REVIEW URRENT C OPINION
Ureteral strictures and reconstruction in the cancer survivor Jordan Siegel a, Jay Simhan b, Timothy J. Tausch b, and Allen F. Morey b
Purpose of review Ureteral stricture disease commonly affects the cancer patients. This report will review the recent literature regarding both the causes and treatment options currently available for the cancer patients with ureteral obstruction. Recent findings Open ureteral reconstruction continues to have durable long-term results, whereas robotic approaches to repair have also demonstrated technical feasibility with equivalent short-term outcomes. Summary Stricture formation in the distal ureter is a common consequence of treatment for patients with pelvic malignancies. In experienced hands, minimally invasive approaches to ureteral reconstruction have proven to be feasible with short-term outcomes that are equivalent to more traditional, open techniques. Additionally, laparoscopic or robotic surgeries offer added benefits of earlier convalescence, decreased blood loss, as well as decreased pain. Nevertheless, open ureteral repair remains a viable option with durable long-term outcomes. Keywords postcancer surgery, ureteral reconstruction, ureteral stricture, ureteroneocystostomy
INTRODUCTION Ureteral obstruction as a result of malignancy can be caused by both extramural and intramural sources. The former is commonly because of an infiltrating malignancy or from mass effect, whereas the latter is often observed as a result of curative therapy. In this article, we will address the ureteral strictures resulting from definitive cancer treatment, review the cause of ureteral strictures in the cancer survivor, and discuss a variety of management options for ureteral obstruction. Lastly, we will discuss the effects of treatment or nontreatment of ureteral obstruction on the quality of life (QOL) of cancer patients.
Like surgery, radiation may have deleterious effects on the ureters [1] because of well described microvascular effects and progressive obliterative endarteritis leading to tissue necrosis [2,3]. Distal ureteral involvement occurs in 92% of iatrogenic injuries [4], with gynecologic procedures accounting for a large portion of these events. Some reports further indicate that up to 75% of distal ureteral injuries are caused during gynecologic procedures, with radical hysterectomy being the most common resulting in injury [5–7]. Additionally, the wide dissemination of minimally invasive gynecologic techniques has potentially made ureteral injury more common in contemporary practice [8,9]. In contrast, colorectal procedures have been
CAUSE OF URETERAL INJURY The location and extent of ureteral injuries vary based on the type of malignancy as well as the treatment modality. Given its location and anatomical relationship to the adjacent structures in the pelvis, the distal ureter is particularly susceptible to iatrogenic injury either during extirpative cancer surgery of the pelvis or in patients undergoing radiation treatment. Radiation therapy may also cause ureteral damage that arises months to years following initial treatment.
a Department of Urology, UC Irvine Medical Center, Orange, California and bDepartment of Urology, UT Southwestern Medical Center, Dallas, Texas, USA
Correspondence to Jordan Siegel, MD, Department of Urology, UC Irvine Medical Center, 333 City Boulevard West, Suite 2100, Orange, CA 92868, USA. Tel: +1 714 456 6719; fax: +1 714 456 5062; e-mail: [email protected] Curr Opin Urol 2014, 24:421–426 DOI:10.1097/MOU.0000000000000067
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KEY POINTS Distal ureteral stricture is commonly the result of cancer treatment for gynecologic, colorectal, and urologic malignancy. Recent literature shows durable success utilizing open techniques for all stricture lengths and location. Robotic reconstruction has demonstrated equivalent outcomes to open repair in short follow-up. Tissue-engineered ureteral segments may provide options for large-segment substitution in the future.
shown to result in ureteral injury less often (0.2–7.6% of cases) [10]. Accounting for 11% of iatrogenic injuries, urologic procedures may also cause ureteral damage, with the majority of insults arising because of endoscopic procedures [4]. A recent review of a large prostatectomy cohort demonstrated a low but significant incidence of ureteral injury during open, laparoscopic, and robotic prostatectomy (1–2%) [11]. Alternatively, panurethral stricture development is a known complication of endoscopic management for low-grade urothelial carcinoma and has been reported to occur in 8.6% of cases [12]. Strictures in these settings pose complex management scenarios, as the reconstruction effort must result in ureteral patency as well as an oncologically sound resection. Isolated ureteral injury during retroperitoneal lymph node dissection for testicular malignancy remains a rare finding [13], as often there is tumor involvement of the renal hilum, thus necessitating nephrectomy. In contrast to the lower ureter, stricture of the upper ureter occurs uncommonly as a result of cancer treatment, representing only 2% of iatrogenic injuries overall [4]. Most often, surgical therapy for tumors of the retroperitoneum may put the upper ureter at risk for injury. In the case of renal cell carcinoma, ureteral injury via partial nephrectomy is rare [14,15], though patients with large tumors of the mid and lower pole face the highest risk of this uncommon complication. Likewise, ablative techniques and radiofrequency ablation (RFA) have been shown to cause thermal injuryinduced ureteral strictures when employed on tumors adjacent to the ureter [16].
