SURGICAL ACCESS FOR NEPHROURETERECTOMY. ONU can be performed with either one incision, via a transperitoneal approach,

. 2010 Laparoscopic and Robotic Urology SURGICAL TECHNIQUES FOR DISTAL URETER REMOVAL DURING NEPHROURETERECTOMY PHÉ ET AL. BJUI Does the surgical technique for management of the distal ureter influence the outcome after nephroureterectomy? Véronique Phé*, Olivier Cussenot, Marc-Olivier Bitker* and Morgan Rouprêt* *Academic Department of Urology of la Pitié-Salpêtrière Hospital, Assistance Publique-Hôpitaux de Paris, Faculté de Médecine Pierre et Marie Curie, University Paris VI, and Centre d Etudes et de Recherche sur les Pathologies Prostatiques (CeRePP), Paris, France Accepted for publication 2 July 2010 Study Type Therapy (case series) Level of Evidence 4 The standard treatment of upper urinary tract urothelial carcinomas (UUT-UCs) must obey oncological principles, which consist of a complete en bloc resection of the kidney and the ureter, as well as excision of a bladder cuff to avoid tumour seeding. The open technique is the gold standard of treatment to which all other techniques developed are necessarily compared, and various surgical procedures have been described. The laparoscopic stapling technique maintains a closed system but risks leaving behind the ureteric and bladder cuff segments. Transvesical laparoscopic detachment and ligation is a valid approach from an oncological stance but is technically difficult. The major inconvenience of the What s known on the subject? and What does the study add? The resection of the distal ureter and its orifice is an oncological principle during radical nephroureterectomy which is based on the fact that it represents a part of the urinary tract exposed to a considerable risk of. After removal of the proximal part it is hardly possible to image or approach it by endoscopy during follow-up. Recent publications on survival after nephroureterectomy do not allow the conclusion that removal of distal ureter and bladder cuff are useless. Several techniques of distal ureter removal have been described but they are not equivalent in term of oncological safety. transurethral resection of the ureteric orifice and intussusception techniques is the potential for tumour seeding. Management of the distal ureter via the robot-assisted laparoscopic method is technically feasible, but outcomes from these procedures are still preliminary. Therefore, prospective comparative studies with more thorough explorations of these techniques are needed to solve the dilemma of the management of the distal ureter during nephroureterectomy. However, bladder cuff excision should remain the standard of care irrespective of the stage of the disease. KEYWORDS upper urinary tract urothelial carcinoma, bladder cuff, nephroureterectomy, laparoscopic, pluck technique, ureteral intususseption, robotics, outcomes INTRODUCTION Open nephroureterectomy (ONU) remains the standard surgical treatment for upper urinary tract urothelial carcinoma (UUT-UC) [1,2]. For the distal ureter, it is standard practice to remove the intramural portion and ureteric orifice (UO), as well as the excision of a bladder cuff. Ideally, this is achieved by removal of an en bloc, closed system, specimen after controlled occlusion of the UO. However, several techniques of ureter and bladder cuff resection have been described. The challenges of all of these techniques are to remove the entire specimen en bloc, without tumour spillage, to conform to stringent oncological principles in the least invasive way possible. The aim of this article is to review the currently available data on the management of the distal ureter during nephroureterectomy. SURGICAL ACCESS FOR NEPHROURETERECTOMY ONU ONU can be performed with either one incision, via a transperitoneal approach, or with two incisions via a flank approach combined with a lower abdominal incision for the distal ureter and the bladder cuff [3]. LAPAROSCOPIC NEPHROURETERECTOMY (LNU) LNU has become a common treatment for UUT-UC with decreased perioperative morbidity [4,5]. Moreover, the oncological outcomes and survival rates are similar to ONU [4,6,7]. However, several precautionary measures must be taken when operating in a pneumo-peritoneal environment that may favour tumour spillage. 130 2010 108, 130 138 doi:10.1111/j.1464-410x.2010.09835.x

