Distal Ureter Management During Nephroureterectomy: Evidence from a Systematic Review and Cumulative Analysis

Abstract

Introduction and Objectives:

Standard of care in upper tract urothelial cancer is nephroureterectomy with bladder cuff excision (BCE). However, alternative techniques such as transurethral incision/resection have been used to simplify distal ureterectomy. The optimum strategy is unclear, and current guidelines do not specify a gold standard technique. The objective of this study was to perform a systematic review of the literature, to compare BCE and transurethral distal ureter methods.

Materials and Methods:

A Cochrane and PRISMA-guided systematic literature search was conducted on English language articles from January 2000 to present, reporting on centers’ experience with either BCE or transurethral distal ureterectomy. A cumulative meta-analysis comparison between the two procedures was performed. Primary outcome was intravesical recurrence. Secondary outcomes were local/distant recurrence, surgical margins, and disease-specific mortality (DSM). Groups were compared using chi-square analysis.

Results:

In total, 66 studies were included after excluding 1795. BCE and transurethral groups contained 6130 and 1183 patients, respectively. Mean/median age ranged from 57.5 to 75.2 years, and follow-up from 6.1 to 78 months. Level of evidence was low, with high risk of bias and small sample size (<100 patients) in 41 (62%) and 52 (79%) studies, respectively. Baseline cancer demographic analysis identified significantly higher rates of high grade, advanced stage, node-positive and carcinoma in situ disease in the BCE group. However, intravesical recurrence (23.6% vs 28.7%, p = 0.0002) and local/distant recurrence (17.9% vs 21.6%, p = 0.02) were significantly lower than the transurethral group. No difference was seen regarding surgical margins (3.1% vs 2.4%, p = 0.27) or DSM (16.8% vs 14.3%, p = 0.06).

Conclusions:

No prospective, randomized comparisons exist for distal ureterectomy at nephroureterectomy. In this analysis, patients undergoing BCE had more advanced disease burden compared with the transurethral group. Despite this, the BCE group had statistically lower intravesical and local/distant recurrence. Further prospective research should be encouraged to identify gold standard ureter management.

Introduction

Upper urinary tract urothelial cancer (UTUC) is a rare disease that accounts for less than 5% of urothelial tumors, with an annual incidence ranging from 0.8 to 1.7 cases per 100,000 people.¹ The disease remains lethal in modern times with 48% 5-year survival.¹ UTUC can arise anywhere from the renal calyces to the distal ureter, and given this, bladder urothelial carcinoma recurrence is common, occurring in 15% to 50% of patients after treatment.²

Management of UTUC remains challenging, with the current standard of care nephroureterectomy with bladder cuff excision (BCE) for patients with a normal contralateral kidney.³ Complete excision of the ureter to the level of the bladder is thought to be important, as a retained ureteral segment after incomplete nephroureterectomy may act as a possible site for local recurrence and may contribute to bladder recurrences or metastases.³

A number of alternative techniques for the management of the distal ureter have been used to simplify distal ureter management, and their use varies from center to center.⁴ This includes transurethral, endoscopic distal ureter management, in the form of intramural ureteral resection, that is, the Pluck method, or circumferential excision of the ureteral orifice. The optimal method of distal ureter management is unclear, and no specific method is recommended in current guidelines from the EAU.³

No randomized, prospective clinical trial has been performed, comparing BCE and transurethral distal ureter techniques, with oncologic outcomes varying in retrospective series.⁵ Given the variability in the use of BCE among centers and the uncertainty of the optimum distal ureteral technique, we performed a systematic review of the contemporary literature and cumulative analysis, to assess oncologic outcomes for patients undergoing BCE vs transurethral distal ureter management.

Materials and Methods

Search strategy and study selection

A PRISMA-guided systematic literature search was conducted for contemporary English language articles from January 2000 to September 2017, using the Medline, PubMed, and Cochrane Library. The MeSH term “nephroureterectomy” and variations thereof, including “nephro-ureterectomy” “ureteronephrectomy,” and “uretero-nephrectomy,” with Boolean operators, were used to refine the search.

Studies report on outcomes following nephroureterectomy in adult patients with nonmetastatic UTUC. Studies had to comply with the following inclusion criteria: report on the primary outcome, that is, bladder recurrence, utilize either BCE or transurethral distal ureter management, and a minimum of 10 participants.

