Management of the Distal Ureter During Nephroureterectomy for Upper Tract Urothelial Carcinoma: A Comprehensive Review of Literature Samuel Morriss1, Homayoun Zargar2,3*, Brendan Hermenigildo Dias2,3 Purpose: Radical open nephroureterectomy (ONU) with bladder cuff excision (BCE) is the traditional gold stand- ard approach for management of high-risk non-metastatic upper tract urothelial cancer. ONU involves two separate procedures; the nephrectomy and distal ureterectomy, with each of these parts being able to be performed with an open or minimally-invasive approach. Multiple approaches have been described for the resection of the distal ureter and bladder cuff after mobilization of the kidney and upper ureter. Materials and Methods: A Medline search of the literature including relevant articles up to March, 2020 was performed. Search terms included “nephroureterectomy”, “upper tract urothelial carcinoma”, “upper urinary tract carcinoma OR UTUC”, “open OR conventional OR ONU OR conventional”, “robotic-assisted nephroureterec- tomy OR RANU”, “laparoscop* OR LNU OR LRNU” and “minimally-invasive nephroureterectomy”. Original articles, case series and review articles were included. Results: There are no randomised studies. Various techniques have been described to manage the distal ureter dur- ing nephroureterectomy. This review provides an overview of these techniques. The perioperative and oncological outcomes following open versus endoscopic techniques and minimally invasive techniques have been described. Although endoscopic approaches have more favourable perioperative outcomes, this comes at the expense of in- creased risk of tumour spillage and recurrence compared to the traditional open approaches. Minimally-invasive techniques (laparoscopic and robotic-assisted NU) largely have superior perioperative outcomes versus their open NU counterparts, with comparable oncological outcomes. Conclusion: Current non-randomised evidence is open to selection bias and is insufficient to support or refute endoscopic management of the distal ureter as an alternative to open bladder cuff excision. The optimal approach to nephroureterectomy and management of the distal ureter continues to remain a surgical dilemma. Keywords: nephroureterectomy; ureteral neoplasms; carcinoma, transitional cell INTRODUCTION Upper tract urothelial carcinoma (UTUC) is rare, comprising 5-10% of all urothelial cancers(1). It can involve the urothelial lining anywhere from the re- nal calyces down to the distal ureteric orifice. Radical open nephroureterectomy (ONU) with bladder cuff ex- cision (BCE) is the traditional gold standard approach for management of high-risk non-metastatic UTUC, recommended by the European Association of Urology guidelines(2). High-risk UTUC is defined as having any of the following factors present: hydronephrosis, tu- mour size greater than 2 cm, high-grade cytology, high- grade URS biopsy, multifocal disease, previous radical cystectomy for high-grade bladder cancer, or variant histology(2). Due to the propensity for recurrence seen with this type of malignancy, the surgical approach in- volves complete en bloc resection of the kidney, ipsilat- eral ureter, and bladder cuff, regardless of the location of the lesion along the urinary tract. It is imperative this 1Melbourne Medical School, The University of Melbourne, Australia. 2Department of Surgery, The University of Melbourne. Australia 3Department of Urology, Western Health, Australia. Correspondence: 2/132 La Scala Avenue, Maribyrnong, Victoria 3032, Australia. Phone:+61 300 927427. Email:homi.zargar@gmail.com Received October 2021 & Accepted November 2021 be done in a manner that is oncologically-sound, where- by tumour spillage and seeding are avoided(3,4). Previously, surveillance following NU has remained as the standard of care for UTUC, with systemic chemo- therapy not being recommended(5). However, recent level 1 RCT evidence from the POUT trial(6) assessed the efficacy of adjuvant platinum-based chemotherapy in patients with locally-advanced UTUC, showing that gemcitabine-platinum combination chemotherapy ad- ministered within 90 days after NU reduces rates of re- currence and improves disease-free survival. This study suggests that adjuvant chemotherapy be recommended as the new guideline for management post-NU. ONU involves two separate procedures; the nephrec- tomy and distal ureterectomy, with each of these parts being able to be performed with an open or minimal- ly-invasive approach. Multiple approaches have been described for the resection of the distal ureter and blad- der cuff after mobilization of the kidney and upper ure- ter. It has been shown that if the distal intramural ureter Urology Journal/Vol 18 No. 6/ November-December 2021/ pp. 585-599. [DOI: 10.22037/uj.v18i.7024] REVIEW Distal ureter in NU-Morriss et al. Review 586 Table 1a. Contemporary (2009 – 2021) oncological data comparing endoscopic vs non-endoscopic approaches Study Approach to NU Patients Mean age Length of Intravesical Other recurrence CFS, OS, CSS (%) DSM and year and distal ureter (N) (years) follow-up (months) recurrence no. (%) no. (%) Metastasis no. (%) (disease- specific mortality), n (%) Xylinas et al. Transvesical 1811 68.7 61.1 388 (21.4) 526 (29) RFS: 66 CSS: 71 419 (23.1) 2014 (36) Extravesical Endoscopic 785 67.7 52.3 160 (20.3) 204 (25.9) OS: 66 175 (22.3) 85 69.6 36.1 29 (34.1) 18 (21.2) RFS: 66 CSS: 70 11 (12.9) OS: 66 RFS: 69 CSS: 82 OS: 69 Chiang et