SURGICAL TECHNIQUES FOR DISTAL URETER REMOVAL DURING NEPHROURETERECTOMY ROBOT-ASSISTED NEPHROURETERECTOMY (RANU) Nazemi et al. [8] described the robotic approach but with no obvious advantages compared with other methods thus far. MANAGEMENT OF THE DISTAL URETER (Tables 1 [4,5,7,9 41] and 2 [4,5,7,9,11,15,16,19 22,27,29,30, 32 35,39 41]) OPEN REMOVAL Technique: Open removal of the distal ureter can occur either after a laparoscopic procedure or after an open procedure to dissect the kidney and the ureter. To excise the lower distal ureter, a lower midline, modified Pfannenstiel or Gibson incision can be performed. The lower ureter is clipped, dissected free, and removed in continuity with the bladder cuff. The bladder cuff may be secured extravesically (using a right angle clamp) or via an anterior cystotomy. The en bloc specimen is delivered through the same incision [4,9 11]. Advantages: This approach conforms to the oncological principles previously described and minimizes the risk of tumour spillage [3,12,13]. It also enables the visual confirmation of complete excision and accurate histological examination. Patient repositioning is usually required but not always mandatory. Disadvantages: The blind extravesical clamping may compromise the contralateral UO and does not inevitably guarantee adequate bladder cuff retrieval [14]. An anterior cystotomy is avoided in the presence of synchronous bladder UC because it retains the potential to seed tumour into the extravesical space [2,3,12]. Furthermore, prior pelvic surgery, irradiation, or obesity may render the open procedure more difficult. Evaluations: Open series are typically used by authors as the standard point of comparison for other techniques, and no authors have reported failures of this method. There are few postoperative complications (e.g. urinoma, urinary infection). The rates of for bladder tumours are 30% [3,4,9 11]. PURE STANDARD LAPAROSCOPIC EXCISION OF THE DISTAL URETER AND THE BLADDER CUFF Technique: A pure classic laparoscopic excision of the distal ureter and the bladder cuff can also be performed. Hattori et al. [15] described this technique where the ureter was ligated at the distal site of the tumour. Retracting the ureter cranially, a stay suture was placed at an anterior point on the bladder, and the bladder was opened. Incising around the UO, the distal ureter was detached with the bladder cuff. The opened bladder wall was closed with running stitches. Advantages/disadvantages: While respecting the aforementioned oncological principles, this method is technically difficult to perform. Evaluations: This method was technically successful in all 10 cases reported, with minimal bleeding and an average operative time of 87 min [15]. The margins of the bladder cuff were all negative, and at a mean follow-up of 19 months revealed there was only 10% bladder tumour. Modified technique: Shoma [16] described a modification for the excision of a bladder mucosal cuff around the ipsilateral ureter. In this procedure, the detrusor muscle was further dissected away from under the bladder mucosa for 1 cm around the UO. Thus, a bladder cuff of mucosal origin only could be retrieved. A purse-string suture was applied at the edge of the dissected mucosa, and the cuff was excised. The mean operative time was 226 min. During a follow-up of 31.5 months, one patient developed in the renal bed. LAPAROSCOPIC EXTRAVESICAL STAPLING OF THE DISTAL URETER AND URETERIC UNROOFING [12 16] Technique: The ureter is clipped early and dissected caudally until it diverges to merge with the detrusor muscle fibres at the vesicoureteric junction. Gentle traction on the ureter will tent up the wall of the bladder at the vesico-ureteric junction, enabling placement of a 12-mm laparoscopic GIA tissue stapler or a large Hem-o-lok clip. A more recent trend describes the stapling of the bladder cuff as the initial step, followed by transurethral resection (TUR) of the ipsilateral UO until the staple line is reached [17]. This method is usually combined with a ureteric unroofing procedure. The ureteric unroofing technique was described by the Washington University group [21]. It can only be used in transperitoneal LNU and comprises cystoscopic incision of the entire anterior length of the intramural ureter, electrocautery to the cut the edges and floor of the intramural ureter, placement of a 7.5 F occlusion ureteric balloon catheter