitated to facilitate reconstruction. The other two patients received robotic midureteral excision with primary ureteroureterostomy with intracorporeal Double-J stent placement.

The only perioperative complication was the development of a postoperative hydrocele in one patient, which resolved with conservative management.

Final pathology results are listed in Table 1. Five of the six patients were found to have urothelial carcinoma; one patient had a diagnosis of non-Hodgkin B cell lymphoma and was subsequently referred to the medical oncology department. There were no positive surgical margins. Of the patients with transitional-cell carcinoma, one patient demonstrated high-grade invasive disease on final pathology results and is under close surveillance. He remains free of recurrence 30 months postoperatively.

At a mean follow-up of 33 months (28–39), there was only one malignant recurrence—a low grade transitional-cell carcinoma detected in the bladder that was treated with transurethral resection. This occurred 6 months postoperatively in a patient who previously had superficial transitional-cell carcinoma of the bladder before his ureteral involvement. Since this recurrence, this patient has been free of disease for 28 months. In addition, no patient has demonstrated obstruction postoperatively.

Discussion

Laparoscopic and robotic techniques are evolving into the standard of care for various ureteral pathologies, as is the case with pyeloplasty for ureteropelvic junction obstruction. While laparoscopic methods have been developed and studied, they require an advanced skill set to perform. Meanwhile, robot-assisted laparoscopy augments traditional minimally invasive methods by offering added advantages of a magnified, high-definition, three-dimensional view, an ergonomic setup with endowristed instruments, a wide working space, motion scaling, tremor filtration, and numerous degrees of motion.

In the past several years, the da Vinci robotic surgical system has been widely used in radical prostatectomies for localized prostate cancer. ^{16 –18} Further applications of this robotic technology have raised interest regarding its appropriateness in other areas of urologic surgery, including ureteral surgery. ¹⁰ In 2006, the feasibility of managing upper urinary tract transitional-cell carcinoma was demonstrated in a series with nine patients using robot-assisted laparoscopic nephroureterectomy. No complications were reported, and all patients had negative surgical margins. One patient experienced remote neoplastic recurrence at the bladder neck 6 months postoperatively. ¹⁹ A newer technique has been reported for upper urinary tract neoplasms without changing the position of the robot or placement of ports. ¹⁴

Shortly thereafter, it was established that laparoscopic robot-assisted distal ureterectomy can be performed, even in cases necessitating a psoas hitch. ²⁰ These authors proposed that robot-assisted laparoscopic distal ureterectomy may provide an alternative in the management of ureteral malignancy. This article was limited, however, in that it merely described the technique used and did not record the number of patients, complications that occurred, or long-term follow-up.

In addition, it has been demonstrated that robot-assisted distal ureterectomy can be performed for both benign and malignant indications. Their series included 11 cases, 5 of which involved upper tract ureteral transitional-cell carcinoma. There were two perioperative complications: An external iliac vein injury and persistent bleeding from an ureterovesical anastomosis. This series reported two cases of ipsilateral recurrence in the renal pelvis managed with hand-assisted laparoscopic nephroureterectomy. For the five transitional-cell carcinoma cases, a mean follow-up time of 24 months was reported. ²¹

The safety and feasibility of robot-assisted ureterectomy with ureteral reconstruction has been illustrated in nine patients with distal ureteral urothelial carcinoma. ²² No patients had positive surgical margins; at a mean follow up of 23 months, seven patients experienced malignant recurrence. Two complications were reported—an aspiration pneumonia and a ureteral stricture at the site of repair—both of which were managed without further sequelae.

Our study builds on these previous investigations by demonstrating the efficacious and durable management of mid and distal ureteral neoplasms with robotic surgery. While the patients in our communication with low-grade urothelial carcinoma are candidates for segmental ureterectomy and subsequent reconstruction, we firmly believe that those with evidence of high-grade or invasive ureteral malignancy are better served oncologically with nephroureterectomy, regional lymphadenectomy, and excision of the bladder cuff. We are also vigorous in terms of our postoperative surveillance, as previously outlined, especially in patients who demonstrate upstaging or upgrading on final pathology results.

Conclusion

Our experience with robot-assisted ureterectomy and reconstruction illustrates a viable alternative in the management of mid and distal ureteral neoplasms in selected patients with low-grade malignancy. Patients with evidence of high-grade or invasive ureteral malignancy are better served oncologically with nephroureterectomy, regional lymphadenectomy, and excision of the cuff of the bladder. This method is achievable, safe, and durable in the hands of an experienced robotic team. Our initial results are encouraging, but further evaluations with more patients and longer follow-up are needed to validate this approach from both oncologic and functional perspectives.