al. Hand-assisted 98 67.54 25.28 26 (26.53) 12 (12.24) Mets: 14 (14.29) 6 (6.12) 2011 (37) retroperitoneoscopic 110 65.2 27.88 32 (29.09) 11 (10.00) Mets: 11 (10.00) 9 (8.18) Transurethral bladder cuff incision-assisted Fragkoulis et al. Open 192 69.2 60 46 (24) - CSS: 74 - 2017 (38) Transurethral 186 68.7 50 (27) CSS: 75 Kapoor et al. Extravesical 316 69.9 24.6 77 (24.4) - RFS: 35.6 136 (16.6) 2014 (7) Intravesical 406 69.2 - 66 (16.3) RFS: 46.3 Endoscopic 98 70.0 23 (23.5) RFS: 30.1 Kim et al. Hand-assisted 28 68 - 6 (21.4) - - - 2014 (39) retroperitoneoscopic Li et al. 2010 (40) Intravesical 81 65.4 33 19 (23.5) 10 (12.3) Mets: 6 (7.4) 15 (18.5) Extravesical 129 39 31 (24.0) 15 (11.6) Mets: 13 (10.1) 17 (13.2) Transurethral 91 30 16 (17.6) 7 (7.7) Mets: 5 (5.5) 9 (9.9) Ou and Yang Hand-assisted 30 69.9 25.8 7 (23) 1 Mets: 0 - 2014 (41) retroperitoneoscopic: no ureteral ligation Hand-assisted 31 67.8 53.1 11 (35) 4 Mets: 2 retroperitoneoscopic: earlier ureteral ligation Cormio et al. Open with transurethral 13 64.7 39.8 4 (30.1) 0 (1) - - 2013 (42) distal ureter balloon occlusion and detachment Cormio et al. Open with flexible 10 68.2 31.1 2 (20.0) 0 (0) - - 2014 (43) cystoscope-assisted transurethral distal ureter balloon occlusion and detachment Geavlete et al. Endoscopic pluck with 42 - 14 6 (14) 2 (5) - 2 (4.8) 2012 (44) bipolar plasma vaporisation Gillan et al. (45) Laparoscopic 6 73.6 12 0 (0) - - - Endoscopic Open 12 75.2 2 12 71.8 1 Lai et al. (46) Intravesical Extravesical 99 69 44.2 (17.2) - CSS: (11.1) 20 (8.1) Transurethral endoscopic 96 (12.5) CSS: (5.2) 53 (13.2) CSS: (7.5) Ryoo et al. (47) Transvesical resection 477 64.4 36.5 157 (32.9) - Intravesical recurrence- - Extravesical ligation 379 65.3 38.2 163 (43.0) free survival IVRFS: 59.9 CSS: 82.0 OS: 79.7 IVRFS: 49.3 CSS: 73.8 OS: 68.0 Allard et al. (48) Extravesical Intravesical 29 72.4 22 8 (26.7) Urothelial recurrence Mets: 6 (20.6) - Transurethral incision 20 70.4 7 (35.0) : 8 (26.7) Mets: 2 (10.0) 61 70.1 19 (31.1) Urothelial recurrence: Mets: 10 (16.4) 8 (38.1) Urothelial recurrence: 20 (32.8) Carrion et al. (49) Endoscopic resection 32 70 32 5 (15.6) 7 (21.9) CSS: 84 months 5 (15.6) Endoscopic bladder cuff 57 70.1 9 (15.8) 13 (22.8) CSS: 89 months 10 (17.5) Open extravesical 21 67.8 4 (19) 11 (52.4) CSS: 48 months 11 (52.4) Open intravesical 42 70.81 20 (47.6) 11 (26.2) CSS: 71 months 10 (23.8) Bragayrac et al. (50) Transvesical 5 70 16.2 0 (0) - Mets: 1 (20) - laparoendoscopic single-site Pang et al. (51) Open Transurethral 24 - - 5 1 - - electrosurgery 17 4 0 Transurethral endoscopic 17 2 0 two-micron thulium laser resection Table 1b. Contemporary (2009 – 2021) oncological data comparing ONU vs minimally-invasive NU Study and Approach Patients (N) Mean age Length of Intravesical Other CFS, OS, DSM year to NU and (years) follow-up recurrence CSS (%) (disease-specific distal ureter (months) no. (%) Metastasis no. (%) mortality), n (%) Ariane et al. (52) Open Laparoscopic 459 69.8 40.4 - - CSS: 78.0 RFS: 50.7 - 150 69.5 24.5 Mets: 97 (21.1) CSS: 90.7 RFS: 52.2 Mets: 21 (14) Blackmur et al. (53) Open Laparoscopic 13 67.5 57.0 4 (30.8) 1 (7.7) OS: 73.5 PFS: - 13 68.0 25.8 4 (30.8) 4 (30.8) 56.0 CSS: 73.5 OS: 59.1 PFS: 24.0 CSS: 60.9 Eandi JA et al. (54) Robotic-assisted 11 67.4 15.2 4 (36.4) - - Mets: 2 (18.2) 4 (36.4) Fairey et al. (55) Open Laparoscopic 403 70.5 26 - - OS: 67 DSS: 73 - 446 72.4 RFS: 43 OS: 68 DSS: 76 RFS: 33 Favaretto RL Open Laparoscopic 109 71 23 51 (31.5) 19 (11.7) CSS: 86 RFS: 38 26 (16.0) et al. (56) 53 73 15 (9.3) 14 (8.6) CSS: 82 RFS: 42 9 (5.6) Hemal et al. (34) Robotic-assisted 15 66.27 Short-term 0 0 - - Lim et al. (57) Robotic-assisted 32 66.5 45.5 10 (31.3) 14 (43.8) OS: 60.9 CSS: 75.8 7 (21.9) RFS: 68.1 Park et al. (58) Laparoscopic 101 66.4 14 Distant + bladder Distant + - 6 (5.9) recurrence: 22.8 bladder recurrence: 22.8 Walton et al. (59) Open Laparoscopic 703 68 36 - 165 (23.5) RFS: 73.7 CSS: 75.4 146 (20.8) 70 70 17 17 (24.3) RFS: 63.4 CSS: 75.2 9 (12.9) Capitano et al. (60) Open Laparoscopic 979 68.3 62 - Total recurrence: 250 (25.5) CSS: 73.1 RFS: 270 70.2 Total recurrence: 27 (10.0) 76.2 CSS: 85.8 RFS: 86.8 217 (22.8) 21 (7.8) Wang et al. (61) Open Laparoscopic 72 66.1 42.4 18 (25.0) 7 (9.7) CSS: 80.3 RFS: 59.2 12 (16.7) 86 68.7 16 (18.6) 15 (17.4) CSS: 80.7 RFS: 62.8 10 (11.6) Zou et al. (62) Open Laparoscopic 101 63.8 53 - - CSS: 79.2 - 21 63.2 CSS: 85.7 Simone et al. (63) Open Laparoscopic 40 61.3 44 9 (22.5) - CSS: 89.9 Mets: 6 (15) 4 (10) 40 59.6 10 (25.0) MFS (metastasis-free 8 (20) survival): 77.4 CSS: 79.8 Mets: 11 (27.5) MFS: 75.5 Greco et al. (64) Open Laparoscopic 70 67.2 60 5 (7.1) - DFS (disease-free - 70 66.4 3 (4.3) survival):73 DFS: 75 Kamihira et al. (65) Laparoscopic 1003 68.6 20 (43) 134 (13.4) RFS: 42 (4) OS: 70 Kitamura et al. (66) Open 34 69 70 - - CSS: 74.2 RFS: 57.1 - Hand-assisted 9 65 CSS: 72.9 RFS: 12.5 laparoscopic CSS: 87.4 RFS: 69.2 Laparoscopic 65 70 Lim et al. (67) Robotic-assisted 38 66.5 40.6 10 (26.3) 145 (39.5) - 7 (18.4) Pugh et al. (68) Robotic-assisted 43 68.3 9.6 6 (14) 3 (7) - - Yang et al. (69) Robotic-assisted 20 70.1 14.7 3 (15) 4 (20) Mets: 4 (20) - Miyazaki et al. (70) Open Laparoscopic 527 69.5 39.0 174 (33.0) 64 (12.1) OS: 69.5 CSS: 73.0 222 70.1 69 (31.1) 27 (12.2) Mets: 186 (35.3) - OS: 72.4 CSS: 76.0 Mets: 75 (33.8) Stewart et al. (71) Open Laparoscopic 39 68.1 177 15 (39) - OS: 64 PFS (progression 8 (21) 23 67.4 146 9 (39) -free survival): 79 CSS: 80 7 (30) OS: 61 PRS: 76 CSS: 71 Aboumohamed Robotic-assisted 65 69.1 25.1 15 (27.2) 13 (20) OS: 62.6 - et al. (31) CSS: 92.9 RFS: 57.1 Mets: 8 (13.3) Ambani et al. (72) Robotic-assisted 22 70.1 10 8 (36) 7 (32) - 2 (9) Laparoscopic 22 70.8 15 7 (37) 5 (23) 2 (9) Badani et al. (33) Robotic-assisted 26 66 7.8 4 (15) 0 (0) - - Chen et al. (73) Open with early ligation 42 63 28 21 (25) 5(6) - - of distal ureter 43 67 Open with late ligation of distal ureter Hattori et al. (26) Laparoscopic 10 19 19 1 (10) 3 (30) - 1 (10) Hu et al. (74) Robotic-assisted 18 70.4 6.1 2 (11.1) 0 (0) Mets: 4 (22.2) 1 (5.6) Hand-assisted laparoscopic 197 67.7 47.8 6 (33.3) 2 (11.1) Mets: 2 (11.1) 3 (16.7) Distal ureter in NU-Morriss et al. Vol 18 No 6 November-December 2021 587 Study and Approach Patients (N) Mean age Length of Intravesical Other CFS, OS, DSM year to NU and (years) follow-up recurrence CSS (%) (disease-specific distal ureter (months) no. (%) Metastasis no. (%) mortality), n (%) Lambert et al. (75) Laparoscopic 22 65.6 20 3 (13.6) 2 (9.1) - - Liu et al. (76) Laparoscopic 31 66.8 10.5 0 (0) 0 (0) - - Mak et al. (77) Pneumovesicum-assisted 10 71.6 46 4 (40) 1 (10) - - laparoscopic Ritch et al. (27) Open Laparoscopic 10 68 16 2 (20) 0 (0) Mets: 0 (0) 0 (0) stapling 14 70 21 2 (14.3) 2 (14.3) Mets: 2 (14.3) 1 ((7.1) Laparoscopic resection 12 71 7 0 (0) 0 (0) Mets: 0 (0) 0 (0) and suturing Shoma et al. (78) Laparoscopic 13 50 31.5 2 (15) 1 (8) - 1 (8) Song et al. (79) Hand-assisted 67 66.2 17.6 9 (13) 9 (13) Mets: 9 (13) 2 (3) laparoscopic Waldert et al. (80) Open Laparoscopic 59 68.46 41 16 (27) 13 (22) CFS: 76 CSS: 80 Mets: - 43 65.56 41 11 (26) 5 (12) 7 (12) CFS: 79 CSS: 85 Mets: 5 (11) Ziaee et al. (81) Laparoscopic NU 22 64.1 36.57 3 (4) 2 (9) 3-yr OS: 95 1 (4.5) with open BCE 3-yr metastasis-free survival: 90 Gillan et al. (45) Laparoscopic 6 73.6 12 0 (0) - - - Endoscopic 12 75.2 2 Open 12 71.8 1 Hora et al. (82) Laparoscopic 12 71.3 25.7 1 (8.3) - Mets: 1 (8.3) - Pai et al. (83) Laparoscopic 59 67 58 9 (53) 8 (47) CSS: 80 - Agarwal et al. (18) Laparoscopic with Poly 6 64.2 12-30 2 (33.3) 0 (0) - - Loop ligation Hoe et al. (19) Laparoscopic with PolyLoop Ligation 76 71.5 Bladder RFS: 24.3 0 (0) - OS: 70.3 - Contralateral RFS 47.9: CSS: 84.7 Local RFS: 49.8 Bladder RFS: 59.6 MFS (metastasis-free Local RFS: 89.0 survival): 52.5 Contralateral RFS: 93.5 OS: 52.5 Metastasis-free survival: CSS: 47.9 73.5 Port-site metastasis: 0 (0) Carrion et al. (84) Laparoscopic 117 70 20 5 (14) 36 (30) CSS: 61 Progression-free 28 (24) survival: 52 Krabbe et al. (11) Laparoscopic with no 46 69.5 32.0 12 (26.1) 13 (28.3) Intravesical recurrence- transvesical bladder cuff free survival (IVR FS): 22 (18.0) Laparoscopic with 76 68.0 33 (43.4) 10 (13.2) 71.6 months transvesical bladder cuff Non-IVR FS: 120.0 CSS: 123.5 months IVR-FS: 82.5 months Non-IVR FS: 83.9 months CSS: 83.0 months Shigeta et al. (85) Laparoscopic 129 71 31.1 61 (47.3) - CSS: 29.5 months 31 (24.0) OS: 35.6 months Guo et al. (86) Laparoscopic with 2- 38 65.3 36.5 4 (10.5) 0 (0) CSS: 100 - micrometer continuous Bladder recurrence-free wave laser rate: 89 Extravesical recurrence-free rate: 100 Mets: 0 (0) Zou et al. (87) Laparoscopic one-port 6 57.2 18 0 (0) 0 (0) - - pneumovesicum Liu et al. (88) Open Laparoscopic 213 62.5 44 40 (18.8) Total Intravesical RFS: 79 52 60.2 6 (11.5) recurrence: Overall RFS: 47 - 109 (51.1) Mets: 71 (33.3) Total CSS: 63 recurrence: OS: 61 20 (38.5) Intravesical RFS: 88 Overall RFS: 59 Mets: 13 (25.0) CSS: 70 OS: 55 Bragayrac et al. (50) Transvesical 5 70 16.2 0 (0) - Mets: 1 (20) - laparoendoscopic single-site Lee et al. (89) Robotic-assisted 20 71 13.5 - 1 - - Khanna et al. (90) Robotic-assisted 3 69.3 17.8 0 (0) 0 (0) - - Ghazi et al. (17) Laparoscopic 8 65.3 12.1 3 (37.5) 1 (12.5) - - Vasdev et al. (91) Robotic-assisted 7 - 59 0 (0) - - - Lister technique Distal ureter in NU-Morriss et al. Review 588 is not fully excised and a ureteric stump left behind, the risk of recurrence is anywhere from 33-75%(7). Lughez- zani et al. reported a 1.25-1.45 times increased risk of cancer-specific mortality if the bladder cuff excision was omitted(8). Here we will review the various surgical techniques and current literature on the management of the distal ureter during nephroureterectomy. MATERIALS AND METHODS A Medline search of the literature including relevant ar- ticles up to March, 2020 was performed. Search terms included “nephroureterectomy”, “upper tract urothe- lial carcinoma”, “upper urinary tract carcinoma OR UTUC”, “open OR conventional OR ONU OR con- ventional”, “robotic-assisted nephroureterectomy OR RANU”, “laparoscop* OR LNU OR LRNU” and “min- imally-invasive nephroureterectomy”. Original articles, case series and review articles were included. RESULTS Approaches to the distal ureter Various approaches have been described as seen in Fig- ure 1. The standard practice is to remove the intramural ureter along with ureteric orifice (UO), and a cuff of bladder around the UO. Ideally, this is achieved by an en bloc removal of specimen after controlled occlusion of the UO. In a systemic review and meta-analysis of clinicopathologic factors associated with intravesical recurrence after RNU by Seisen et al(9) it was shown that there is significant risk of tumor recurrence in the dis- tal ureter and its orifice. Poorer cancer-specific survival and overall survival has been seen in patients who did not have a bladder cuff excision during their NU(10,11). The