in the renal pelvis to prevent urine spillage, laparoscopic dissection of the kidney and ipsilateral ureter down to the level of the bladder, and specimen detachment following placement of an Endo-GIA stapler on the bladder cuff. Advantages: It may help reduce operative duration and facilitates a minimally invasive procedure while maintaining a closed urinary tract, thus, preventing tumour spillage. Disadvantages: Operating the stapler may prove awkward in the restricted pelvic space. Additionally, an error in judgement might result in either part of the intramural ureter being left behind or inadvertent injury to the contralateral UO. In addition, the stapled margin cannot be assessed histologically, and the staple line can be a source of stone formation. Contraindications: The presence of mid or lower ureteric and bladder tumours. Evaluations: A comparison at nearly 4 years after LNU showed an increased positive margin rate and local rate, and decreased -free intervals were noted in the laparoscopic-stapled group when compared with the open group [19]. However, none of these results is statistically significant, probably owing to the few patients. Several authors have compared the various methods of distal ureteric excision and reported a higher incidence of positive surgical margins (up to 25%) and local (up to 15%) in the pure LNU with laparoscopic stapling cohort [20,21]. Modified technique: Tsivian et al. [22] described a variation on the laparoscopicstapling technique, using a 10-mm LigaSure Atlas. There were two bladder s distant from the site of surgery but no reports of local in 13 patients followed for nearly 1 year after surgery. 2010 131

PHÉ ET AL. TABLE 1 Different methods to manage the distal ureter in NU Methods Approach Principles Advantages Disadvantages Contraindications References [4,5,9 14] Open excision Open or laparoscopic Pure laparoscopic excision of the bladder cuff Extravesical laparoscopic stapling of the distal ureter Transvesical laparoscopic detachment and ligation technique Pluck technique = TURUO Open or laparoscopic Ureteric intussusception/ ureteric stripping Creation of an anterior cystotomy through a lower midline, Pfannenstiel or Gibson incision. Removing of a formal bladder cuff Laparoscopic Ligation of the distal ureter Incising around the UO, Formal bladder cuff detachment of the distal ureter with the bladder cuff The opened bladder wall is closed with running sutures Laparoscopic Laparoscopic stapling of the distal ureter Or Ligasure use Or Hem-o-lok clip Laparoscopic Placement of two laparoscopic ports transvesically, thus enabling one to place an Endoloop at the distal ureter after cystoscopic detachment. Or pneumovesicum use Open or laparoscopic Cystoscopic detachment of the intramural ureter by TUR before NU Pluck + Endoloop Pluck + Hem-o-lok clip Pluck + Tisseel HALNU Division and intussusception of the ureter, followed by cystoscopic detachment and transurethral removal Robot-assisted excision Robotic Bladder cuff excised either extravesically or via anterior cystotomy Standard adheres to oncological principles. Avoids tumour spillage. Formal bladder cuff. Bladder closed under direct vision. Adheres to oncological principles Bladder closed under direct vision Reduced operative duration Minimally invasive Prevent tumour spillage Adheres to oncological principles Distal occlusion of the ureter Obeys pure laparoscopic principles Avoids another incision Maximally invasive Difficult in anatomically unfavourable patients: obesity, prior pelvic surgery or irradiation, Technically difficult [15,16] Stapled margins cannot be assessed histologically Risk of stone formation Learning curve Additional ports Risk of extravasation of the irrigant solution Possibility of port-site metastasis Time consuming Risk of incomplete resection Potential leakage of tumour cells Repositioning of the patient necessary Presence of mid/lower ureteric and bladder tumour Prior pelvic surgery Obesity Distal ureter TCC Concomitant bladder tumour [5,17,19 22] Distal ureter tumour [27,28] Prevents tumour spillage Ureteric tumours [29 34] in the case of ureter perforation Minimally invasive principles Dexterity deep in pelvis improved Improved visualization Risk of ureteric breakage increased risk of tumour Cost Need to re-dock the robot Ureteric tumours [35 39] [7,18,20,23 26] [40,41] HALNU, hand-assisted LNU. 132 2010

