Iatrogenic ureteral injuries, more than half of which occur during gynecologic surgery, may have devastating consequences for both patients and physicians. Gynecologists have employed various techniques such as cystoscopy, ureteral stents, and lighted ureteral stents to prevent ureteral injuries. The emergence and increasing prevalence of robotic surgery necessitates that we not only reevaluate the utility of these techniques, but also develop new ones specific for the robotic modality. In the robotic setting, the surgeon lacks tactile feedback and must rely primarily on visual cues. The use of intraureteral indocyanine green and subsequent visualization under near-infrared fluorescence appears to be a promising technique to primarily and secondarily prevent ureteral injuries during robotic gynecologic surgery.
Robotic surgery maintains the advantages inherent to minimally invasive surgery, and provides the surgeon with magnified 3-dimensional vision, improved ability to operate in limited anatomic spaces, and wristed instrumentation to enhance intracorporeal dexterity. These attributes make the robotic modality well suited for gynecologic surgeries, and the robotic platform is increasingly utilized for the operative management of benign and malignant gynecologic pathologies. The rate of robotic hysterectomies increased from 0.5% in 2007 to 9.5% in 2010 of all hysterectomies in the United States. In a 2015 survey of the members of the Society of Gynecologic Oncology, 97% of respondents performed robotic surgery compared to 29% of respondents in 2007.
Iatrogenic ureteral injuries, more than half of which occur during gynecologic surgery, have potentially devastating consequences for both patients and physicians. The rate of clinically apparent iatrogenic ureteral injuries during routine gynecologic pelvic operations ranges from 0.2-2.5%, and during radical procedures for malignant conditions ranges from 10-30%. Gynecologists have employed various techniques such as cystoscopy, ureteral stents, and lighted ureteral stents to prevent ureteral injuries. However, the emergence and increasing prevalence of robotic surgery necessitates that we not only reevaluate the utility of these techniques, but also develop new ones specific for the robotic modality. During robotic surgery, the surgeon lacks tactile feedback and must rely primarily on visual cues.
The purpose of our report is 2-fold: first, to review the major techniques used to prevent iatrogenic ureteral injuries and to assess their efficacy during robotic surgery; and second, to highlight the use of intraureteral indocyanine green (ICG) and subsequent visualization using near-infrared fluorescence (NIRF) to prevent iatrogenic ureteral injuries.
Background
Iatrogenic ureteral injuries have significant implications for both patients and physicians. Patients with ureteral injuries may develop urinomas, abscesses, fistulae, and permanent renal compromise. Management of such patients often requires prolonged ureteral catheterization and additional surgical intervention, which may increase hospital stay and require additional follow-up. Physicians responsible for unintended ureteral injury may experience significant personal and financial costs due to the high relative risk for litigation. Ureteral injury is the most common gynecologic surgery complication resulting in litigation, and accounts for 17% of nonobstetric legal action against gynecologists in the United States. To prevent these detrimental outcomes, the surgeon must take measures to primarily and secondarily prevent ureteral injuries.
Primary prevention refers to preventing a ureteral injury from occurring in the first place. Accurate identification of the ureters is the most vital step in prevention of iatrogenic ureteral injuries. A thorough understanding of ureteral anatomy, including its course and fragile blood supply, is essential and cannot be overemphasized. Neuman et al noted that accurate identification and dissection of the ureter during abdominal hysterectomy resulted in a 0.2-0.7% decrease in the rate of iatrogenic ureteral injuries. Risk factors that inhibit accurate identification of the ureters are the same as those associated with iatrogenic ureteral injuries. These risk factors include those that distort normal anatomy such as endometriosis, pelvic masses, and congenital anomalies; and those that cause periureteral fibrosis such as radiation, prior pelvic surgery, and pelvic inflammatory disease. As such, surgical techniques that assist the surgeon accurately identify the ureter are paramount.