INITIAL MANAGEMENT AND QUALITY OF LIFE Delayed relief of ureteral obstruction has been shown to have a multitude of deleterious health 422
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effects, including risks of infection, stone formation, renal deterioration, and development or worsening of hypertension [17]. For this reason, initial management of urinary obstruction often involves drainage of the affected collecting system with an indwelling ureteral stent or percutaneous nephrostomy. Although these measures are temporary interventions prior to formal repair, they have nevertheless been shown to have a detrimental impact on the patient’s QOL [18–20]. Nevertheless, serial stents and nephrostomy tubes have become a definitive means for chronic management in select patients with competing medical risks who are not healthy enough to undergo formal reconstruction. There is a paucity of reports that investigate the QOL of the cancer patient who develops ureteral obstruction. In one of the few reports that address this important issue, Einstein et al. [21 ] reported strikingly poor QOL in a small cohort of cervical cancer patients with ureteral obstruction. The investigators also demonstrated a large discrepancy between physician’s perception of patient’s QOL and actual QOL score, highlighting the notion that providers often assume higher QOL scores for cancer survivors. As such, recognition of poor QOL is imperative, and prompt referral for the treatment of ureteral strictures is often encouraged as the negative impact of ureteral obstruction is significant on these patients. Additionally, there appears to be no surgical benefit to delaying reconstruction in uninfected individuals as operative outcomes in patients undergoing early ureteral repair are equivalent to those undergoing delayed intervention [22]. &
OPEN URETERAL RECONSTRUCTION There are various techniques that are available to the urologist for reconstruction of the strictured ureter. A properly reconstructed ureter necessitates the creation of a tension-free, watertight anastomosis using absorbable sutures with widely spatulated ends [23,24]. Some surgeons strongly advocate for maintaining continuity of the urothelium (i.e. avoiding intestinal interposition) as the preferred technique in ureteral reconstruction [25–27]. As the vascular supply of the ureter runs longitudinally in periadventitial tissue, dissection of nondiseased portions of the ureter should be minimized to avoid disruption. Nevertheless, complete excision of the diseased portions of ureter is paramount to prevent recurrent strictures [28]. A full description of all open ureteral reconstructive procedures is beyond the scope of this review; however, we have previously reported the details of our techniques for ureteral reimplantation in complex cases encountered at our institution [29 ]. &&
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Ureteroneocystostomy, psoas hitch, and Boari flap Distal ureteral strictures have traditionally been managed with ureteroneocystostomy with psoas hitch and Boari flap in order to achieve a tensionfree repair over a large distance (Figs. 1 and 2). Recent long-term data from Benson and colleagues of 100 distal ureteral repairs (including 58 psoas hitch and 18 Boari flaps) demonstrated durable resolution of hydronephrosis in 81% of patients with a median follow-up of 48.7 months [30]. Notably, the authors identified the elderly and patients with chronic ureteral obstruction as those more likely to have progressive renal deterioration. A similar report from Italy described a long-term experience with ureteral reimplantation and psoas hitch in 24 patients with a mean follow-up of 53 months [31]. Utilizing an antirefluxing technique for ureteral reimplantation, the study investigators noted successful repair (defined as ‘normal renal imaging’) in 91.6% of patients with strictures up to 10 cm in length. Though normally used for mid and distal ureteral repairs, promising results utilizing a spiral
bladder flap for proximal ureteral strictures have been reported by small, single-institution series [32]. In a Chinese study with a mean follow-up of 4 years, study investigators reported six patients with a mean stricture length of 22.5 cm who underwent successful reconstruction with spiral bladder flaps. Though preoperative bladder volumes or postoperative bladder capacity was not assessed, the reported findings are promising. We have also recently reported favorable results with downward nephropexy and Boari flap reconstruction in patients with proximal ureteral strictures [33]. Our institutional report highlights the notion that downward nephropexy could be used as an adjunctive maneuver that helps bridge long gaps at the time of repair.
Interposed bowel segments In rare cases when the ureteral defect is too long for reconstruction with urothelial tissue, or in patients who have poor bladder capacity or function, the surgeon can interpose bowel segments to achieve continuity. Ileal ureter creation is the most common method for ureteral substitution with these strictures, with proven durable outcomes (Fig. 3) [34]. Reconfigured bowel segments offer yet another alternative. Lazica et al. [35] report on their experience using reconfigured colon in 14 patients with a median follow-up of 52.4 months. The investigators were able to reconstruct defects up to 18 cm in length with double-colon segments for a combined length of 7 cm. Furthermore, they did not experience any deleterious effects of intestinal reabsorption, potentially because of less mucosal surface area when compared to the traditional ileal ureter.
LAPAROSCOPIC AND ROBOTIC RECONSTRUCTIVE TECHNIQUES
FIGURE 1. Postoperative cystogram of a patient who underwent a distal ureterectomy and ureteroneocystostomy with psoas hitch for an iatrogenic distal ureteral stricture following radical hysterectomy.