SURGICAL TECHNIQUES FOR DISTAL URETER REMOVAL DURING NEPHROURETERECTOMY TABLE 2 Oncological outcomes of the different management techniques for the distal ureter during NU Management techniques for the distal ureter: reference Approach Open distal ureteric excision No. of patients Follow-up, months Mean op. duration, min Mean blood loss, ml Duration of catheter, days Mean hospital stay, days Failure Complication Positive margin Bladder Locoregional Klingler et al., 2003 [9] ONU/LNU 19 LNU 22.1 198 282 7 8.1 0 0 0 0 0 5.2 ND 15 ONU 23.1 220 532 7 13.3 0 26.7 femoralis embolus, 0 6.6 0 0 phlebitis, abdominal wall relaxation Metastasis Oncological outcomes; survival Tsujihata et al., 2006 [11] ONU/LNU 25 LNU 22.4 305.9 321.5 7.6 4 ND 0 ND 28 0 0 DFS rate 24 ONU 22.1 271.2 557.7 10.1 0 33 8 comparable (value?) Taweemonkongsap et al., 2008 [10] ONU/LNU 31 LNU 26.4 258.8 289.3 ND 9.32 ND 6.4 is chaemic heart disease, urinary infection 29 ONU 27.9 190.6 313.7 8.69 6.9 bleeding with reintervention, urinoma Waldert et al., 2009 [4] ONU/LNU 43 LNU 41 220 300 ND 8.1 0 2 bleeding with reintervention ND 29 6.4 9.6 2-year DFS 86.3 44.8 3.4 6.9 92.5 0 26 0 11 5-year DFS 79 0 27 10 12 76 Simone et al., 2009 [5] ONU 40 41 78 430 ND 3.65 0 0 ND 22.5 0 15 5-year CSS 89.9 Pure laparoscopic excision of the bladder cuff Hattori et al., 2008 [15] LNU 10 19 87 0 7 ND 0 10: urine leakage 0 10 1 1 ND Shoma, 2009 [16] LNU with 13 31.5 226 233 7 7 ND 0 0 15.3 7.6 0 ND 59 ONU 41 212 542 13.8 0 3 bleeding with reintervention pursestring suture Laparoscopic extravesical uretericstapling Matin and Gill 2005 [20] LNU 36 23 ND ND ND ND ND ND 25 41.7 8.3 25 Tsivian et al., 2007 [22] LNU 13 11.6 215 120 3 3.8 0 15.3 acute urinary retention, 0 15.3 0 0 ND haematoma Simone et al., 2009 [5] LNU 40 41 82 78 ND 2.3 0 0 ND 25 0 27.5 5-year CSS 79.8% Romero et al., 2007 [19] LNU 12 54.5 292.9 400 ND 3.8 0 25 25 50 16.7 50 ND Shalhav et al., 2000 [21] LNU 24 24 462 199 2/3 6.1 0 2 bleeding, urine leakage 0 23 12.5 31 ND 2010 133

PHÉ ET AL. TABLE 2 Continued Management techniques for the distal ureter: reference Approach Transvesical laparoscopic detachment and ligation technique Gill et al., 2000 [7] LNU 42 11 222 242 7.6 2.3 ND 5 fluid extravasation, renal vein injury, atelectasis 3 23 0 8.6 ND Matin and Gill, 2005 [20] LNU 12 23 ND ND ND ND ND ND 2.8 13.9 5.6 8.3 Pluck technique Keeley and Tolley, 1998 [27] LNU 22 ND 156 ND ND 5.5 13.6 27.3 bleeding, atelectasis, wound infection, myocardial infarction Agarwal et al., 2008 [29] LNU 13 15.3 230 303.8 7 7.3 0 15.3 acute myocardial infarction Mueller et al., 2010 [30] LNU 8 11 308 150 10 6 0 2 5 minor complication: ileus Wong and Leveillee 2002 [32] No. of patients Follow-up, months Mean op. duration, min Mean blood loss, ml HALNU 14 8 ND ND No blood transfusion Duration of catheter, days Mean hospital stay, days Failure Complication 12 major complication: Intraoperative bleeding from the left lumbar vein. ND 0 4.5 4.5 ND 0 38 0 7.6 ND 0 0 0 0 ND ND 2 0 0 ND 14.2 0 0 ND Kurzer et al., 2006 [33] HALNU 49 10.6 ND 273 7 3 0 8.1 pulmonary emboli, upper gastrointestinal bleeding, congestive heart failure Vardi et al., 2006 [34] HALNU 6 31 264 254 7 10 6.3 0 1 complication: 1 pulmonary embolus 4 49 0 6 ND 0 16.6 0 0 ND Ureteral stripping Giovansili et al., 2004 [35] ONU 32 35.2 180 220 5 8 18.7 3.1 wound haematoma ND 18.7 6.2 3.1 5-year RFS 62.3% Saika et al., 2004 [39] ONU 28 5.5 183 150 7 ND 0 0 0 35.7 0 7.1 3-year OS 90.9% Robotic Park et al., 2009 [41] RANU 11 ND 220 188 ND 7.7 0 0 0 ND ND ND ND Nanigian et al., 2006 [40] RANU 11 6 264 ND ND 3 9 0 0 30 0 0 ND Positive margin Bladder Locoregional Metastasis Oncological outcomes; survival CSS, cancer-specific survival; DFS; disease-free survival; HALNU, hand-assisted LNU; ND, not done; OS, overall survival; RFS, -free survival; RANU, robotic-assisted NU. 134 2010