Secondary prevention refers to recognizing a ureteral injury as early as possible so that it may be promptly repaired. Intraoperative diagnosis and immediate repair of ureteral injuries, compared to postoperative diagnosis and delayed repair, significantly reduces morbidity and improves outcomes. Failure to intraoperatively identify and fix a ureteral injury may result in additional diagnostic studies, hospital readmissions, and surgeries. Also, delayed recognition of ureteral injuries may require temporary urinary diversion via a percutaneous nephrostomy tube for months prior to definitive surgical repair. The reason for this is because postoperative tissue edema and inflammation make ureteral reconstruction difficult in the immediate postoperative period. For physicians, intraoperative diagnosis and immediate repair of ureteral injuries is associated with reduced medicolegal risks. A cost-analysis by Schimpf et al showed that the cost of an undiagnosed iatrogenic ureteral injury requiring readmission and delayed open repair was 1.72 times the cost of injuries repaired immediately. Despite this, 80-89% of ureteral injuries are diagnosed postoperatively. As such, surgical techniques that assist the surgeon intraoperatively detect ureteral injuries, and thus facilitate immediate repair, are imperative.
Intraoperative cystoscopy
Intraoperative cystoscopy involves inserting a cystoscope into the bladder to visualize the ureteral orifices to assess for hematuria, and/or the efflux of previously administered intravenous indigo carmine or methylene blue, or oral phenazopyridine. Intravenous furosemide may be administered to expedite the excretion of dye. The presence of bloody efflux or failure to see the dye suggests a ureteral injury. The technique is a means of secondary prevention against iatrogenic ureteral injuries. In a systematic review of studies from 1998 through 2004, Gilmour et al found that routine cystoscopy allowed for the detection of 88-100% of ureteral injuries during gynecologic surgery. The ureteral injury rate was found to be higher by as much as 5 times when routine cystoscopy was performed, compared to when it was not performed. Investigators utilizing intraoperative cystoscopy to identify ureteral injuries have noted the procedure to be safe and rarely associated with complications. In a report in which 251 patients underwent cystoscopy at time of hysterectomy, there were no complications resulting from cystoscopy. Another study of 224 patients undergoing cystoscopy at the time of urogynecologic reconstructive pelvic surgery revealed no association between cystoscopy and morbidity. The complication rate of cystoscopy is generally accepted to be extremely low. Potential complications include infection, temporary pain, hematuria, and urinary tract injury.
Although intraoperative cystoscopy has been shown to detect ureteral injuries with a high rate of success, a normal cystoscopy does not guarantee that there is no ureteral injury. Ureteral injuries that cause partial obstruction may be difficult to elicit with cystoscopy. Thermal damage to the ureter may take several days for the full extent of injury to develop, and may not be detectable with intraoperative cystoscopy. In addition, not all ureteral injuries are clinically significant and may resolve without medical intervention. For example, patients with an absorbable suture partially constricting a ureter but not affecting renal drainage could resolve once the suture reabsorbs. As such, the use of intraoperative cystoscopy may lead to overdiagnosis and subsequent overmanagement of ureteral injuries.
In a cost analysis, Visco et al found that routine cystoscopy was cost-saving at a threshold ureteral injury rate of 1.5% for abdominal hysterectomy and 2% for vaginal or laparoscopic vaginal hysterectomy. Although this may lead some surgeons to reserve intraoperative cystoscopy only for cases with a high risk of ureteral injury, the majority of iatrogenic ureteral injuries have been shown to occur during routine surgical procedures. As such, the decision to use intraoperative cystoscopy based solely on a surgeon’s estimated ureteral injury risk in a given case may be limited.
Only a few reports have investigated the role of intraoperative cystoscopy during robotic gynecologic surgery. Nguyen et al retrospectively compared the rate of lower urinary tract injuries after robotic oncologic gynecologic surgery between 2 academic medical centers in which one performed routine cystoscopy and the other did not. Among the 140 cases with no cystoscopy and 109 cases with routine cystoscopy, there were no ureteral and/or bladder injuries. Interestingly, the mean operative time for the routine cystoscopy group was shorter than that of the no cystoscopy group. The authors suggested that it is possible to efficiently incorporate routine cystoscopy into robotic oncologic gynecologic surgeries without significantly increasing operative time. Furthermore, given that iatrogenic lower urinary tract injuries are less commonly recognized intraoperatively during minimally invasive surgery the authors suggested that routine cystoscopy is a “worthy safeguard” during robotic oncologic gynecologic procedures.