Laparoscopy has been used for ureteral reconstruction since the early 1990s [36,37]. More recently, laparoscopy has given way to robotic techniques as the primary platform for the minimally invasive ureteral surgeon. Potential advantages of laparoscopy and robotics include early convalescence, decreased postoperative pain, and decreased blood loss, with the additional advantage of robotic threedimensional imaging and seven degrees of instrument articulation. Robotics has revolutionized the complex minimally invasive ureteral repair, as anastomotic suturing is made significantly more facile by the instrumentation capabilities. The same surgical principles of open ureteral reconstruction apply to laparoscopic and robotic techniques and remain paramount: creation of a tension-free, watertight anastomosis of healthy
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FIGURE 2. (a) Antegrade nephrostogram of a 21-year-old patient with a right ureteral injury at the time of abdominal desmoid tumor resection. Contrast tapering of the proximal ureter is noted. The patient ultimately underwent successful repair through a right ureteral reimplantation with Boari flap and psoas hitch (b).
ureter with good mucosal apposition [23–27]. The surgeon must use caution, however, as minimally invasive techniques rely on the stricture length and location to plan appropriate patient positioning and port placement. This notion is highlighted in a recent publication describing robotic distal ureteral reconstruction [38 ]. Reports comparing open vs. robotic ureteral reconstruction are sparse, though Kozinn et al. [39] attempted this comparison via a matched cohort study. When analyzing 10 robotic and 24 open cases, blood loss (30.6 vs. 327.5 ml) and hospital stay (2.4 vs. 5.1 days) statistically favored the robot, and robotic cases only averaged an additional 36 min of operative time. Outcomes for both cohorts were good with no evidence of recurrent disease at follow-up of 30 and 24 months for open and robotic cases, respectively. In a similar comparison, Isac et al. [40] analyzed the outcomes for ureteroneocystostomy performed robotically in 24 patients and open in 41 patients, and reported nearly equivalent success rates (92.4 vs. 90.3%) with less blood loss and shorter hospital stays in the robotic group. However, not all reports favor robotic over laparoscopic approaches. Baldie et al. [41] compared the outcomes of 16 robotic and six laparoscopic cases, concluding equivalency based on the operative &&
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times, blood loss, hospital stay, and recurrence rates at a mean of 6.4 months’ follow-up. It is important to note that open conversion was required in two robotic cases and one laparoscopic case in order to complete the reconstruction. The findings, however, must be considered in the context of a small sample size in the laparoscopic arm. Eun and colleagues reported a contemporary single-surgeon experience utilizing the robot for strictures of the upper, mid, and distal ureter, all managed via ureteroureterostomy [42]. This study is notable for its successful (seven out of seven patients recurrence free at follow-up between 3 and 36 months) use of ureteroureterostomy in the distal ureter (stricture located >2 cm from the bladder), a clinical scenario that is traditionally managed by ureteroneocystostomy. Moreover, the importance of correct port placement is highlighted with multiple configurations described based on the location of the strictured segment. More complex techniques are being undertaken via a robotic approach as demonstrated by a recent study from Stolzenberg and colleagues [43]. The investigators demonstrated successful robotic ureteral reimplantation with Boari flap creation in a group of eight patients with distal ureteral stricture. Though this technique has been previously reported Volume 24 Number 4 July 2014
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FIGURE 3. (a) Antegrade nephrostogram of a 45-year-old woman who sustained a distal mid-ureteral injury during a gynecologic procedure. A poor bladder capacity (100 cc) precluded aggressive bladder mobilization to bridge the gap, and an ileal ureter interposition was created, demonstrating excellent postoperative results (b).
[44,45], this series is one of the largest, with excellent results at a minimum of 12 months’ follow-up. As with any new technological advances, the robotic literature is limited by low sample sizes, short follow-up, and biases inherent in the retrospective study methodology. Therefore, it is difficult to draw any wide-ranging and generalizable conclusions. However, it does appear that nearly all types of ureteral reconstruction are technically feasible robotically, with promising short-term outcomes. Longer term follow-up with prospective data in large series will provide a more reasonable comparison with outcomes from open series.
EXPERIMENTAL GRAFT AND TISSUE The search for viable graft material for ureteral reconstruction parallels urethral reconstruction. It is, therefore, not surprising that drawing on excellent results obtained with oral mucosal graft urethroplasty, several case series of oral mucosal graft ureteroplasty have been reported [46–48]. As they are free grafts, oral mucosal grafts are typically supported with omental wraps to provide a vascular supply. More research and longer term follow-up are needed to validate this innovative approach.
Tissue-engineered ureteral grafts have also been investigated as a potential autologous source of tissue for reconstruction [49–51]. In general, the two subtypes for such grafts include acellular and cellular grafts. The former are simply biologic scaffolding that when implanted relies on the body to populate the graft with appropriate cell types. Alternatively, cellular grafts are created by seeding biologic scaffolding with urothelial and smooth muscle cells in vitro and then subsequently implanting this complex in vivo. Biopsies of the implanted grafts have demonstrated similar histologic architecture to native ureteral tissues. Although these are promising options for the future, more research is necessary before widespread dissemination of this technology.