optimal approach to managing the distal ureter and bladder cuff has been controversial due to different techniques described. These techniques can be classi- fied as open (intravesical/transvesical approaches), en- doscopic or minimally-invasive approaches, with some techniques employing a combination of these(12). The open approach has been traditionally regarded as the gold standard(2). However, advances in minimally-inva- sive technology have enabled urologists to expand their armamentarium in managing the distal ureter. The chal- lenges of all these techniques are to remove the entire specimen en bloc, without tumour spillage, and to con- form to strict oncological principles in the least invasive way possible. Open excision (ONU) An open approach to the distal ureter is considered the gold standard for excision of the distal ureter and blad- der cuff. It is generally performed after the nephrecto- my is complete, occurring after either a laparoscopic or open procedure to dissect the kidney and ureter. The distal ureter may then be approached in two ways, ei- ther intravesically/transvesically or extravesically(13). The intravesical or transvesical approach begins with an anterior cystotomy to provide access to the bladder cuff, followed by dissection of the ureter. Once the contralat- eral ureteral orifice is identified, followed by a 5-10 mm circumferential excision around the ipsilateral ureteral orifice through the full thickness of the bladder. The in- tramural ureter is dissected until the proximal ureteral dissection is reached, allowing the specimen to be re- moved en bloc. Benefits to this technique include better visualisation of the contralateral ureter and intramural Study Approach Patients Mean age Complication Clavien Mean Mean length of Estimated blood and year to NU (N) (years) rate, no. (%) Classification operating hospital stay loss (mL) ≥ 3 (III-V) time (min) (days), range Chen et al. (73) Open with early 42 63 - 0 (0) 220.19 9.5 105.15 ligation of distal ureter Open with late ligation 43 67 0 (0) 215.73 10 110.12 of distal ureter Chiang et al. (37) Hand-assisted 98 67.54 - - 144 7.3 67 retroperitoneoscopic Transurethral bladder 110 65.2 173 8.8 86 cuff incision-assisted Fragkoulis et al. (38) Open 192 69.2 - - 143 7.1 - Transurethral resection/Pluck 186 68.7 115 6.9 Cormio et al. (42) Open with transurethral 13 64.7 1 (7.7) 0 (0) Open NU: 8.1 (5-10) - distal ureter balloon 108 occlusion before detachment Distal ureter and BCE: 21.3 Cormio et al. (43) Open with flexible 10 68.2 0 (0) - 113.4 6.5 (5-10) - cystoscope-assisted transurethral distal ureter balloon occlusion and detachment Geavlete et al. (44) Endoscopic pluck with 42 - 2 (4.8) - 15 - - bipolar plasma vaporisation Gillan et al. (45) Laparoscopic 6 73.6 0 (0) - 190 6.3 (4-8) 200 Endoscopic 12 75.2 0 (0) 180 7.1 (5-12) 180 Open 12 71.8 1 200 12 (7-19) 240 Pang et al. (51) Open 24 - - - 233 12.7 352.0 Transurethral 17 148.1 9.8 136.5 electrosurgery Transurethral endoscopic 17 126.5 9.9 141.0 two-micron thulium laser resection Table 2a. Contemporary (2009 – 2021) perioperative outcomes comparing endoscopic vs non-endoscopic approaches Distal ureter in NU-Morriss et al. Vol 18 No 6 November-December 2021 589 Review 590 Study Approach Patients Mean age Complication Clavien Classification Mean operating Mean length of Estimated and year to NU (N) (years) rate, no. (%) ≥ 3 (III-V) time (min) hospital stay blood loss (mL) (days), range Ariane et al. (52) Open 459 69.8 23 (5) 19 (4.1) 180 9 (7-12) - Laparoscopic 150 69.5 9 (6) 7 (4.6) 240 8 (6-12) Blackmur et al. (53) Open 13 67.5 4 (30.8) 2 (15.4) 194 10 (5-29) - Laparoscopic 13 68.0 3 (23.1) 0 (0) 191 7 (3-10) Eandi JA et al. (54) RALNU 11 67.4 - - 326 4.7 200 Favaretto RL Open 109 71 - - 164 5 (4-6) 250 et al. (56) Laparoscopic 53 73 265 3 (3-4) 200 Hemal et al. (34) Robotic 15 66.27 0 (0) - 183.87 2.73 (2-5) 103 -assisted Lim et al. (57) Robotic- 32 66.5 7 (28.1) 2 (6.2) 250.1 6.2 263 assisted Park et al. (58) Laparoscopic 101 66.4 6 (5.9) 1 (1.0) 221.4 6.3 231.7 Wang et al. (61) Open 72 66.1 - - 148.5 7.3 286.1 Laparoscopic 86 68.7 133.2 5.5 176.3 Simone et al. (63) Open 40 61.3 0 (0) - 78 3.65 (3-5) 430 Laparoscopic 40 59.6 82 2.3 (2-3) 104 Greco et al. (64) Open 70 67.2 - 240 - - 190 Laparoscopic 70 66.4 - Kamihira et al. (65) Laparoscopic 1003 68.6 93 (9.3) - 320 - 232 Kitamura et al. (66) Open 34 69 5 (15) - 286 14.5 (5-36) 475 Hand- 9 65 2 (22) 325 17 (9-24) 250 assisted laparoscopic Laparoscopic 65 70 7 (11) 327 10 (4-62) 220 Lee et al. (92) Laparoscopic 10 62.79 4 (40) - 225.63 4.75 187.50 Lim et al. (67) Robotic- 38 66.5 10 (25.0) 2 (5.3) 249 6.0 264 assisted Pugh et al. (68) Robotic- 43 68.3 6 (14) - 247 3 (2-87) 131 assisted Trudeau et al. (93) Laparoscopic 735 70.6 134 (18.2) - - 5.83 - Robotic- 715 70.7 85 (11.9) 5.6 assisted Yang et al. (69) Robotic- 20 70.1 0 (0) - 251.6 6.7 (4-12) 50.0 assisted Hanske et al. (94) Minimally- 599 71 77 (12.9) - 160 (26.7) > 282 mins 137 (22.9) > 6 days - invasive (laparoscopic + robotic-assisted) Open 297 69 37 (12.5) 66 (22.2) > 282 mins 135 (45.5) > 6 days - Stewart et al. (71) Open 39 68.1 - 5 (12.8) 180 10 (5-29) 398 Laparoscopic 23 67.4 1 (4.3) 165 7 (2-30) 280 Ambani et al. (72) Robotic- 22 70.1 8 (36.4) 1 (5) 298 3.1 380 assisted Laparoscopic 22 70.8 6 (27.3) 1 (5) 251 3.1 233 Badani et al. (33) Robotic- 26 66 0 (0) - 230 2 (1-15) 66 assisted Chen et al. (73) Open with 42 63 - 0 (0) 220.19 9.5 105.15 early ligation of distal