Randomized clinical trials as well as prospective or retrospective nonrandomized comparative studies and noncomparative series reporting on outcomes in ≥10 patients were included in this systematic review. If two or more studies reported outcomes of overlapping series (i.e., by the same surgical team), the one with the greater sample size was selected.

The primary outcome was intravesical recurrence. Secondary outcomes were other recurrence (local [nonintravesical], lymph nodes or distant metastases), positive margins, and disease-specific mortality (DSM).

Data extraction and analysis

Data from all selected studies were independently extracted by two authors (S.M.L. and A.M.) and subsequently cross-checked by the senior author to ensure accuracy. A standardized data extraction form was created and used to collect the following variables extracted from each study: tumor location, tumor stage, tumor grade, presence of carcinoma in situ (CIS), nodal status, positive surgical margins, intravesical (bladder) recurrence, other recurrence (local, lymph nodes, or metastases), and DSM. Where DSM was not directly reported, DSM was back subtracted from living patients based on reported follow-up.

Articles included in the study were assessed for risk of bias (RoB) using two domains of the Quality in Prognosis Studies (QUIPs) tool, relevant to observational studies: study participation and outcome measurement. The risk was graded as low, medium, or high independently by two authors. In case of discrepancies, the senior author was involved in the decision process. If an item of the domain was not fulfilled, the risk was ranked as moderate; if two or more items were not fulfilled, the risk was deemed as high. If the risk ranks of the two domains were discordant, the worst rank was used to summarize RoB for the series.

Data were collected using Excel 2013 (Microsoft Corporation, Redmond, WA) and analyzed using SPSS (version 20; IBM, Armonk, NY). Continuous variables were described using mean and standard deviation, or alternatively, median and interquartile range. Chi-square test was used to compare variables. Statistical significance was defined as p < 0.05.

Results

Literature search

After removal of duplicates, two authors independently screened the titles and abstracts of the records for eligibility. Full texts of 163 eligible studies were retrieved and screened independently by two authors. Any disagreement was resolved by consulting the senior author (O.A.). According to the above mentioned criteria, 66 studies were deemed relevant for this systematic review. A PRISMA flowchart describing the study selection process is presented in Figure 1.

FIG. 1.

Flowchart of article selection process for review.

Characteristics of included studies

Overall, the 66 studies enrolled 7313 patients: 6130 with a mean age of 69.8 years in the BCE and 1183 with a mean age of 70 years in the transurethral groups.^{6

–71} The BCE group consisted of 51 studies, while the transurethral group had 25 studies. Only 10 studies directly compared BCE and transurethral distal ureter techniques. The majority of reports had small sample sizes, with only 14 studies having greater than 100 patients included. Mean/median follow-up varied greatly between studies. Mean/median follow-up ranged from 6.1 to 78 months, across all studies. For each group, follow-up ranged from 6.1 to 78 months in the BCE group and 8 to >60 months in the transurethral group.

Patient characteristics for the studies comprising the BCE and transurethral groups are summarized in Tables 1 and 2, respectively. Within both groups, variables, including nephroureterectomy technique (open or minimally invasive), tumor grade, tumor stage, and tumor location, were well reported in 73% to 100% of studies. However, possible confounders, including previous bladder cancer, CIS, and nodal status, were poorly reported, with only 45%, 22%, and 49% of studies in the BCE group and 36%, 16%, and 52% of studies in the transurethral group reporting on these variables, respectively.

Table 1.

