Abstract
Background and Purpose:
During the last decade, the annual volume of robot-assisted prostatectomies performed in the United States has risen steadily. Refinements in surgical technique, understanding of anatomy, and experience have led to more complex patients being offered surgery for management of organ-confined prostate cancer. Complication rates of robot-assisted prostatectomy have been reported in several articles; however, a paucity of data exists when evaluating ureteral injuries sustained during robot-assisted prostatectomy. No standardized universal criteria for reporting and grading of complications exists; therefore, the Martin-Donat criteria with Clavien-Dindo classification system were used to evaluate ureteral injuries in our series.
Patients and Methods:
From January 2001 to June 2013, 6442 consecutive patients were treated with robot-assisted prostatectomy at the same institution by one of five surgeons. All complications were documented through a prospectively maintained prostate cancer database with supplementation from electronic medical records, operative and nursing notes, claims data, discharge summaries, outpatient and emergency visits, institutional morbidity and mortality data, as well as National Surgical Quality Improvement Program data. The Martin-Donat criteria were used to facilitate the accurate and comprehensive reporting of surgical complications while complication severity was assigned following the Clavien-Dindo classification system.
Results:
Three patients sustained ureteral injuries (ureteral transection) in our series. Both surgeons were beyond their learning curve (greater than 1000 cases) when the injuries occurred; one patient needed readmission, and all patients had risk factors predisposing them to ureteral injury. Each patient was managed with robot-assisted ureteroneocystostomy (1), open transureteroureterostomy (1) and robot-assisted ureteroureterostomy (1) respectively.
Conclusions:
Ureteral injuries are uncommon; however, thorough preoperative evaluation and surgical planning could identify patients at high risk for sustaining ureteral injury during prostatectomy. Measures can be taken preoperatively or intraoperatively to reduce the probability of ureteral injury, eliminating the necessity for additional procedures postoperatively.
Introduction
R
Ureteral injury has been reported in many prostatectomy series regardless of surgical approach. Possible treatments include percutaneous nephrostomy tube placement, ureteral stent placement, ureterostomy, or reimplantation and even hemodialysis in the case of a solitary kidney, which result in delayed convalescence. 4 Risk factors for ureteral injury include: History of infection, transurethral resection of the prostate, abdominal surgery, radiation therapy, extended pelvic lymphadenectomy for high-risk disease, large prostate glands and median lobes. 4
Recent publications have prompted us to review our own experience with ureteral injury during RARP using our prospectively maintained, single-institution, multisurgeon series. We provide an in-depth analysis of three patients who sustained ureteral injuries while undergoing RARP. Complications were captured using the Martin-Donat criteria for comprehensive reporting of complications and the Clavien-Dindo classification system for severity of injury. 5 –8 We also provide a review of contemporary series evaluating ureteral injury for all surgical approaches while providing comparisons with our robotic series.
Patients and Methods
Patient selection and hospital course
From January 2001 to June 2013, 6442 patients received RARP for treatment of clinically localized prostate cancer by one of five surgeons using the technique of Menon and associates 9 with technical modifications in 2007 and 2009. 10,11 All surgeries were performed using either a three- or four-arm da Vinci Surgical System (Intuitive Surgical, Sunnyvale, CA). Our surgical approach consisted of a six-port transperitoneal technique with anterior dissection and early identification of the prostatovesical junction. Pelvic lymphadenectomy was performed in intermediate- or high-risk patients (prostate-specific antigen (PSA) >10, Gleason ≥7, clinical T2 disease, salvage prostatectomy) after prostatectomy. Lymph nodes were removed routinely from the external iliac, internal iliac, and obturator nodal groups, while extended lymph node dissection included removal of tissue to the level of the common iliac bifurcation.
All patients had sequential decompression devices placed before anesthesia induction, and some patients received 5000 units of unfractionated subcutaneous heparin. A clear liquid diet was initiated on postoperative day (POD) 0, and patients were advanced to a regular diet as tolerated. Postoperative laboratory studies were not routinely obtained. Before 2008, a urethral catheter was left in place after the anastomosis; since 2008, a percutaneous suprapubic cystostomy catheter was the preferred method of urinary drainage. Patients return 6 to 10 days after prostatectomy for catheter removal, and cystography was performed if clinically indicated. 11 A Jackson-Pratt drain was left at the discretion of the surgeon.