CONCLUSION Ureteral strictures can significantly impact a patient’s QOL following cancer treatment. Ureteral injuries in the cancer patient pose a challenging clinical scenario with various locations, length, and severity that all factor into the ultimate reconstructive technique. Innovative robotic procedures are increasingly adopted in lieu of open surgery. The myriad of treatment options and surgical
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approaches highlight the importance of surgeon’s experience in selecting the appropriate technique that can best restore a patient’s urinary tract anatomy. Acknowledgements None. Conflicts of interest There are no conflicts of interest.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Sewell JM, Rao A, Elliott SP. Validating a claims-based method for assessing severe rectal and urinary adverse effects of radiotherapy. Urology 2013; 82:335–340. 2. Hall EJ, Astor M, Bedford J, et al. Basic radiobiology. Am J Clin Oncol 1988; 11:220–252. 3. Turina M, Mulhall AM, Mahid AA, et al. Frequency and surgical management of chronic complications related to pelvic radiation. Arch Surg 2008; 143:46– 52; discussion 52. 4. Abboudi H, Ahmed K, Royle J, et al. Ureteric injury: a challenging condition to diagnose and manage. Nat Rev Urol 2013; 10:108–115. 5. Hwang JH, Lim MC, Joung JY, et al. Urologic complications of laparoscopic radical hysterectomy and lymphadenectomy. Int Urogynecol J 2012; 23:1605–1611. 6. Lee JS, Choe JH, Lee HS, Seo JT. Urologic complications following obstetric and gynecologic surgery. Korean J Urol 2012; 53:795–799. 7. Hwang JH. Urologic complication in laparoscopic radical hysterectomy: metaanalysis of 20 studies. Eur J Cancer 2012; 48:3177–3185. 8. Harkki-Siren P, Sjoberg J, Titinen A. Urinary tract injuries after hysterectomy. Obstet Gynecol 1998; 92:113–118. 9. Gilmour DT, Das S, Flowerdew G. Rates of urinary tract injury from gynecologic surgery and the role of intraoperative cystoscopy. Obstet Gynecol 2006; 107:1366–1372. 10. Da Silva G, Boutros M, Wexner SD. Role of prophylactic ureteric stents in colorectal surgery. Asian J Endosc Surg 2012; 5:105–110. 11. Tewari A, Sooriakumaran P, Bloch DA, et al. Positive surgical margin and perioperative complication rates of primary surgical treatments for prostate cancer: a systematic review and meta-analysis comparing retropubic, laparoscopic, and robotic prostatectomy. Eur Urol 2012; 62:1–15. 12. Chen GL, Bagley DH. Ureteroscopic surgery for upper tract transitional-cell carcinoma: complications and management. J Endourol 2001; 15:399–404. 13. Djaladat H, Nichols C, Daneshmand S. Adjuvant surgery in testicular cancer patients undergoing postchemotherapy retroperitoneal lymph node dissection. Ann Surg Oncol 2012; 19:2388–2393. 14. MacLennan S, Imamura M, Lapitan MC, et al. Systemic review of perioperative and quality of life outcomes following surgical management of localized renal cancer. Eur Urol 2012; 62:1097–1117. 15. Reyes JM, Carter DJ, Sirohi M, et al. Delayed proximal ureteric stricture formation after complex partial nephrectomy. BJU Int 2011; 109:539–543. 16. Cantwell CP, Wah TM, Gervais DA, et al. Protecting the ureter during radiofrequency ablation of renal cell cancer: a pilot study of retrograde pyeloperfusion with cooled dextrose 5% in water. J Vasc Interv Radiol 2008; 19:1034–1040. 17. Lucarelli G, Ditonno P, Bettocchi C, et al. Delayed relief of ureteral obstruction is implicated in the long-term development of renal damage and arterial hypertension in patients with unilateral ureteral injury. J Urol 2012; 189:960–965. 18. Joshi HB, Newns N, Stainthorpe A, et al. Ureteral stent symptom questionnaire: development and validation of a multidimensional quality of life measure. J Urol 2003; 169:1060–1064. 19. Monsky WL, Molloy C, Jin B, et al. Quality of life assessment after palliative interventions to manage malignant ureteral obstruction. Cardiovasc Intervent Radiol 2013; 36:1355–1363. 20. Izumi K, Mizokami A, Maeda Y, et al. Current outcomes of patients with ureteral stents for the management of malignant ureteral obstruction. J Urol 2011; 185:556–561. 21. Einstein MH, Rah JK, Chappell RJ, et al. Quality of life in cervical cancer & survivors: patient and provider perspectives on common complications of cervical cancer and treatment. Gynecol Oncol 2012; 125:163–167. The authors focus on the impact of complications on the quality of life of the cancer survivor, with particular interest in the divergence in the patient’s and physician’s perceptions of that impact.