Patient Characteristics of Studies Included in Bladder Cuff Excision Group

Author	Distal ureter, Mx	Follow-up, months	Pts, n	Age, years ± SD (range)	Male, n (%)	Open, n (%)	G3/HG, n (%)	Stage T2–T4, n (%)	Renal or pelvis tumor, n (%)	Prev. BCa, n (%)	CIS, n (%)	N+, n (%)	+ve Margins, n (%)	IV Recur, n (%)	Other recur, n (%)	DSM, n (%)
Aboumohamed et al.⁶	Robotic	Med. 25.1	65	Mean 69.1 ± 11.1	44 (68)	0 (0)	51 (78)	32 (49)	22 (34)	8 (12)	8 (12)	7 (11)	5 (8)	15 (23)	13 (20)	20 (31)
Ambani et al.⁸	Robotic	Med. 10	22	Mean 70.1 ± 2.2	14 (64)	0 (0)	—	10 (45)	14 (64)	—	—	—	2 (9)	8 (36)	7 (32)	2 (9)
Badani et al.¹⁰	Robotic	Med. 7.8	26	Med. 66 (57–89)	18 (69)	0 (0)	—	17 (65)	—	—	—	2 (8)	0 (0)	4 (15)	0 (0)	0 (0)
Cannon et al.¹¹	Open intravesical	Med. 13.9	34	Mean 70.3 ± 10.6	—	0 (0)	—	18 (53)	—	—	—	—	0 (0)	8 (24)	2 (6)	2 (6)
Chen et al.¹²	Open (Early ligation)	Med. 28	85	Med. 67 (37–82)	58 (68)	85 (100)	54 (64)	63 (74)	56 (66)	0 (0)	—	19 (22)	0 (0)	21 (25)	5 (6)	0 (0)
Chen et al.¹²	Open (Late ligation)	Med. 28	85	Med 63 (42–81)	58 (68)	85 (100)	54 (64)	63 (74)	56 (66)	0 (0)	—	19 (22)	0 (0)	21 (25)	5 (6)	0 (0)
Chiang et al.¹³	Open extravesical	Med. 26.7	98	Mean 67.5 ± 10.5	44 (45)	0 (0)	83 (85)	42 (43)	68 (69)	20 (20)	—	—	0 (0)	26 (27)	26 (27)	6 (6)
Chung et al.¹⁴	Open extravesical (Transabdominal cohort)	Med. 47.5	48	Mean 66	26 (54)	0 (0)	22 (46)	23 (48)	11 (23)	—	1 (2)	—	—	20 (42)	12 (25)	5 (10)
Chung et al.¹⁴	Open extravesical (Retroperitoneal cohort)	Med. 32	25	Mean 70	14 (56)	0 (0)	11 (44)	12 (48)	7 (28)	—	0 (0)	—	—	9 (36)	6 (24)	2 (8)
Eandi et al.¹⁷	Robotic	Mean 15.2	10	Mean 67.4	8 (80)	0 (0)	—	4 (40)	—	4 (40)	1 (10)	0 (0)	0 (0)	2 (20)	2 (20)	2 (20)
Fang et al.¹⁸	Open extravesical	Med. 30.8	36	Mean 65.1 ± 11.3	—	36 (100)	—	—	—	—	—	—	0 (0)	8 (22)	3 (8)	0 (0)
Fang et al.¹⁸	Laparoscopic	Med. 22.4	29	Mean 65.1 ± 11.3	—	29 (100)	—	—	—	—	—	—	0 (0)	11 (38)	4 (14)	1 (3)
Favaretto et al.¹⁹	Open extravesical	Med. 23	112	Med. 72	—	112 (100)	68 (61)	55 (49)	—	37 (33)	28 (25)	7 (6)	0 (0)	51 (46)	0 (0)	0 (0)
Fragkoulis et al.²⁰	Open	—	192	Med. 69.2	125 (65)	192 (100)	129 (67)	100 (52)	127 (66)	0 (0)	—	21 (11)	—	46 (24)	0 (0)	50 (26)
Giannakopoulos et al.²³	Laparoscopic transvesical	Med. 31	10	Mean 67.8	—	2 (20)	1 (10)	3 (30)	—	—	—	—	0 (0)	3 (30)	2 (20)	2 (20)