Data collection and complication analysis
The patients comorbid conditions as well as complications were captured through a review of a prospectively maintained prostate cancer database supplemented by institutional electronic medical records, operative and nursing notes, discharge summaries, outpatient and emergency room visits, hospital claims data, institutional morbidity and mortality records, a hospital-mandated sampling of National Surgical Quality Improvement Program data 12 ; telephone or written correspondence with patients, referring physicians or hospitals. 8
All complications from the date of surgery to the date of analysis are included in this report. The Institutional Review Board of Henry Ford Hospital approved this study, and data collection with follow-up correspondence was performed in accordance with the United States Health Insurance Portability and Accountability Act. Ureteral complications were categorized using Clavien-Dindo severity of injury classification system 7 while the Martin-Donat criteria allowed investigators to accurately report the clinical course and treatment for the injury sustained. 5,6
The Martin criteria are a set of 10 guidelines that facilitate the accurate and comprehensive reporting of surgical complications. 5 The following criteria and requirement for each aspect of data collection are recommended. The method of accruing data should be defined in either a prospective or retrospective fashion. The duration of follow-up should clarify a specific time frame for accrual of postoperative of complications (e.g., 30 days or same hospitalization). The outpatient information after discharge should be included while complications whether in the same or separate hospital system are documented. A definition and specific inclusion criteria for the complications are provided. The mortality rates as well as cause of death are included in the postoperative period. The morbidity rate and overall total number of complications are recorded. Procedure-specific complications are included. Some type of severity grading index should be used that designates minor and major complications. Either median or mean length of stay data are documented. Risk factors with evidence-based stratification are isolated and discussed. Our study satisfied all 10 Martin criteria. 5
Statistical analysis
Categoric distributions are reported as counts. In series in which fewer than five events occurred, the Fisher exact test was used to calculate statistically significant differences between previously published data and our series. If greater than five events occurred, chi-square analysis was used to determine significant differences. A two-tailed P value of <0.05 was considered statistically significant. Analyses were performed using the statistical package for social sciences (SPSS version 19).
Results
Review of the database (N=6442) found three ureteral injuries that occurred in the patients operated on by two of the five surgeons. At the time of the injury, both surgeons had performed more than 1000 robot-assisted prostatectomy cases each, a series that is well beyond an acceptable learning curve of 100 cases. None of the injuries were identified intraoperatively, and all patients needed cross-sectional imaging or antegrade pyelography to confirm ureteral disruption postoperatively. Each complication was managed with a different surgical approach: Robot-assisted ureteroneocystostomy, (UNC–1) open transureteroureterostomy (TUU–1), and robot-assisted ureteroureterostomy (UU–1).
The first patient presented with abdominal pain, general malaise, and high fluid output from a port site during the first month of his convalescence. Cystograms obtained did not show contrast extravasation while laboratory studies revealed mild elevation of serum creatinine. This prompted an abdominal CT scan, which demonstrated a right distal ureteral injury and urinoma. He was admitted for percutaneous drainage and nephrostomy tube placement. A ureteral stent was placed for several months. On removal of the stent, the ureter began to obstruct, and he underwent robot-assisted ureteral reimplant approximately 1 year after the prostatectomy. We postulate that ureteral injury occurred during bladder takedown as a result of difficult dissection secondary to adhesions.
The second patient had received brachytherapy for low-risk prostate cancer. Surveillance PSA testing revealed biochemical failure, and rebiopsy proved high-risk disease; he then underwent prostatectomy. As a result of his salvage status and adverse pathologic biopsy features, an extended pelvic lymphadenectomy was performed. We believe that his ureter was transected during pelvic lymphadenectomy as a result of a laterally deviated left ureter. Although he had chronic kidney disease (CKD) stage 1 at baseline, he progressed to CKD stage 2 after a prolonged hospitalization, then required open TUU and bladder repair.