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22. Li J, Chen Z, Zhu Q, et al. Early repair of pelvic and abdominal nonurological surgery-induced iatrogenic ureteral injuries in three distinct waiting-for-repair time periods. Am Surg 2012; 78:1270–1275. 23. Austin JC. Approaches to reconstruction of the ureter. J Urol 2010; 184:825–826. 24. Brandes S, Coburn M, Armenakas N, et al. Diagnosis and management of ureteric injury: an evidence-based analysis. BJU Int 2004; 94:277– 289. 25. Passerini-Glazel G, Meneghini A, Aragona F, et al. Technical options in complex ureteral lesions: ‘ureter-sparing’ surgery. Eur Urol 1994; 25:273– 280. 26. Hensle TW, Burbige KA, Levin RK. Management of the short ureter in urinary tract reconstruction. J Urol 1987; 137:707–711. 27. Tanagho EA. A case against incorporation of bowel segments into the closed urinary system. J Urol 1975; 113:796–802. 28. Png JC, Chapple CR. Principles of ureteric reconstruction. Curr Opin Urol 2000; 10:207–212. 29. Knight RB, Hudak SJ, Morey AF. Strategies for open reconstruction of upper && ureteral strictures. Urol Clin N Am 2013; 40:351–361. A comprehensive review of the open techniques to the management of upper ureteral strictures, with detailed descriptions of the steps and guiding principles. 30. Wenske S, Olsson CA, Benson MC. Outcomes of distal ureteral reconstruction through reimplantation with psoas hitch, Boari flap, or ureteroneocystostomy for benign or malignant ureteral obstruction or injury. Urology 2013; 82:231–236. 31. Manassero F, Mogorovich A, Fiorini G, et al. Ureteral reimplantation with psoas hitch in adults: a contemporary series with long-term follow up. Sci World J 2012; 2012:1–4. 32. Li Y, Yang S, Zhang X, et al. Curative effect analysis of spiral pedunculated bladder muscle flap in repairing long segment ureteral defects. Chin Med J 2013; 126:2580–2581. 33. Mauck RJ, Hudak SJ, Terlecki RP, Morey AF. Central role of Boari bladder flap and downward nephropexy in upper ureteral reconstruction. J Urol 2011; 186:1345–1349. 34. Armatys SA, Mellon MJ, Beck SDW, et al. Use of ileum as ureteral replacement in urological reconstruction. J Urol 2009; 181:177–181. 35. Lazica DA, Ubrig B, Brandt AS, et al. Ureteral substitution with reconfigured colon: long-term follow up. J Urol 2012; 187:542–548. 36. Nezhat C, Nezhat F, Green B, et al. Laparoscopic treatment of obstructed ureter due to endometriosis by resection and ureteroureterostomy: a case report. J Urol 1992; 148:865–868. 37. Ehrlich RM, Gershman A. Laparoscopic seromyotomy (auto-augmentation) for nonneurogenic neurogenic bladder in a child: initial case report. Urology 1993; 42:175–178; The initial report of laparoscopic ureteral reimplant. 38. Windsperger AP, Duchene DA. Robotic reconstruction of lower ureteral && strictures. Urol Clin N Am 2013; 40:363–370. A thorough description of the technique employed for the robotic management of distal ureteral strictures. 39. Kozinn SI, Canes D, Sorcini A, Moinzadeh A. Robotic versus open distal ureteral reconstruction and reimplantation for benign stricture disease. J Endourol 2012; 26:147–151. 40. Isac W, Kaouk J, Altunrende F, et al. Robot-assisted ureteroneocystostomy: technique and comparative outcomes. J Endourol 2013; 27:318–323. 41. Baldie K, Angell J, Ogan K, et al. Robotic management of benign mid and distal ureteral strictures and comparison with laparoscopic approaches at a single institution. Urology 2012; 80:596–601. 42. Lee Z, Llukai E, Reilly C, et al. Single surgeon experience with robot-assisted ureteroureterostomy for pathologies at the proximal, middle, and distal ureter in adults. J Endourol 2013; 27:994–999. 43. Do M, Kallindonis P, Qazi H, et al. Robotic-assisted technique for Boari flap ureteral reimplantation: is the robotic-assistance beneficial? J Endourol 2014; 1–7. [Epub ahead of print] 44. Musch M, Hohenhorst L, Pailliart A, et al. Robotic-assisted reconstructive surgery of the distal ureter: single institution experience in 16 patients. BJU Int 2013; 111:773–783. 45. Schimpf MO, Wagner JR. Robotic-assisted laparoscopic Boari flap ureteral reimplantation. J Endourol 2008; 22:2691–2694. 46. Sadhu S, Pandit K, Roy MK, et al. Buccal mucosa ureteroplasty for the treatment of complex ureteric injury. Indian J Surg 2011; 73:71–72. 47. Kroepfl D, Loewen H, Klevecka V, et al. Treatment of long ureteric strictures with buccal mucosal grafts. BJU Int 2010; 105:1452–1455. 48. Badawy AA, Abolyosr A, Saleem MD, et al. Buccal mucosa graft for ureteral stricture substitution: initial experience. Urology 2010; 76:971– 975. 49. Atala A, Vacanti JP, Peters CA, et al. Formation of urothelial structures in vivo from dissociated cells attached to biodegradable polymer scaffolds in vitro. J Urol 1992; 148:658–662. 50. Shi J-G, Fu J-W, Wang X-X, et al. Tissue engineering of ureteral grafts by seeding urothelial differentiated HADSCs onto biodegradable ureteral scaffolds. J Biomed Mater Res 2012; 100A:2612–2622. 51. Liao W, Yang S, Song C, et al. Construction of ureteral grafts by seeding bone marrow mesenchymal stem cells and smooth muscle cells into bladder acellular matrix. Transplant Proc 2013; 45:730–734.