SURGICAL TECHNIQUES FOR DISTAL URETER REMOVAL DURING NEPHROURETERECTOMY TRANSVESICAL LAPAROSCOPIC DETACHMENT AND LIGATION TECHNIQUE Technique: During retroperitoneal LNU, this technique of securing the distal ureter and bladder cuff using transvesically placed laparoscopic ports was described by Gill et al. [7]. In this procedure, a transurethral Collin s knife incision of the bladder cuff is made after placement of a catheter into the affected ureter. Traction on the incised bladder cuff enables the mobilization of 3 4 cm of distal ureter into the bladder. The entire ureter can then be pulled through in a cephalad fashion after radical nephrectomy and ureteric dissection. Advantages: The transvesical technique adheres to general oncological principles of complete and controlled en bloc specimen extraction. The ureteric catheter and Endoloop occlude the ureter, thereby reducing urine leakage. Further, an indwelling ureteric catheter can aid identification and mobilization of the ureter during the laparoscopic procedure. Complete retrieval is confirmed by visualization of the Endoloop. Disadvantages: This may be a difficult technique to master for most urologists, and the operating duration is usually lengthened by 60 90 min [23,24]. Other criticisms of this approach include the potential for irrigation fluid extravasation resulting in dilutional hyponatraemia, the need for patient repositioning, and the possibility of port-site metastases. Contraindications: The presence of distal ureteric tumour or concomitant bladder tumours, previous pelvic surgery, or irradiation and obesity [22]. Evaluations: Matin and Gill [20] reviewed retrospectively the outcomes in 60 patients after LNU, who had either had a laparoscopic stapling (12 patients) or transvesical laparoscopic detachment of the distal ureter (36). After a mean follow-up of 23 months, positive margins were more common in the former group (25% vs 2.8%), as were the rates of bladder s at the ipsilateral UO/ scar (41.7% vs 13.9%), retroperitoneal (8.3% vs 5.6%), and distant metastasis (25% vs 8.3%). None of these differences were statistically significant, and definitive conclusions are difficult to derive from such a small retrospective series. Modified technique: A similar technique has been described using a pneumovesicum to secure the UO and bladder cuff [25,26]. This approach has several theoretical advantages, including en bloc removal of the entire specimen, excellent visualization in the bladder and minimization of the potential for tumour seeding with early closure of the UO during distal ureteric dissection, and the use of pneumovesicum instead of fluid irrigation. Another advantage of a pneumovesicum approach is that the ports are placed extraperitoneally (similar to a suprapubic tube), and the need for a large transvesical incision is eliminated, which potentially improves recovery times, minimizes bladder spasms and haematuria, and allows for earlier Foley catheter removal. However, there are no data concerning the long-term oncological outcomes of this technique. THE ORIGINAL TUR OF THE UO TECHNIQUE, I.E. THE PLUCK TECHNIQUE Standard technique Technique: The original TUR of the UO (TURUO) technique, also known as the pluck technique, was originally used during ONU and subsequently adapted for LNU. Patients undergo rigid cystoscopy with aggressive resection of the UO and intramural ureter into the perivesical fat. Once the proximal specimen is mobilized, the previous TUR eases the subsequent bladder cuff excision. In 1998, Keeley and Tolley [27] first described the use of the pluck technique in LNU, thus making the procedure purely laparoscopic. This involves initial endoscopic resection of the UO. The ureteric lumen is completely coagulated to prevent urinary spillage. NU is then performed using a flank incision, with gentle traction of the ureter. Disadvantages: One disadvantage of this technique is the increase in procedure duration caused by the need for repositioning. Notably, the potential for incomplete resection of the intramural ureter exists. Thus, this procedure should be avoided in patients with distal ureteric tumour [25]. Evaluations: Salvador-Bayarri et al. [28] compared the results of the pluck technique with those of standard NU and concluded that the pluck technique did not increase the risk of tumour after NU for upper urinary tract carcinoma. Pluck Technique modifications Various modifications on the pluck theme have been described to minimize tumour spillage. A preformed polydioxanone Endoloop can be passed through the cystoscope to ligate and occlude the UO [29]. Mueller et al. [30] recently described a technique with injection of Tisseel into the ureter after confirming the absence of bladder tumours and introducing an 8 F olive-tipped ureteric catheter into the UO. Pluck Technique in hand-assisted LNU Alternatives to endoscopic management of