Guidelines for the use of intraoperative cystoscopy to diagnose iatrogenic ureteral injuries during robotic gynecologic surgery have yet to be established. In a committee opinion, the American Congress of Obstetricians and Gynecologists advised that cystoscopy may be beneficial in procedures with a 1-2% risk for ureteral injuries. The group recommended intraoperative cystoscopy in difficult laparoscopic procedures, without specifically differentiating traditional laparoscopic from robotic surgery. In a practice guideline report, the American Association of Gynecologic Laparoscopists recommended that surgeons use intraoperative cystoscopy more liberally, and consider routine implementation of cystoscopy at the time of laparoscopic total hysterectomy. However, the level of evidence precluded a recommendation for making cystoscopy an integral component of laparoscopic hysterectomy. While intraoperative cystoscopy only allows for secondary prevention of ureteral injuries, the technique deserves further evaluation to determine its precise role during robotic gynecologic surgery given the well-documented implications for both patients and clinicians.
Intraoperative cystoscopy
Intraoperative cystoscopy involves inserting a cystoscope into the bladder to visualize the ureteral orifices to assess for hematuria, and/or the efflux of previously administered intravenous indigo carmine or methylene blue, or oral phenazopyridine. Intravenous furosemide may be administered to expedite the excretion of dye. The presence of bloody efflux or failure to see the dye suggests a ureteral injury. The technique is a means of secondary prevention against iatrogenic ureteral injuries. In a systematic review of studies from 1998 through 2004, Gilmour et al found that routine cystoscopy allowed for the detection of 88-100% of ureteral injuries during gynecologic surgery. The ureteral injury rate was found to be higher by as much as 5 times when routine cystoscopy was performed, compared to when it was not performed. Investigators utilizing intraoperative cystoscopy to identify ureteral injuries have noted the procedure to be safe and rarely associated with complications. In a report in which 251 patients underwent cystoscopy at time of hysterectomy, there were no complications resulting from cystoscopy. Another study of 224 patients undergoing cystoscopy at the time of urogynecologic reconstructive pelvic surgery revealed no association between cystoscopy and morbidity. The complication rate of cystoscopy is generally accepted to be extremely low. Potential complications include infection, temporary pain, hematuria, and urinary tract injury.
Although intraoperative cystoscopy has been shown to detect ureteral injuries with a high rate of success, a normal cystoscopy does not guarantee that there is no ureteral injury. Ureteral injuries that cause partial obstruction may be difficult to elicit with cystoscopy. Thermal damage to the ureter may take several days for the full extent of injury to develop, and may not be detectable with intraoperative cystoscopy. In addition, not all ureteral injuries are clinically significant and may resolve without medical intervention. For example, patients with an absorbable suture partially constricting a ureter but not affecting renal drainage could resolve once the suture reabsorbs. As such, the use of intraoperative cystoscopy may lead to overdiagnosis and subsequent overmanagement of ureteral injuries.
In a cost analysis, Visco et al found that routine cystoscopy was cost-saving at a threshold ureteral injury rate of 1.5% for abdominal hysterectomy and 2% for vaginal or laparoscopic vaginal hysterectomy. Although this may lead some surgeons to reserve intraoperative cystoscopy only for cases with a high risk of ureteral injury, the majority of iatrogenic ureteral injuries have been shown to occur during routine surgical procedures. As such, the decision to use intraoperative cystoscopy based solely on a surgeon’s estimated ureteral injury risk in a given case may be limited.
Only a few reports have investigated the role of intraoperative cystoscopy during robotic gynecologic surgery. Nguyen et al retrospectively compared the rate of lower urinary tract injuries after robotic oncologic gynecologic surgery between 2 academic medical centers in which one performed routine cystoscopy and the other did not. Among the 140 cases with no cystoscopy and 109 cases with routine cystoscopy, there were no ureteral and/or bladder injuries. Interestingly, the mean operative time for the routine cystoscopy group was shorter than that of the no cystoscopy group. The authors suggested that it is possible to efficiently incorporate routine cystoscopy into robotic oncologic gynecologic surgeries without significantly increasing operative time. Furthermore, given that iatrogenic lower urinary tract injuries are less commonly recognized intraoperatively during minimally invasive surgery the authors suggested that routine cystoscopy is a “worthy safeguard” during robotic oncologic gynecologic procedures.