ureter Open with late 43 67 0 (0) 215.73 10 110.12 ligation of distal ureter Hu et al. (74) Robotic- 18 70.4 - - 255.17 6.79 (3.7-12) 68.89 assisted Hand-assisted 197 67.7 250.17 9.61 (4-26) 358.33 laparoscopic Kim et al. (39) Hand- 28 68 5 (17.9) - 240 8 (5-10) 250 assisted retroperitoneoscopic Lambert et al. (75) Laparoscopic 22 65.6 4 - 227 3.5 (1-13) 158 Liu et al. (76) Laparoscopic 31 66.8 0 (0) - 146.6 6 (4-8) 47.3 Mak et al. (77) Laparoscopic 10 71.6 1 (10) - 7.5 10.2 (6-16) Minimal Ritch et al. (27) Open 10 68 1 (10) - 276 3.5 (2-6) 163 Laparoscopic 14 70 1 (7) 152 2.7 (2-7) 209 stapling Laparoscopic 12 71 1 (8) 163 2.0 (1-3) 112 resection and suturing Shoma et al. (78) Laparoscopic 13 50 3 (23.1) - 226 7 233 Song et al. (79) Hand- 67 66.2 1 - 243.5 8.1 - assisted laparoscopic Waldert et al. (80) Open 59 68.46 2 (3) - 212 13.8 (9-16) 542 Laparoscopic 43 65.56 1 (2) 220 8.1 (7-9) 300 Table 2b. Contemporary (2009 – 2021) perioperative outcomes comparing ONU vs minimally-invasive NU Distal ureter in NU-Morriss et al. Vol 18 No 6 November-December 2021 591 Study Approach Patients Mean age Complication Clavien Classification Mean operating Mean length of Estimated and year to NU (N) (years) rate, no. (%) ≥ 3 (III-V) time (min) hospital stay blood loss (mL) (days), range Ziaee et al. (81) Laparoscopic 22 64.1 2 (9) - 216 4.3 314 NU with open BCE Gillan et al. (45) Laparoscopic 6 73.6 0 (0) - 190 6.3 (4-8) 200 Endoscopic 12 75.2 0 (0) 180 7.1 (5-12) 180 Open 12 71.8 1 200 12 (7-19) 240 Hora et al. (82) Laparoscopic 12 71.3 1 (8.3) - 164.9 9.3 150.0 Pai et al. (83) Laparoscopic 59 67 2 (3) 2 (3) 194.4 3.4 125 Agarwal et al. (18) Laparoscopic 6 64.2 0 (0) - 27 - Minimal with PolyLoop ligation Hoe et al. (19) Laparoscopic 76 71.5 23 (30.3) 3 (3.9) 258 6 (3-23) - with PolyLoop Ligation Guo et al. (86) Laparoscopic 38 65.3 1 (2.6) - 126 9.6 (5-20) 69.4 with 2-micrometer continuous wave laser Zou et al. (87) Laparoscopic 6 57.2 0 (0) - 114 8.2 (8-9) 89 one-port pneumovesicum Bragayrac et al. (50) Transvesical 5 70 2 (40) 0 (0) 198 3.8 (2-8) 234 laparoendoscopic single-site Roslan et al. (95) Transvesical 5 57.4 1 (20) - 59 5.2 (4-9) 54 laparoendoscopic single-site Vasdev et al. (91) Robotic- 7 - - 0 (0) 241.4 3 (3-7) 101.9 assisted Lister technique Lee et al. (89) Robotic- 20 71 2 (10) 0 (0) 161.3 3 (1-16) 98.8 assisted Won Lee et al. (96) Robotic- 68 56 3 (4.4) - 219 4.5 (1-16) 319 assisted Khanna et al. (90) Robotic- 3 69.3 1 - 300 3.3 183 assisted Ghazi et al. (17) Laparoscopic 8 65.3 1 (12.5) - 157 10.2 (7-15) - Figure 1. Overview of techniques used to manage the distal ureter during nephroureterectomy Distal ureter in NU-Morriss et al. ureter and enabling visual confirmation of excision of the bladder cuff. The anterior cystostomy is then closed in two layers. However, there is increased morbidity and longer patient recovery time due to an additional low abdominal incision and cystotomy. This technique should be avoided in patients with bladder urothelial carcinoma, as there is a risk of tumour seeding into the extravesical space(14). The extravesical approach involves mobilisation of the distal ureter down to its insertion into the bladder, se- curing the bladder cuff with a right-angle clamp, and excising the intramural ureter along with its cuff in a similar 5-10 mm circumferential excision. The speci- men is then removed en bloc. Compared to the transves- ical approach, there is a shorter patient recovery time due to the lack of additional surgical incisions required (14). However, there is the potential for damage to the contralateral ureter and incomplete excision of the dis- tal ureter and bladder cuff due to poorer access and vis- ualisation of the intramural ureter and bladder cuff(3). Endoscopic excision The distal ureter can also be approached endoscopically using the pluck technique, also referred to as transure- thral resection/excision of the ureteral orifice, or intus- susception, also known as the stripping technique. The pluck technique begins prior to nephrectomy, where the ureteral orifice and bladder cuff is endoscop- ically circumscribed and resected with a Collins knife or resectoscope through the intramural portion of the ureter into the perivesical fat(15). Following nephrecto- my and after dissecting the ureter, the distal ureter is detached or ‘plucked’ from its attachment to the blad- der, and removed along with the whole specimen(16). An issue with this technique includes the potential for locoregional tumour recurrence following spillage of tumour cells from an unclamped ureter into the perives- ical space. Other issues include fluid shifts due to usage of bladder irrigant and the potential for incomplete re- section of the ureter if remnant ureter remains follow- ing plucking. The pluck technique is therefore contrain- dicated in patients with distal ureteral tumours(17). To minimise the risk of tumour seeding, early coagulation of the ureteral orifice before dissecting the bladder cuff and early ligation of the ureter before nephroureterecto- my recommended. Agarwal et al.(18) and Hoe et al.