the distal ureter during hand-assisted LNU have been reported [31 34]. Gonzalez et al. [31] described a technique implementing insertion of a laparoscopic port, followed by introduction of a 24 F nephroscope, allowing endoscopic Collin s knife incision of the bladder cuff. This is performed subsequent to dissection of the kidney and ureter and after clips have been placed on the lower ureter. Alternatively, a similar technique may be performed without the need for a bladder port or patient repositioning [32]. Vardi et al. [34] reported a novel modification to this technique by inserting a flexible cystoscope per urethra and a 5 F electrode (ACMI, Norwalk, Conn, USA) to incise a circumferential 2-cm cuff of bladder around the UO using a cutting and coagulating current. Patient repositioning after the nephrectomy is avoided, and the bladder opening is not closed. There were no pelvic s in their small group of patients after a mean follow-up of 31 months. Conclusions None of the endoscopic techniques have been evaluated extensively. There are no randomised trials and no comparative data on outcomes due to the rarity of UUT-UCs. INTUSSUSCEPTION TECHNIQUE OR URETERIC STRIPPING Technique: Principles of this technique include initial catheterization of the ureter, using either a ureteric catheter or a stone 2010 135

PHÉ ET AL. FIG. 1. Flow-chart of available options for distal ureter management during nephroureterectomy. UUT-CC NEPHROURETERECTOMY MANAGEMENT OF THE DISTAL URETER GOLD STANDARD: Open removal of the distal ureter + bladder cuff Pure standard laparoscopic excision of the distal ureter + bladder cuff Laparoscopic extravesical stapling of the distal ureter + ureteric unroofing Transvesical laparoscopic detachment and ligation technique Pluck technique Intussusception technique or ureteric stripping Robot assisted Technically difficult Risk of leaving behind the ureteral and bladder cuff segments Technically difficult Risk of tumour seeding Risk of tumour seeding Preliminary outcomes SAFE ONCOLOGICAL APPROACH basket ligation, and division of the ureter as part of the renal mobilization. This is followed by securing the distal ureter to the ureteric catheter/stone basket, transurethral incision of the bladder cuff, and removal of the distal ureter by gentle traction on the catheter via the urethra [35]. The distal ureter intussuscepts into the bladder and can either be removed transurethrally or via a small lower midline incision and anterior cystotomy. Various technical devices, including sutures, vein strippers, balloon catheters, and double ligations, have been described in an attempt to improve ureteric excision of the ureter [36,37]. Disadvantages: The main drawback of this procedure is a failure to guarantee adequate excision of the intramural ureter and bladder cuff, potentially resulting in tumour. Contraindications: Because the ureter is transected, it is contraindicated for ureteric tumours and primarily confined to low-grade renal pelvic tumours. Additionally, any cause for pelvic fibrosis, such as previous surgery or irradiation and retroperitoneal fibrosis, may further increase the risk of retention of ureteric remnants. Evaluations: The stripping and pluck techniques were compared in a systematic review [38]. Whereas there were no reports of local disease in the stripping group, this technique was associated with a 10% complication rate (including retained ureters and catheter breakage), resulting in an open conversion rate of 9.5 12.5% in patients after difficult extraction. In a comparative study of patients who underwent total NU with transurethral ureteric stripping and patients who underwent the standard two-incision NU, transurethral stripping appears to be associated with significantly greater intravesical tumour rate [39]. ROBOT A robot-assisted laparoscopic approach has also been reported [40,41]. The principal advantage of the robotic approach appears to be that repositioning of the patient from flank to supine and movement of the patient cart are unnecessary. Keeping the patient in the flank position not only shortens the operative duration, but also improves exposure of the distal ureterectomy and closure of the bladder cuff. All current available options for distal ureter management are presented in Fig. 1. CONCLUSION Each technique of distal ureter management has inherent advantages and disadvantages. However, thus far, no prospective, randomised trials have compared the different approaches. The reported rates within the bladder after various management techniques of the distal ureter during NU vary considerably from 6.7% to 50%. Additional long-term comparative outcomes are needed to solve the dilemma of the distal ureter. CONFLICT OF INTEREST None declared. 136 2010