In our third patient who was postcadaveric renal transplant into the right iliac fossa, anuria developed as a result of complete transplant ureteral transection during the bladder takedown. This necessitated hemodialysis, then robotic UU on the same admission. His renal failure improved to preoperative levels, and he was discharged. Table 1 details individual patient characteristics.
BL=bilateral; LND=lymph node dissection; ESRD=end-stage renal disease; GFR=glomerular filtration rate; CKD=chronic kidney disease.
Discussion
Ureteral injury is a known complication of any pelvic surgery, and most investigators report low frequency of complications and repairs during prostatectomy. Several published series have evaluated ureteral injuries during radical prostatectomy in the open, perineal, laparoscopic, and robotic approaches. Retropubic prostatectomy reveals the incidence of ureteral injury to be 0.05% to 1.6% 13 –16 while laparoscopic varies from 0.1% to 0.5%. 17 –23 Review Table 2 summarizes recent publications (after 2000) in English regarding ureteral injury. 1,2,4,13,17 –21,24 –26 Review series did not provide patient-specific data regarding injuries but documented frequency. 1,2
Indicates review manuscript data extraction.
ORP=open radical prostatectomy (retropubic); NA=not available; LARP=laparoscopic assisted radical prostatectomy; RPP=radical perineal prostatectomy; BL=bilateral; PCN=percutaneous nephrostomy; RARP=robot-assisted radical prostatectomy; IV=intravenous; MIRP=minimally invasive radical prostatectomy (laparoscopic/robotic).
Table 3 details comparisons between the current series and previously published data. One publication described bilateral ureteral ligation with bilateral ureteroneocystostomies during perineal prostatectomy. 24 Comparing our robotic series to available review data reveals that our series has far fewer ureteral complications and repairs when compared with larger aggregates of published data. In addition, significantly fewer injuries were noted in our series in comparison with Guillonneau and colleagues, 17 Yee and coworkers, 26 and Park and associates, 21 in the laparoscopic and robotic groups. Other series did not have statistically significant differences in the frequency and repair of ureteral injuries, regardless of approach.
Indicates review manuscript data extraction.
We present data from the largest series of consecutive robot-assisted prostatectomies with ureteral complications documented by Martin-Donat criteria and Clavien grades. 5 –7 Our results, showing a low rate of injury (incidence of 0.046%, frequency less than 1 in 2000 patients), are consistent with other published series of both minimally invasive and open prostatectomy. 1,2,4,13 –26 All patients who sustained injury had difficult aspects to their dissections and altered anatomy, presenting a unique challenge to the surgical team.
Our first patient had previous surgeries that complicated his dissection. Initially, extensive adhesiolysis was needed for port placement because of bilateral inguinal mesh herniorrhaphy. Dense extensive fibrotic tissue reactions resulted in difficult dissection and ill-defined anatomic planes. His ureter was most likely injured during bladder takedown and lysis of adhesions. He needed percutaneous nephrostomy decompression, ureteral stent placement, and observation for 12 months. Mag-3 Lasix renal scan revealed hydronephrosis and obstruction with T ½ greater than 30 minutes after stent removal; he therefore underwent successful robot-assisted UNC. A UU was not performed because of dense scaring of the distal ureter. His postoperative course was uncomplicated. Failure to identify the ureter in situations of complex and unusual anatomy has been described as a factor contributing to ureteral compromise. 4,17 Review of the CT images that demonstrated the injury showed an unusually lateral course to the distal ureter. This variation in anatomy may have contributed to ureteral damage (Fig. 1).

Computed tomography reveals a complete right distal ureteral transection with resultant large urinoma formation.
Teber and colleagues 4 similarly reported that one of their patients with a history of prostatitis had a difficult posterior dissection resulting in the inability to differentiate the vas deferens from the ureter. Authors postulate that because of excessive traction and dissection posteriorly and laterally, ureteral injury occurred after bladder neck transection. In that same series, another patient experienced ureteral transection as a result of a protruding median lobe mandating a lateral dissection during bladder neck transection placing the ureters at risk.