(19) suggest a novel mod- ification to this pluck technique called the Agarwal loop-ligation technique involving endoscopic loop liga- tion in a bid to occlude the ureter. Following dissection of the distal ureter and bladder cuff with the Collins knife, a PolyLoop placed around the ureteric stump to ligate and occlude the distal ureter, preventing urine spillage from the upper tract. Complete excision of dis- tal ureter is ensured as the distal end is marked with the detachable loop. The distal ureteral stump is ligated prior to detaching the ureter or exposing the perivesi- cal fat, providing protection against urine spillage into perivesical space. The distal ureter is then dissected by dividing the periureteric adhesions with a Collins knife. Although the outcomes of this technique were only an- alysed in a small series of 6 patients, no perioperative complications were present and with no perivesical tu- mour recurrence reported in the short-term. The intussusception technique takes place following nephrectomy. The ureter is dissected as distally as pos- sible. Then, a bulb-tipped ureteric catheter (Chevassu catheter) is inserted past the resected and open end of the ureter. It is then folded over on itself and sutured in place. After resecting the intramural ureter and ure- teral orifice endoscopically, the catheter is pulled out, bringing the intussuscepted ureter with it, thus allowing for the entire distal ureter to be removed. The patient is transferred into a lithotomy position to allow for tran- surethral access and the catheter is pulled inward, caus- ing intussusception of the distal ureter into the bladder. Excision is facilitated with a resectoscope(13). Issues with this technique include inadequate removal of the distal ureter following stripping and the risk of tumour spillage into the perivesicle space, much like the pluck technique(17). Contraindications to this technique are similar to the pluck technique, mainly urothelial carci- noma involving the distal ureter as there is a higher like- lihood of incomplete resection with a positive margin. Additionally, patients with duplicated ureters, ureteral strictures, prior ureteral surgery, and prior radiation should undergo a different strategy to excise the bladder cuff and distal ureter(13). Minimally-invasive excision Laparoscopic and robotic-assisted techniques comprise the minimally-invasive methods of managing the distal ureter, and are regarded as the contemporary counter- parts to ONU. In both, early ligation of the ureter during nephrectomy is performed to prevent tumour seeding to the bladder. Earlier works warned about the risk of retroperitoneal metastasis and tumour spillage or port site recurrences(20,21). EAU recommends that minimal- ly-invasive techniques are contraindicated for invasive or large (T3/T4 and/or N+/M+) tumours given worse oncological outcomes(2). Precautions suggested to low- er the risk of tumour spillage include avoiding opening the urinary tract and avoiding direct contact between instruments and the tumour. In addition, avoiding mor- cellation of the tumour using an Endobag for tumour extraction and en bloc removal of the kidney and ureter with the bladder cuff is suggested to ensure the proce- dure is in carried out in a closed system(2).In modern practice however large tumours can still be managed in a minimally invasive fashion. The first laparoscopic NU was described by Clayman et al. in 1991(22), prompting a new age of minimally-inva- sive techniques to be applied to the treatment of UTUC. The laparoscopic approach to the distal ureter and BCE can include a transvesical approach using a cystoscopic secured detachment and ligation method (CDL), or it can involve an extravesical approach using a laparo- scopic stapling device with the stapling technique being associated with suboptimal oncologic outcomes(23). Laparoscopic nephroureterectomy can be performed transperitoneally or retroperitoneally depending on sur- geon preference, with retroperitoneal nephroureterecto- my having the advantages of reducing bowel mobiliza- tion, reducing the risk of visceral injury and reducing the risk of ileus. In addition, if tumor spillage present, it would be confined to the extraperitoneal space(24). The pure laparoscopic technique involves either extravesi- cal stapling of the distal ureter or complete laparoscopic dissection of ureter and bladder cuff and suture closure of the bladder defect(25,26). However, the pure laparo- scopic technique is more difficult to perform and port site seeding has been reported(21). The laparoscopic ex- travesical stapling approach has been associated with remnant ureteric orifice present post-excision in 50% Review 592 Distal ureter in NU-Morriss et al. of the cases(27). Robotic-assisted NU(28-30) is being increasingly utilised, with the aim of having equivalent oncological results to open surgery whilst limiting perioperative morbidity and minimising the technical challenges of laparoscop- ic surgery. It is less technically challenging than lapa- roscopic NU given the extra degrees of freedom and ar- ticulation of the robotic platform. Multiple reports(31-34) have been published documenting the perioperative feasibility and safety of the robotic approach as well as encouraging early oncologic outcomes. However, there is a dearth of long-term oncological outcomes fol- lowing robotic-assisted NU. Early experience with this modality(35) as reported in 2008 involved patient reposi- tioning and robot redocking throughout the procedure. However, innovations in this field have eliminated the need for this. Hemal et al.