SURGICAL TECHNIQUES FOR DISTAL URETER REMOVAL DURING NEPHROURETERECTOMY REFERENCES 1 Oosterlinck W, Solsona E, van der Meijden AP et al. EAU guidelines on diagnosis and treatment of upper urinary tract transitional cell carcinoma. Eur Urol 2004; 46: 147 54 2 Azemar MD, Comperat E, Richard F, Cussenot O, Roupret M. Bladder after surgery for upper urinary tract urothelial cell carcinoma: frequency, risk factors, and surveillance. Urol Oncol 2009; [Epub ahead of print]. DOI:10.1016/ j.urolonc.2009.06.003 3 Margulis V, Shariat SF, Matin SF et al. Outcomes of radical nephroureterectomy: a series from the Upper Tract Urothelial Carcinoma Collaboration. Cancer 2009; 115: 1224 33 4 Waldert M, Remzi M, Klingler HC, Mueller L, Marberger M. The oncological results of laparoscopic nephroureterectomy for upper urinary tract transitional cell cancer are equal to those of open nephroureterectomy. BJU Int 2009; 103: 66 70 5 Simone G, Papalia R, Guaglianone S et al. Laparoscopic versus open nephroureterectomy: perioperative and oncologic outcomes from a randomised prospective study. Eur Urol 2009; 56: 520 6 6 Capitanio U, Shariat SF, Isbarn H et al. Comparison of oncologic outcomes for open and laparoscopic nephroureterectomy: a multiinstitutional analysis of 1249 cases. Eur Urol 2009; 56: 1 9 7 Gill IS, Sung GT, Hobart MG et al. Laparoscopic radical nephroureterectomy for upper tract transitional cell carcinoma: the Cleveland Clinic experience. J Urol 2000; 164: 1513 22 8 Nazemi T, Galich A, Sterrett S, Klingler D, Smith L, Balaji KC. Radical nephrectomy performed by open, laparoscopy with or without hand-assistance or robotic methods by the same surgeon produces comparable perioperative results. Int Braz J Urol 2006; 32: 15 22 9 Klingler HC, Lodde M, Pycha A, Remzi M, Janetschek G, Marberger M. Modified laparoscopic nephroureterectomy for treatment of upper urinary tract transitional cell cancer is not associated with an increased risk of tumour. Eur Urol 2003; 44: 442 7 10 Taweemonkongsap T, Nualyong C, Amornvesukit T et al. Outcomes of surgical treatment for upper urinary tract transitional cell carcinoma: comparison of retroperitoneoscopic and open nephroureterectomy. World J Surg Oncol 2008; 6: 3 11 Tsujihata M, Nonomura N, Tsujimura A, Yoshimura K, Miyagawa Y, Okuyama A. Laparoscopic nephroureterectomy for upper tract transitional cell carcinoma: comparison of laparoscopic and open surgery. Eur Urol 2006; 49: 332 6 12 Hall MC, Womack S, Sagalowsky AI, Carmody T, Erickstad MD, Roehrborn CG. Prognostic factors,, and survival in transitional cell carcinoma of the upper urinary tract: a 30-year experience in 252 patients. Urology 1998; 52: 594 601 13 Lughezzani G, Sun M, Perrotte P et al. Should bladder cuff excision remain the standard of care at nephroureterectomy in patients with urothelial carcinoma of the renal pelvis? A population-based study. Eur Urol 2010; 57: 956 62 14 Strong DW, Pearse HD, Tank ES Jr, Hodges CV. The ureteral stump after nephroureterectomy. J Urol 1976; 115: 654 5 15 Hattori R, Yoshino Y, Komatsu T, Matsukawa Y, Ono Y, Gotoh M. Pure laparoscopic complete excision of distal ureter with a bladder cuff for upper tract urothelial carcinoma. World J Urol 2009; 27: 253 8 16 Shoma AM. Purse-string technique for laparoscopic excision of a bladder mucosal cuff in patients with transitional cell carcinoma of the upper urinary tract: initial report with intermediate follow-up. BJU Int 2009; 104: 1505 9 17 Tan BJ, Ost MC, Lee BR. Laparoscopic nephroureterectomy with bladder-cuff resection: techniques and outcomes. J Endourol 2005; 19: 664 76 18 Gill IS, Soble JJ, Miller SD, Sung GT. A novel technique for management of the en bloc bladder cuff and distal ureter during laparoscopic nephroureterectomy. J Urol 1999; 161: 430 4 19 Romero FR, Schaeffer EM, Muntener M, Trock B, Kavoussi LR, Jarrett TW. Oncologic outcomes of extravesical stapling of distal ureter in laparoscopic nephroureterectomy. J Endourol 2007; 21: 1025 7 20 Matin SF, Gill IS. Recurrence and