Guidelines for the use of intraoperative cystoscopy to diagnose iatrogenic ureteral injuries during robotic gynecologic surgery have yet to be established. In a committee opinion, the American Congress of Obstetricians and Gynecologists advised that cystoscopy may be beneficial in procedures with a 1-2% risk for ureteral injuries. The group recommended intraoperative cystoscopy in difficult laparoscopic procedures, without specifically differentiating traditional laparoscopic from robotic surgery. In a practice guideline report, the American Association of Gynecologic Laparoscopists recommended that surgeons use intraoperative cystoscopy more liberally, and consider routine implementation of cystoscopy at the time of laparoscopic total hysterectomy. However, the level of evidence precluded a recommendation for making cystoscopy an integral component of laparoscopic hysterectomy. While intraoperative cystoscopy only allows for secondary prevention of ureteral injuries, the technique deserves further evaluation to determine its precise role during robotic gynecologic surgery given the well-documented implications for both patients and clinicians.
Preoperative ureteral stents
Preoperative ureteral stents involves cystoscopically placing open-ended ureteral catheters prior to the primary procedure. These catheters are generally removed at the conclusion of, or within a few days of, the operation. The technique is a means of primary and secondary prevention against iatrogenic ureteral injuries. With regards to primary prevention, ureteral stents may be palpated during open surgery to identify the ureters. This has been shown to be particularly beneficial in cases with periureteral inflammation or fibrosis where definitive identification of the ureters may be difficult. During minimally invasive surgeries, ureteral stents may straighten the course of the ureter and correct anatomic deviations to allow for easier identification. With regards to secondary prevention, full-thickness ureteral injuries are identified by visualization of the intraluminal stent. The majority of studies regarding the use of preoperative ureteral stents to prevent iatrogenic ureteral injuries are derived from the colorectal surgery literature, and the colorectal surgery experience supplements our understanding of this technique in gynecologic surgery.
Studies have shown that preoperative ureteral stents may be placed without significantly increasing operating room time. In a report by Abu-Rustum et al, 38 patients underwent ureteral catheterization prior to fertility-sparing radical trachelectomy for cervical cancer. Preoperative ureteral catheterization was noted to be a simple procedure that took 15-20 minutes to perform, and facilitated identification of the ureter in all cases. Tanaka et al retrospectively compared outcomes in patients who underwent laparoscopic hysterectomy with and without preoperative ureteral stents. One of 34 patients who did not receive preoperative ureteral stents, and 0 of 60 patients who received preoperative ureteral stents, experienced a ureteral injury. Furthermore, there was no significant difference in mean operating room time between the 2 cohorts, and the group with bilateral ureteral stents actually had shorter mean operating room times (168 vs 181 minutes, P = .18). The authors reasoned that the technique ultimately shortened operating room time by decreasing the time required to identify the ureter and its course.
Although the insertion of preoperative ureteral stents is generally considered to be safe, it may rarely lead to more serious complications such as reflux anuria. This is thought to occur when the insertion of ureteral stents leads to urothelial edema and subsequent ureteral obstruction after stent removal. Reflux anuria occurs in 0-7.6% of cases of bilateral preoperative ureteral stent placement, and may lead to acute kidney injury and electrolyte abnormalities. In severe cases, reflux anuria is managed with restenting of the ureters or temporary hemodialysis. Although investigators have recommended staged removal of ureteral catheters to prevent this complication, reflux anuria may still occur after stepwise catheter removal.
To our knowledge, there have been no studies evaluating the role of preoperative ureteral stenting in robotic gynecologic surgery. Presumably, the role of preoperative ureteral stents for primary prevention is significantly diminished in robotic gynecologic surgery compared to their role in open surgery due to the inability to palpate ureteral stents with robotic assistance. Although the aforementioned report by Tanaka et al noted that the ureteral stents straightened the ureteral course and allowed for easier identification during laparoscopic gynecologic surgery, the utility of this technique during robotic gynecologic surgery appears to be limited.
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