Our second patient presented for salvage prostatectomy. He had brachytherapy for low-risk Gleason (3+3) prostate adenocarcinoma 2 years previously; PSA nadir was 0.5 ng/mL. He had a biochemical recurrence with a PSA rise to 13.3 ng/mL, and repeated biopsy demonstrated multifocal Gleason 8 and 9 disease. Lysis of adhesions was needed as a result of previous appendectomy and cholecystectomy. As a result of high-risk pathologic features, an extended pelvic lymphadenectomy was performed. 26 His left ureter was likely transected during the extended lymphadenectomy. 4,19
His postoperative course was complicated by a urine leak and wound infection at the umbilicus that was treated with open TUU. The decision to perform an open surgery was made because of purulent drainage from the umbilical incision. Because of the recent anastomosis in a radiated field and ureteral length available, left to right TUU was performed. He had preexisting CKD stage 1. Although the patient did have a mild decrease in postoperative glomerular filtration rate (GFR) and increase in creatinine, he recovered with stable stage 2 CKD 1 year postoperatively. He progressed to end-stage renal disease necessitating hemodialysis.
CKD stage 4 developed in the third patient because of hypertension, and he underwent renal transplant (right iliac fossa 2006) with subsequent progression to end-stage renal disease because of chronic allograft nephropathy, although dialysis was not yet necessary. He received a diagnosis of low-risk prostate cancer, and after consultation with his nephrologist, elected definitive local therapy in order to be replaced on the renal transplant recipient list. During robot-assisted prostatectomy, extensive lysis of adhesions was performed. Review of intraoperative film revealed that his ureter was transected during bladder takedown. Postoperatively, the patient was anuric, renal ultrasonography demonstrated mild pelvicaliectasis, and antegrade nephrostography revealed a complete ureteral transection (Fig. 2). The patient received one dialysis session, and an uncomplicated robotic UU (end-to-end) was performed on POD 3. The intraoperative decision to perform a UU was made because of the proximity and viability of the ureteral ends. His GFR returned to baseline postoperatively.

Antegrade nephrostogram shows a complete midureteral transection demonstrating contrast extravasation in a solitary kidney.
Despite its relatively rare occurrence, previous studies have isolated trends for patients who are at high risk for ureteral injury during prostatectomy. All of our patients had previous abdominal surgery, and none of their injuries was noted intraoperatively. Salvage prostatectomy or extensive adhesiolysis as a result of altered or ambiguous anatomic planes was noted in all instances. 4,17,20 Extended lymphadenectomy is another significant risk factor for ureteral injury. 4,19 Our patient who underwent extended pelvic lymphadenectomy for high-risk prostate cancer recurrence needed a TUU as a result of the extent of ureteral loss and recent anastomosis in an irradiated field. Lymph node dissection around the common and internal iliac vessels may result in inadvertent injury because of the close proximity of the ureter to these structures. 19,26 If an incomplete ureteral transection is noted intraoperatively, ureteral stent placement and primary repair may result in restoration. 27
Guillonneau and coworkers 17 reported a 0.5% incidence of ureteral injury with three injuries in 576 laparoscopic prostatectomies. One injury occurred during posterior dissection of the vas and seminal vesicles and was laparoscopically repaired with an end-to-end primary anastomosis intraoperatively. Two other injuries were noted during peritoneal incision (at the lateral vesical peritoneum) but were identified postoperatively. One needed ureteral stent insertion and the other needed open ureteral reimplant.
Lepor and associates 13 described one patient with a ureteral ligation with subsequent UNC in their open retropubic prostatectomy series. This was the result of undiagnosed schistosomiasis infection and adhesions. Stolzenburg and colleagues 19 reported two patients with ureteral injuries during endoscopic extraperitoneal prostatectomy; one was treated with bilateral ureteral stent placement and one with bilateral percutaneous nephrostomy tubes. Investigators believe that ureteral injuries were most likely to occur during extensive pelvic lymph node dissection or during dissection of the posterior bladder neck and anastomosis because of the proximity of adjacent structures. Hu and coworkers 20 reported a ureteral injury during bladder neck dissection that was managed with ureteral reimplant. Dinlenc and colleagues 28 described a patient in their robotic series who had a ureteral injury during posterior dissection of the seminal vesicles, managed by primary UU at the time of transection.