survival following laparoscopic radical nephroureterectomy with various forms of bladder cuff control. J Urol 2005; 173: 395 400 21 Shalhav AL, Dunn MD, Portis AJ, Elbahnasy AM, McDougall EM, Clayman RV. Laparoscopic nephroureterectomy for upper tract transitional cell cancer: the Washington University experience. J Urol 2000; 163: 1100 4 22 Tsivian A, Benjamin S, Sidi AA. A sealed laparoscopic nephroureterectomy: a new technique. Eur Urol 2007; 52: 1015 9 23 Kaouk JH, Savage SJ, Gill IS. Retroperitoneal laparoscopic nephroureterectomy and management options for the distal ureter. J Endourol 2001; 15: 385 90 24 Steinberg JR, Matin SF. Laparoscopic radical nephroureterectomy: dilemma of the distal ureter. Curr Opin Urol 2004; 14: 61 5 25 Cheng CW, Ng CF, Mak SK et al. Pneumovesicum method in en-bloc laparoscopic nephroureterectomy with bladder cuff resection for upper-tract urothelial cancer. J Endourol 2007; 21: 359 63 26 Guzzo TJ, Schaeffer EM, Allaf ME. Laparoscopic radical nephroureterectomy with en-bloc distal ureteral and bladder cuff excision using a single position pneumovesicum method. Urology 2008; 72: 850 2 27 Keeley FX Jr, Tolley DA. Laparoscopic nephroureterectomy: making management of upper-tract transitionalcell carcinoma entirely minimally invasive. J Endourol 1998; 12: 139 41 28 Salvador-Bayarri J, Rodriguez-Villamil L, Imperatore V, Palou Redorta J, Villavicencio-Mavrich H, Vicente- Rodriguez J. Bladder neoplasms after nephroureterectomy: does the surgery of the lower ureter, transurethral resection or open surgery, influence the evolution? Eur Urol 2002; 41: 30 3 29 Agarwal DK, Khaira HS, Clarke D, Tong R. Modified transurethral technique for the management of distal ureter during laparoscopic assisted nephroureterectomy. Urology 2008; 71: 740 3 30 Mueller TJ, DaJusta DG, Cha DY, Kim IY, Ankem MK. Ureteral fibrin sealant injection of the distal ureter during 2010 137

PHÉ ET AL. laparoscopic nephroureterectomy a novel and simple modification of the pluck technique. Urology 2010; 75: 187 92 31 Gonzalez CM, Batler RA, Schoor RA, Hairston JC, Nadler RB. A novel endoscopic approach towards resection of the distal ureter with surrounding bladder cuff during hand assisted laparoscopic nephroureterectomy. J Urol 2001; 165: 483 5 32 Wong C, Leveillee RJ. Hand-assisted laparoscopic nephroureterectomy with cystoscopic en bloc excision of the distal ureter and bladder cuff. J Endourol 2002; 16: 329 3 33 Kurzer E, Leveillee RJ, Bird VG. Combining hand assisted laparoscopic nephroureterectomy with cystoscopic circumferential excision of the distal ureter without primary closure of the bladder cuff is it safe? J Urol 2006; 175: 63 8 34 Vardi IY, Stern JA, Gonzalez CM, Kimm SY, Nadler RB. Novel technique for management of distal ureter and en block resection of bladder cuff during hand-assisted laparoscopic nephroureterectomy. Urology 2006; 67: 89 92 35 Giovansili B, Peyromaure M, Saighi D, Dayma T, Zerbib M, Debre B. Stripping technique for endoscopic management of distal ureter during nephroureterectomy: experience of 32 procedures. Urology 2004; 64: 448 52 36 Angulo JC, Hontoria J, Sanchez- Chapado M. One-incision nephroureterectomy endoscopically assisted by transurethral ureteral stripping. Urology 1998; 52: 203 7 37 Roth S, van Ahlen H, Semjonow A, Hertle L. Modified ureteral stripping as an alternative to open surgical ureterectomy. J Urol 1996; 155: 1568 71 38 Laguna MP, de la Rosette JJ. The endoscopic approach to the distal ureter in nephroureterectomy for upper urinary tract tumor. J Urol 2001; 166: 2017 22 39 Saika T, Nishiguchi J, Tsushima T et al. Comparative study of ureteral stripping versus open ureterectomy for nephroureterectomy in patients with transitional carcinoma of the renal pelvis. Urology 2004; 63: 848 52 40 Nanigian DK, Smith W, Ellison LM. Robot-assisted laparoscopic nephroureterectomy. J Endourol 2006; 20: 463 6 41 Park SY, Jeong W, Ham WS, Kim WT, Rha KH. Initial experience of robotic nephroureterectomy: a hybrid-port technique. BJU Int 2009; 104: 1718 21 Correspondence: Morgan Rouprêt, Hôpital Pitié-Salpêtrière, 47 83 Boulevard de l hôpital, 75013 Paris, France. e-mail: morgan.roupret@psl.aphp.fr Abbreviations: (O)(L)(RA)NU, (open) (laparoscopic) (robot-assisted) nephroureterectomy; TUR, transurethral resection; UC, urothelial carcinoma; UO, ureteric orifice; UUT, upper urinary tract. 138 2010