Gill et al.²⁴	Open extravesical	Mean 34.4	35	Mean 68.3	—	30 (86)	16 (46)	11 (31)	—	—	—	1 (3)	5 (14)	11 (31)	4 (11)	9 (26)
Gillan et al.²⁵	Open	Med. 12	12	Mean 71.8 ± 8.3	9 (75)	0 (0)	4 (33)	6 (50)	0 (0)	—	—	—	0 (0)	1 (8)	—	—
Gillan et al.²⁵	Laparoscopic	Med. 12	6	Mean 73.6 ± 6.4	6 (100)	0 (0)	2 (33)	3 (50)	0 (0)	—	—	—	0 (0)	0 (0)	—	—
Hattori et al.²⁶	Open extravesical (Open cohort)	Med. 35	60	Mean 65.5 ± 11.2	48 (80)	60 (100)	23 (38)	38 (63)	28 (47)	5 (8)	—	7 (12)	0 (0)	24 (40)	16 (27)	13 (22)
	Open extravesical (Lap cohort)	Med. 31	36	Mean 66.9 ± 10.6	23 (64)	0 (0)	13 (36)	15 (42)	13 (36)	4 (11)	—	5 (14)	0 (0)	12 (33)	10 (28)	7 (19)
	Laparoscopic stapling	Med. 17	53	Mean 67.1 ± 10.2	34 (64)	0 (0)	18 (34)	21 (40)	25 (47)	5 (9)	—	7 (13)	0 (0)	20 (38)	8 (15)	10 (19)
Hattori et al.²⁷	Laparoscopic	Med. 19	10	—	—	0 (0)	—	7 (70)	6 (60)	1 (10)	—	0 (0)	0 (0)	1 (10)	3 (30)	1 (10)
Hou et al.³⁰	Open	Med. 43.8	192	Mean 69.8 (43–89)	79 (41)	147 (77)	179 (93)	110 (57)	97 (51)	—	—	—	0 (0)	57 (30)	32 (17)	—
Hsueh et al.³¹	Open intravesical (Open cohort)	Mean 35.1	87	Mean 66.6 (44–83)	43 (49)	43 (49)	—	34 (39)	—	—	—	—	0 (0)	8 (9)	9 (10)	0 (0)
Hsueh et al.³¹	Open intravesical (Lap cohort)	Mean 16	58	Mean 66.6 (44–83)	25 (43)	0 (0)	—	29 (50)	—	—	—	—	0 (0)	5 (9)	6 (10)	0 (0)
Hu et al.³²	Open	Med. 47.8	18	Mean 67.7 ± 10.6	5 (28)	0 (0)	15 (83)	9 (50)	10 (56)	—	—	2 (11)	0 (0)	6 (33)	4 (22)	3 (17)
Hu et al.³²	Robotic	Med. 6.1	18	Mean 70.4 ± 6.3	5 (28)	0 (0)	17 (94)	10 (56)	10 (56)	—	—	1 (6)	0 (0)	2 (11)	4 (22)	1 (6)
Kapoor et al.³³	Open intravesical	Med. 24.6	406	Mean 69.2 ± 10.5	—	201 (50)	261 (64)	204 (50)	205 (50)	—	105 (26)	26 (6)	39 (10)	77 (19)	8 (2)	—
Kapoor et al.³³	Extravesical stapling	Med. 24.6	316	Mean 69.9 ± 11.3	—	166 (53)	206 (65)	189 (60)	170 (54)	—	76 (24)	25 (8)	32 (10)	66 (21)	5 (2)	—
Kim et al.³⁴	Open extravesical	—	28	Mean 68.2 (51–81)	26 (93)	0 (0)	12 (43)	18 (64)	12 (43)	1 (4)	—	—	0 (0)	6 (21)	0 (0)	0 (0)
Klinger et al.³⁵	Open intravesical	—	34	Mean 66 (24–90)	16 (47)	15 (44)	11 (32)	12 (35)	20 (59)	6 (18)	—	5 (15)	0 (0)	1 (3)	1 (3)	1 (3)
Koda et al.³⁶	Open (Open cohort)	Mean 24	27	Mean 67.4 ± 11.3	18 (67)	27 (100)	8 (30)	13 (48)	15 (56)	8 (30)	—	—	0 (0)	9 (33)	0 (0)	0 (0)
Koda et al.³⁶	Open (Lap cohort)	Mean 24	79	Mean 71.4 ± 8.2	62 (78)	0 (0)	36 (46)	32 (41)	37 (47)	20 (25)	—	—	0 (0)	22 (28)	0 (0)	0 (0)