Preventing ureteral injuries remains the best practice. A thorough history can identify patients with complicated anatomy who are at higher risk for ureteral injury. Those who are at high risk may benefit from intraoperative dissection and identification of the ureters, which may prohibit injury. 4 We do not advocate routine placement of preoperative ureteral catheters, although there may be some cases in which this would be helpful. Risk factors include: Previous surgeries (prostate resection), renal transplant, extensive adhesiolysis, previous pelvic irradiation, difficult posterior dissection, enlarged glands and median lobes. Intraoperative methods to ensure ureteral integrity include infusion of indigo carmine with furosemide intravenously to evaluate leakage from the ureter. Ureteral stent insertion is encouraged if there is suspicion of ureteral damage or if the bladder neck transection is in very close proximity to the ureteral orifices. 27 –29
In those who have undergone previous resection of the prostate or have large median lobes, insertion of open-ended ureteral catheters or Double-J stents before or during prostatectomy is an effective strategy to identify vital structures and preclude injury. 4,19,29 Early identification of small injuries may be amenable to ureteral stent placement, primary repair, or immediate UNC or UU for larger injuries. If ureteral injury does occur, intraoperative identification and early repair reduces postoperative morbidity and may obviate the need for additional procedures or surgery. 1,2,4,17 –22,24 –26,28 Failure to detect a ureteral injury can result in prolonged hospitalization, catheterization time, and potentially the loss of renal function. 4,17
Some reported series did not fully describe the mechanism of ureteral injury or give the details of the surgical repair. 1,2 Most Clavien graded complications necessitated operative intervention with general anesthesia (IIIB) regardless of approach. 4,13,17,18 –20,24 No previous series had used an open TUU for definitive repair, and one patient in a robotic series was admitted for pain control and hydration, but never needed operative intervention. 26
Our consecutive case series contains data for five surgeons that are prospectively maintained with >80% follow-up consistent with level 2C evidence; outcomes research. 30 We could only compare ureteral injury incidence with available literature and hypothesized the mechanisms of ureteral injury in the first two patients without confirming when the ureter was actually transected during prostatectomy. We were able to confirm injury on video review for our third patient.
One of the technical innovations that we have conceived during robot-assisted prostatectomy is the placement of a percutaneous suprapubic cystostomy for urinary drainage. The reason we have changed our technique from a traditional urethral Foley catheter is primarily because of patient preference. In our experience, patients perceive less postoperative penile discomfort while the necessity for anticholinergic medication is abated when using the percutaneous suprapubic cystostomy. Furthermore, long-term complication rates for those receiving a percutaneous suprapubic cystostomy have been minimal; at 24 months, only 15 of 339 patients had a procedure-specific complication. Thirteen were minor complications, Clavien I–II (3.8%) and two major complications, Clavien III–IV (0.6%). Continence rates remained the same or were favorable in comparison with other groups receiving a traditional urethral Foley catheter. 31,32
Conclusion
We found a 0.046% rate of ureteral injury during robot-assisted prostatectomy. This compares favorably with other published data for radical prostatectomy. Risk factors that may contribute to ureteral injury include: Previous pelvic surgeries, prostate resection, renal transplant, need for extensive adhesiolysis, previous pelvic irradiation (salvage treatment), difficult posterior dissection, enlarged glands and median lobes.
Patients with these risk factors should be considered higher risk for ureteral injury, and care should be taken to identify the course of the ureters and the location of the ureteral orifices during prostatectomy and pelvic lymphadenectomy. At the surgeon's discretion, ureteral catheterization or Double-J stent placement can be performed preoperatively or intraoperatively to facilitate identification of the ureters. Prompt identification and repair of ureteral injury will reduce morbidity and obviate the need for future readmissions or operative interventions.
Footnotes
Acknowledgment
We thank Michele Nowitzke, CPC.
Disclosure Statement
No competing financial interests exist.