Volume 24 Number 4 July 2014
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Ureteral strictures and reconstruction in the cancer survivor Jordan Siegel a, Jay Simhan b, Timothy J. Tausch b, and Allen F. Morey b
Purpose of review Ureteral stricture disease commonly affects the cancer patients. This report will review the recent literature regarding both the causes and treatment options currently available for the cancer patients with ureteral obstruction. Recent findings Open ureteral reconstruction continues to have durable long-term results, whereas robotic approaches to repair have also demonstrated technical feasibility with equivalent short-term outcomes. Summary Stricture formation in the distal ureter is a common consequence of treatment for patients with pelvic malignancies. In experienced hands, minimally invasive approaches to ureteral reconstruction have proven to be feasible with short-term outcomes that are equivalent to more traditional, open techniques. Additionally, laparoscopic or robotic surgeries offer added benefits of earlier convalescence, decreased blood loss, as well as decreased pain. Nevertheless, open ureteral repair remains a viable option with durable long-term outcomes. Keywords postcancer surgery, ureteral reconstruction, ureteral stricture, ureteroneocystostomy
INTRODUCTION Ureteral obstruction as a result of malignancy can be caused by both extramural and intramural sources. The former is commonly because of an infiltrating malignancy or from mass effect, whereas the latter is often observed as a result of curative therapy. In this article, we will address the ureteral strictures resulting from definitive cancer treatment, review the cause of ureteral strictures in the cancer survivor, and discuss a variety of management options for ureteral obstruction. Lastly, we will discuss the effects of treatment or nontreatment of ureteral obstruction on the quality of life (QOL) of cancer patients.
Like surgery, radiation may have deleterious effects on the ureters [1] because of well described microvascular effects and progressive obliterative endarteritis leading to tissue necrosis [2,3]. Distal ureteral involvement occurs in 92% of iatrogenic injuries [4], with gynecologic procedures accounting for a large portion of these events. Some reports further indicate that up to 75% of distal ureteral injuries are caused during gynecologic procedures, with radical hysterectomy being the most common resulting in injury [5–7]. Additionally, the wide dissemination of minimally invasive gynecologic techniques has potentially made ureteral injury more common in contemporary practice [8,9]. In contrast, colorectal procedures have been
CAUSE OF URETERAL INJURY The location and extent of ureteral injuries vary based on the type of malignancy as well as the treatment modality. Given its location and anatomical relationship to the adjacent structures in the pelvis, the distal ureter is particularly susceptible to iatrogenic injury either during extirpative cancer surgery of the pelvis or in patients undergoing radiation treatment. Radiation therapy may also cause ureteral damage that arises months to years following initial treatment.
a Department of Urology, UC Irvine Medical Center, Orange, California and bDepartment of Urology, UT Southwestern Medical Center, Dallas, Texas, USA
Correspondence to Jordan Siegel, MD, Department of Urology, UC Irvine Medical Center, 333 City Boulevard West, Suite 2100, Orange, CA 92868, USA. Tel: +1 714 456 6719; fax: +1 714 456 5062; e-mail: [email protected] Curr Opin Urol 2014, 24:421–426 DOI:10.1097/MOU.0000000000000067
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Reconstructive urology and the cancer survivor
KEY POINTS Distal ureteral stricture is commonly the result of cancer treatment for gynecologic, colorectal, and urologic malignancy. Recent literature shows durable success utilizing open techniques for all stricture lengths and location. Robotic reconstruction has demonstrated equivalent outcomes to open repair in short follow-up. Tissue-engineered ureteral segments may provide options for large-segment substitution in the future.
shown to result in ureteral injury less often (0.2–7.6% of cases) [10]. Accounting for 11% of iatrogenic injuries, urologic procedures may also cause ureteral damage, with the majority of insults arising because of endoscopic procedures [4]. A recent review of a large prostatectomy cohort demonstrated a low but significant incidence of ureteral injury during open, laparoscopic, and robotic prostatectomy (1–2%) [11]. Alternatively, panurethral stricture development is a known complication of endoscopic management for low-grade urothelial carcinoma and has been reported to occur in 8.6% of cases [12]. Strictures in these settings pose complex management scenarios, as the reconstruction effort must result in ureteral patency as well as an oncologically sound resection. Isolated ureteral injury during retroperitoneal lymph node dissection for testicular malignancy remains a rare finding [13], as often there is tumor involvement of the renal hilum, thus necessitating nephrectomy. In contrast to the lower ureter, stricture of the upper ureter occurs uncommonly as a result of cancer treatment, representing only 2% of iatrogenic injuries overall [4]. Most often, surgical therapy for tumors of the retroperitoneum may put the upper ureter at risk for injury. In the case of renal cell carcinoma, ureteral injury via partial nephrectomy is rare [14,15], though patients with large tumors of the mid and lower pole face the highest risk of this uncommon complication. Likewise, ablative techniques and radiofrequency ablation (RFA) have been shown to cause thermal injuryinduced ureteral strictures when employed on tumors adjacent to the ureter [16].