(34) was the first to describe a technique of robotic-assisted NU with BCE without requiring intraoperative patient repositioning or redock- ing of the robot. This technique allows for a seamless transition from upper tract to lower tract surgery with- out the need to reposition the patient or re-dock the robot. The three ports are strategically placed to allow access to the kidney, ureter, and bladder. After divid- ing the renal vascular structures, the ureter is clipped, though not divided. The ureter is then dissected distally as much as possible. In cases of ureteric tumours, wide dissection of the ureter is carried out to avoid a positive margin or entry into the ureter. Lymphadenectomy is also carried out. Bladder stay sutures are placed lateral to the ureterovesical junction to prevent retraction of the bladder once the bladder cuff is excised. It was reported that all fifteen patients were operated on successfully without perioperative complications, no positive surgi- cal margins present and with no recurrences detected in the short-term. Zargar et al.(32) describes a similar technique for robot- ic-assisted NU where there is also no need for patient repositioning or robot redocking. The approach to BCE involves dissecting the detrusor muscle until there is tenting of the bladder mucosa, followed by placement of lateral and medial 2-0 Vicryl polyglactin sutures. Following circumferential excision of the bladder cuff, the two sutures are tied together to close the bladder de- fect and ensure watertight closure. Another difference with this approach is port placement where the ports are all placed along the lateral rectus muscle to combine maximum accessibility for the nephrectomy portion of the surgery and further enabling pelvic access to facili- tate proper bladder cuff dissection. There were no major complications in the thirty-one patients included in this series. NU using a three-arm robotic approach cannot only provide the surgeon with a more feasible approach for performing the operation, but also provides for a less expensive operation. Comparing oncological and perioperative outcomes of endoscopic techniques with non-endoscopic techniques 17 studies were found that assessed oncological out- comes of endoscopic versus non-endoscopic tech- niques, as can be seen in Table 1a. The largest study found was a retrospective analysis of 2681 patients undergoing an open transvesical, open extravesical or endoscopic approach by Xylinas et al.(36), finding that the endoscopic approach was associated with higher rates of intravesical recurrence (34.1%) compared to the other two approaches (21.4% and 20.3%). As dis- cussed previously, this lends credence to the issue of tu- mour spillage associated with the endoscopic approach. Interestingly, no differences in non-bladder recurrence and survival were seen between the approaches. Other large studies that compared endoscopic and non-endo- scopic approaches such as Kapoor et al.(7) found that in 820 patients, open intravesical excision was associ- ated with lower intravesical recurrence in comparison to endoscopic and extravesical approaches. On the other hand, Li et al.(40) analysed 301 patients and found that there was no statistically significant difference in recurrence-free and cancer-specific survival between endoscopic and non-endoscopic techniques. Allard et al.(48) found similar recurrence and metastasis rates in 110 patients who underwent either open or endoscopic approaches, with Lai et al.(46) also finding comparable intravesical recurrence rates, along with no statistical- ly significant differences in cancer-specific and over- all survival. Novel endoscopic approaches such as that described by Geavlete et al.(44) involving a variation of the pluck technique using bipolar plasma vaporisation found intravesical recurrences in 14% of patients. 8 studies were found that assessed perioperative out- comes of endoscopic versus non-endoscopic approach- es as can be seen in Table 2a. Endoscopic approaches are generally associated with better perioperative out- comes, including shorter operating times, length of stay and less blood loss as can be seen in Table 3a. Fragkou- lis et al.(38) collected data from 378 patients and found the endoscopic approach had a lower mean operating time of 115 minutes versus the open approach of 143 minutes. In another study, Gillan et al.(45) compared laparoscopic, endoscopic and open approaches, con- cluding that the endoscopic approach had the shortest mean operating time and estimated blood loss. Similar- ly, Pang et al.(51) found that operating time, length of stay and blood loss were lower in the endoscopic group compared with the open approach. Comparing oncological and perioperative outcomes of open with minimally-invasive techniques 51 studies were found that assessed oncological out- comes of open versus minimally-invasive techniques, as can be seen in Table 1b. Ariane et al.(52) found a higher cancer-specific survival and reduced metastasis rate in those who underwent a laparoscopic versus an open approach. However, in an analysis of 159 patients Blackmur et al. did not find significant difference in 5-year survival between these two approaches. This was also seen with Fairey et al.(55), with no significant differ- ence in overall survival seen between the two groups. Although Favaretto et al.(56) also found similar rates of cancer-specific and recurrence-free survival, there was a reduced number of intravesical recurrences seen in the laparoscopic (9.3%) versus the open group (31.5%). However, Walton et al.(59) found there to be no signif- icant difference in non-bladder recurrence between the two groups. A meta-analysis by Piszczek et al.