Lambert et al.³⁸	Extravesical ligasure	Med. 20	22	Mean 65.6 (38–84)	14 (64)	0 (0)	—	7 (32)	16 (73)	0 (0)	—	—	0 (0)	3 (14)	2 (9)	0 (0)
Li et al.⁴⁰	Open intravesical	Med. 33	81	Mean 65.4 (23–87)	33 (41)	77 (95)	49 (60)	56 (69)	25 (31)	0 (0)	—	—	0 (0)	19 (23)	12 (15)	15 (19)
Li et al.⁴⁰	Open extravesical	Med. 39	129	Mean 65.4 (23–87)	63 (49)	102 (79)	66 (51)	73 (57)	43 (33)	0 (0)	—	—	0 (0)	31 (24)	23 (18)	17 (13)
Lim et al.⁴¹	Robotic	Med. 45.5	32	Med. 66.5 (43–83)	22 (69)	0 (0)	26 (81)	10 (31)	16 (50)	—	—	—	1 (3)	10 (31)	14 (44)	7 (22)
Liu et al.⁴²	Robotic	Med. 10.5	31	Mean 66.8 (53–77)	19 (61)	0 (0)	10 (32)	15 (48)	22 (71)	—	—	—	0 (0)	0 (0)	0 (0)	0 (0)
Mak et al.⁴³	Laparoscopic intravesical	Med. 46	10	Mean 71.6 (47–82)	9 (90)	0 (0)	2 (20)	7 (70)	6 (60)	—	—	—	0 (0)	4 (40)	1 (10)	0 (0)
Matin and Gill⁴⁴	Extravesical stapling	Med. 19	12	Med. 73 (53–91)	—	0 (0)	7 (58)	7 (58)	5 (42)	7 (58)	—	0 (0)	3 (25)	5 (42)	5 (42)	4 (33)
Nakashima et al.⁴⁵	Open (Open cohort)	Med. 56	37	Med. 70.9 ± 7.1	28 (76)	37 (100)	13 (35)	—	18 (49)	5 (14)	—	—	0 (0)	21 (57)	3 (8)	7 (19)
Nakashima et al.⁴⁵	Open (Lap cohort)	Med. 23	36	Med. 70.9 ± 7.1	24 (67)	0 (0)	18 (50)	—	14 (39)	11 (31)	—	—	0 (0)	12 (33)	4 (11)	4 (11)
Oehlschlager et al.⁴⁶	Open	Mean 40.4	29	Mean 69.5 (39–84)	—	26 (90)	17 (59)	17 (59)	—	0 (0)	—	0 (0)	2 (7)	11 (38)	3 (10)	3 (10)
Okegawa et al.⁴⁷	Open	Med. 24.3	48	Mean 66	30 (63)	23 (48)	13 (27)	25 (52)	27 (56)	6 (13)	—	0 (0)	0 (0)	9 (19)	5 (10)	—
Ou and Yang⁴⁸	Open	Med. 39.7	61	Mean 68.6	34 (56)	0 (0)	28 (46)	32 (52)	60 (98)	0 (0)	—	0 (0)	—	18 (30)	7 (11)	—
Ritch et al.⁵⁰	Open intravesical	Med. 16	10	Mean 69.6	7 (70)	0 (0)	6 (60)	5 (50)	—	—	—	2 (20)	3 (30)	2 (20)	0 (0)	0 (0)
	Extravesical stapling	Med. 21	14		11 (79)	0 (0)	8 (57)	7 (50)	—	—	—	1 (7)	1 (7)	2 (14)	2 (14)	2 (14)
	Laparoscopic	Med. 7	12		5 (42)	0 (0)	2 (17)	3 (25)	—	—	—	0 (0)	2 (17)	0 (0)	0 (0)	0 (0)
Romero et al.⁵¹	Open	Mean 39.2	12	Mean 68.3 (56–85)	—	12 (100)	10 (83)	9 (75)	12 (100)	0 (0)	6 (50)	—	0 (0)	4 (33)	1 (8)	0 (0)
Romero et al.⁵¹	Extravesical stapling	Mean 54.5	12	Mean 65.6 (51–84)	—	0 (0)	10 (83)	7 (58)	12 (100)	0 (0)	5 (42)	—	3 (25)	6 (50)	5 (42)	0 (0)
Roupret et al.⁵²	Open (Open cohort)	Med. 78	26	Mean 71.1 ± 6.5	—	26 (100)	19 (73)	15 (58)	—	—	—	5 (19)	0 (0)	4 (15)	10 (38)	8 (31)