INITIAL MANAGEMENT AND QUALITY OF LIFE Delayed relief of ureteral obstruction has been shown to have a multitude of deleterious health 422
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effects, including risks of infection, stone formation, renal deterioration, and development or worsening of hypertension [17]. For this reason, initial management of urinary obstruction often involves drainage of the affected collecting system with an indwelling ureteral stent or percutaneous nephrostomy. Although these measures are temporary interventions prior to formal repair, they have nevertheless been shown to have a detrimental impact on the patient’s QOL [18–20]. Nevertheless, serial stents and nephrostomy tubes have become a definitive means for chronic management in select patients with competing medical risks who are not healthy enough to undergo formal reconstruction. There is a paucity of reports that investigate the QOL of the cancer patient who develops ureteral obstruction. In one of the few reports that address this important issue, Einstein et al. [21 ] reported strikingly poor QOL in a small cohort of cervical cancer patients with ureteral obstruction. The investigators also demonstrated a large discrepancy between physician’s perception of patient’s QOL and actual QOL score, highlighting the notion that providers often assume higher QOL scores for cancer survivors. As such, recognition of poor QOL is imperative, and prompt referral for the treatment of ureteral strictures is often encouraged as the negative impact of ureteral obstruction is significant on these patients. Additionally, there appears to be no surgical benefit to delaying reconstruction in uninfected individuals as operative outcomes in patients undergoing early ureteral repair are equivalent to those undergoing delayed intervention [22]. &
OPEN URETERAL RECONSTRUCTION There are various techniques that are available to the urologist for reconstruction of the strictured ureter. A properly reconstructed ureter necessitates the creation of a tension-free, watertight anastomosis using absorbable sutures with widely spatulated ends [23,24]. Some surgeons strongly advocate for maintaining continuity of the urothelium (i.e. avoiding intestinal interposition) as the preferred technique in ureteral reconstruction [25–27]. As the vascular supply of the ureter runs longitudinally in periadventitial tissue, dissection of nondiseased portions of the ureter should be minimized to avoid disruption. Nevertheless, complete excision of the diseased portions of ureter is paramount to prevent recurrent strictures [28]. A full description of all open ureteral reconstructive procedures is beyond the scope of this review; however, we have previously reported the details of our techniques for ureteral reimplantation in complex cases encountered at our institution [29 ]. &&
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Ureteral strictures and reconstruction Siegel et al.
Ureteroneocystostomy, psoas hitch, and Boari flap Distal ureteral strictures have traditionally been managed with ureteroneocystostomy with psoas hitch and Boari flap in order to achieve a tensionfree repair over a large distance (Figs. 1 and 2). Recent long-term data from Benson and colleagues of 100 distal ureteral repairs (including 58 psoas hitch and 18 Boari flaps) demonstrated durable resolution of hydronephrosis in 81% of patients with a median follow-up of 48.7 months [30]. Notably, the authors identified the elderly and patients with chronic ureteral obstruction as those more likely to have progressive renal deterioration. A similar report from Italy described a long-term experience with ureteral reimplantation and psoas hitch in 24 patients with a mean follow-up of 53 months [31]. Utilizing an antirefluxing technique for ureteral reimplantation, the study investigators noted successful repair (defined as ‘normal renal imaging’) in 91.6% of patients with strictures up to 10 cm in length. Though normally used for mid and distal ureteral repairs, promising results utilizing a spiral
bladder flap for proximal ureteral strictures have been reported by small, single-institution series [32]. In a Chinese study with a mean follow-up of 4 years, study investigators reported six patients with a mean stricture length of 22.5 cm who underwent successful reconstruction with spiral bladder flaps. Though preoperative bladder volumes or postoperative bladder capacity was not assessed, the reported findings are promising. We have also recently reported favorable results with downward nephropexy and Boari flap reconstruction in patients with proximal ureteral strictures [33]. Our institutional report highlights the notion that downward nephropexy could be used as an adjunctive maneuver that helps bridge long gaps at the time of repair.
Interposed bowel segments In rare cases when the ureteral defect is too long for reconstruction with urothelial tissue, or in patients who have poor bladder capacity or function, the surgeon can interpose bowel segments to achieve continuity. Ileal ureter creation is the most common method for ureteral substitution with these strictures, with proven durable outcomes (Fig. 3) [34]. Reconfigured bowel segments offer yet another alternative. Lazica et al. [35] report on their experience using reconfigured colon in 14 patients with a median follow-up of 52.4 months. The investigators were able to reconstruct defects up to 18 cm in length with double-colon segments for a combined length of 7 cm. Furthermore, they did not experience any deleterious effects of intestinal reabsorption, potentially because of less mucosal surface area when compared to the traditional ileal ureter.
LAPAROSCOPIC AND ROBOTIC RECONSTRUCTIVE TECHNIQUES
FIGURE 1. Postoperative cystogram of a patient who underwent a distal ureterectomy and ureteroneocystostomy with psoas hitch for an iatrogenic distal ureteral stricture following radical hysterectomy.