(97) also concluded that laparoscopic and open NU have com- parable oncological outcomes, with no statistically sig- nificant difference present among any of the measured oncological outcomes (cancer-specific survival, overall survival, intravesical recurrence-free survival, recur- rence-free survival). Novel minimally-invasive techniques like the Agarw- al PolyLoop Ligation Technique(19) has been shown to Distal ureter in NU-Morriss et al. Vol 18 No 6 November-December 2021 593 be oncologically valid in the long-term, with no cases of intravesical recurrence detected, and cancer-specific and overall survival comparable to other studies seen in the table. Moschini et al.(98) compared oncological outcomes of laparoscopic versus open approaches using a propen- sity matching analysis approach, concluding that there is no difference in oncological efficacy (overall recur- rence and cancer-specific mortality) between the two approaches. Another systematic review of open versus laparoscopic NU by Peyronnet et al.(99) concluded that there are worse cancer-specific survival and overall sur- vival in patients who have locally advanced high-risk that have underwent laparoscopic NU compared to open NU. However, in another systematic review and me- ta-analysis between open and laparoscopic NU, Liu et al. (100) found that there was no significant difference in oncological and perioperative outcomes between the two techniques, but did note a longer mean operative time in those that underwent laparoscopic NU. Nouralizadeh et al. (101) performed a meta-analysis comparing oncological and perioperative outcomes of open, laparoscopic, and hand-assisted laparoscopic NU, finding that the three techniques had comparable onco- logical outcomes, but with laparoscopic and hand-as- sisted laparoscopic NU having better perioperative out- comes when compared with open surgery. It was also found that a laparoscopic approach was associated with a longer operative time. Looking at a perioperative standpoint as can be seen in Table 2b, minimally-invasive techniques are on aver- age associated with a higher mean operating time but with less blood loss. As seen in table 3b, Ariane et al.(52), Favaretto et al.(56), Wang et al.(61), Greco et al.(64), Kita- mura et al.(66) and Hanske et al.(94) report higher mean operating times versus open approaches. Favaretto et al. (56), Wang et al.(61), Simone et al.(63), Kitamura et al.(66), Waldert et al.(80) and Gillan et al.(45) found lower esti- mated blood loss with minimally-invasive approaches versus open procedures. Trudeau et al.(93) retrospective- ly analysed robotic-assisted NU vs laparoscopic NU and found that they perioperative complication rate for robotic-assisted NU was lower versus laparoscopic NU. In a systematic review by Mullen et al.(102) comparing open versus laparoscopic versus robotic-assisted NU, laparoscopic techniques were similarly found to be on- cologically comparable to open NU but with improved perioperative outcomes (estimated blood loss and length of hospital stay). The paucity of high-quality ev- idence surrounding the use of robotic-assisted NU was noted and therefore no conclusions with respect to this modality could be drawn. However, estimated blood loss and hospital length of stay tend to be lower in the minimally-invasive groups versus the open approach. A similar 2019 systematic review and meta-analysis of over 87,000 patients by Veccia et al.(103) sought to com- pare robotic-assisted NU with other techniques (includ- ing open, laparoscopic and hand-assisted laparoscopic NU), also noting the lack of high quality data surround- ing this topic and was unable to conclude the best tech- nique for NU. They concluded that the techniques an- alysed in the review are all oncologically-valid, with more long-term oncologic data needed surrounding robotic-assisted NU. Additional approaches to NU Kidney-sparing surgery (KSS) is utilised for low-risk UTUC, as opposed to radical NU for high-risk dis- ease. This is since radical NU significantly reduces the nephron mass by at least 50%, predisposing the patient to chronic kidney disease and associated increased risk of cardiovascular events, morbidity, and mortality. KSS has been shown to have comparable oncological outcomes compared to radical NU in low-risk disease (104,105), and as a result the European Association of Urol- ogy(2) recommends this modality for all low-risk patients irrespective of the status of the contralateral kidney, and in select patients with CKD or that have a solitary kid- ney(106). Low-risk disease (localised, non-metastatic dis- ease) is defined as having all of the following features: unifocal disease, tumor size less than 2 cm, low-grade cytology, low-grade URS biopsy and no invasive aspect on CT urography. An important point to note when of- fering KSS is that the patient must be willing to undergo repeated and stringent surveillance follow-up including upper tract imaging, flexible cystoscopy, ureteroscopy, and urine cytology(106). CONCLUSIONS Although endoscopic approaches have more favoura- ble perioperative outcomes, this comes at the expense of increased risk of tumour spillage and recurrence compared to the traditional open approaches. Minimal- ly-invasive techniques (laparoscopic and robotic-assist- ed NU) largely have superior perioperative outcomes versus their open NU counterparts, with comparable oncological outcomes. The majority of studies found were retrospective studies. 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