Laparoscopy has been used for ureteral reconstruction since the early 1990s [36,37]. More recently, laparoscopy has given way to robotic techniques as the primary platform for the minimally invasive ureteral surgeon. Potential advantages of laparoscopy and robotics include early convalescence, decreased postoperative pain, and decreased blood loss, with the additional advantage of robotic threedimensional imaging and seven degrees of instrument articulation. Robotics has revolutionized the complex minimally invasive ureteral repair, as anastomotic suturing is made significantly more facile by the instrumentation capabilities. The same surgical principles of open ureteral reconstruction apply to laparoscopic and robotic techniques and remain paramount: creation of a tension-free, watertight anastomosis of healthy
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FIGURE 2. (a) Antegrade nephrostogram of a 21-year-old patient with a right ureteral injury at the time of abdominal desmoid tumor resection. Contrast tapering of the proximal ureter is noted. The patient ultimately underwent successful repair through a right ureteral reimplantation with Boari flap and psoas hitch (b).
ureter with good mucosal apposition [23–27]. The surgeon must use caution, however, as minimally invasive techniques rely on the stricture length and location to plan appropriate patient positioning and port placement. This notion is highlighted in a recent publication describing robotic distal ureteral reconstruction [38 ]. Reports comparing open vs. robotic ureteral reconstruction are sparse, though Kozinn et al. [39] attempted this comparison via a matched cohort study. When analyzing 10 robotic and 24 open cases, blood loss (30.6 vs. 327.5 ml) and hospital stay (2.4 vs. 5.1 days) statistically favored the robot, and robotic cases only averaged an additional 36 min of operative time. Outcomes for both cohorts were good with no evidence of recurrent disease at follow-up of 30 and 24 months for open and robotic cases, respectively. In a similar comparison, Isac et al. [40] analyzed the outcomes for ureteroneocystostomy performed robotically in 24 patients and open in 41 patients, and reported nearly equivalent success rates (92.4 vs. 90.3%) with less blood loss and shorter hospital stays in the robotic group. However, not all reports favor robotic over laparoscopic approaches. Baldie et al. [41] compared the outcomes of 16 robotic and six laparoscopic cases, concluding equivalency based on the operative &&
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times, blood loss, hospital stay, and recurrence rates at a mean of 6.4 months’ follow-up. It is important to note that open conversion was required in two robotic cases and one laparoscopic case in order to complete the reconstruction. The findings, however, must be considered in the context of a small sample size in the laparoscopic arm. Eun and colleagues reported a contemporary single-surgeon experience utilizing the robot for strictures of the upper, mid, and distal ureter, all managed via ureteroureterostomy [42]. This study is notable for its successful (seven out of seven patients recurrence free at follow-up between 3 and 36 months) use of ureteroureterostomy in the distal ureter (stricture located >2 cm from the bladder), a clinical scenario that is traditionally managed by ureteroneocystostomy. Moreover, the importance of correct port placement is highlighted with multiple configurations described based on the location of the strictured segment. More complex techniques are being undertaken via a robotic approach as demonstrated by a recent study from Stolzenberg and colleagues [43]. The investigators demonstrated successful robotic ureteral reimplantation with Boari flap creation in a group of eight patients with distal ureteral stricture. Though this technique has been previously reported Volume 24 Number 4 July 2014
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FIGURE 3. (a) Antegrade nephrostogram of a 45-year-old woman who sustained a distal mid-ureteral injury during a gynecologic procedure. A poor bladder capacity (100 cc) precluded aggressive bladder mobilization to bridge the gap, and an ileal ureter interposition was created, demonstrating excellent postoperative results (b).
[44,45], this series is one of the largest, with excellent results at a minimum of 12 months’ follow-up. As with any new technological advances, the robotic literature is limited by low sample sizes, short follow-up, and biases inherent in the retrospective study methodology. Therefore, it is difficult to draw any wide-ranging and generalizable conclusions. However, it does appear that nearly all types of ureteral reconstruction are technically feasible robotically, with promising short-term outcomes. Longer term follow-up with prospective data in large series will provide a more reasonable comparison with outcomes from open series.
EXPERIMENTAL GRAFT AND TISSUE The search for viable graft material for ureteral reconstruction parallels urethral reconstruction. It is, therefore, not surprising that drawing on excellent results obtained with oral mucosal graft urethroplasty, several case series of oral mucosal graft ureteroplasty have been reported [46–48]. As they are free grafts, oral mucosal grafts are typically supported with omental wraps to provide a vascular supply. More research and longer term follow-up are needed to validate this innovative approach.
Tissue-engineered ureteral grafts have also been investigated as a potential autologous source of tissue for reconstruction [49–51]. In general, the two subtypes for such grafts include acellular and cellular grafts. The former are simply biologic scaffolding that when implanted relies on the body to populate the graft with appropriate cell types. Alternatively, cellular grafts are created by seeding biologic scaffolding with urothelial and smooth muscle cells in vitro and then subsequently implanting this complex in vivo. Biopsies of the implanted grafts have demonstrated similar histologic architecture to native ureteral tissues. Although these are promising options for the future, more research is necessary before widespread dissemination of this technology.
CONCLUSION Ureteral strictures can significantly impact a patient’s QOL following cancer treatment. Ureteral injuries in the cancer patient pose a challenging clinical scenario with various locations, length, and severity that all factor into the ultimate reconstructive technique. Innovative robotic procedures are increasingly adopted in lieu of open surgery. The myriad of treatment options and surgical
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approaches highlight the importance of surgeon’s experience in selecting the appropriate technique that can best restore a patient’s urinary tract anatomy. Acknowledgements None. Conflicts of interest There are no conflicts of interest.
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