Roupret et al.⁵²	Open (Lap cohort)	Med. 68.5	20	Mean 68.5 ± 7.3	—	0 (0)	8 (40)	5 (25)	—	—	—	1 (5)	0 (0)	2 (10)	2 (10)	2 (10)
Saika et al.⁵³	Open	Med. 42	32	Mean 65.2	23 (72)	32 (100)	8 (25)	19 (59)	—	—	0 (0)	—	0 (0)	7 (22)	6 (19)	7 (22)
Salvador-Bayarri et al.⁵⁴	Open	Med. 44	87	Med 64 (40–89)	—	87 (100)	48 (55)	45 (52)	—	—	9 (10)	—	0 (0)	34 (39)	0 (0)	0 (0)
Shalhav et al.⁵⁶	Open	Mean 43	17	Mean 62 (28–84)	11 (65)	17 (100)	13 (76)	12 (71)	—	—	—	0 (0)	0 (0)	6 (35)	3 (18)	3 (18)
Shoma⁵⁷	Laparoscopic	Med. 31.5	13	—	10 (77)	0 (0)	4 (31)	6 (46)	12 (92)	—	—	—	0 (0)	2 (15)	1 (8)	1 (8)
Simone et al.⁵⁸	Open	Med. 44	40	Mean 61.3 (52–70)	26 (65)	40 (100)	13 (33)	28 (70)	13 (33)	—	—	0 (0)	0 (0)	9 (23)	6 (15)	4 (10)
Simone et al.⁵⁸	Extravesical ligasure		40	Mean 59.6 (48–71)	24 (60)	0 (0)	12 (30)	20 (50)	16 (40)	—	—	0 (0)	0 (0)	10 (25)	11 (28)	8 (20)
Song et al.⁵⁹	Laparoscopic	Mean 17.6	67	Mean 66.2 ± 10.6	45 (67)	0 (0)	—	33 (49)	30 (45)	6 (9)	—	4 (6)	1 (1)	9 (13)	9 (13)	2 (3)
Taweemonkongsap et al.⁶⁰	Open (Open cohort)	Mean 27.9	29	Mean 66.8 (39–88)	22 (76)	29 (100)	19 (66)	16 (55)	10 (34)	13 (45)	—	3 (10)	0 (0)	13 (45)	3 (10)	2 (7)
Taweemonkongsap et al.⁶⁰	Open (Lap cohort)	Mean 26.4	31	Mean 63.8 (26–79)	11 (35)	0 (0)	13 (42)	15 (48)	14 (45)	11 (35)	—	1 (3)	0 (0)	9 (29)	5 (16)	3 (10)
Tsivian et al.⁶¹	Extravesical ligasure	Med. 11.6	13	Mean 64.5 (47–84)	10 (77)	0 (0)	6 (46)	8 (62)	8 (62)	—	3 (23)	—	0 (0)	2 (15)	0 (0)	0 (0)
Tsujihata et al.⁶²	Open (Open cohort)	Med. 22.1	24	Mean 68.3 (50–87)	14 (58)	24 (100)	5 (21)	6 (25)	14 (58)	—	—	—	0 (0)	8 (33)	2 (8)	2 (8)
Tsujihata et al.⁶²	Open (Lap cohort)	Med. 22.4	25	Mean 66.6 (34–85)	19 (76)	0 (0)	12 (48)	13 (52)	18 (72)	—	—	—	0 (0)	7 (28)	0 (0)	0 (0)
Waldert et al.⁶⁴	Open (Open cohort)	Mean 41	59	Mean 65.6 ± 12.3	40 (68)	59 (100)	24 (41)	30 (51)	33 (56)	15 (25)	—	4 (7)	0 (0)	16 (27)	13 (22)	0 (0)
Waldert et al.⁶⁴	Open (Lap cohort)		43	Mean 68.5 ± 9.3	21 (49)	0 (0)	18 (42)	23 (53)	23 (53)	13 (30)	—	7 (16)	0 (0)	11 (26)	5 (12)	11 (26)
Walton et al.⁶⁵	Open	Med. 39	48	Mean 68.3 ± 1.4	30 (63)	48 (100)	19 (40)	21 (44)	9 (19)	—	5 (10)	0 (0)	1 (2)	23 (48)	0 (0)	6 (130
Xylinas et al.⁶⁸	Open	Med. 57.5	1811	—	1208 (67)	1533 (85)	1511 (83)	953 (53)	1152 (64)	555 (31)	471 (26)	174 (10)	—	388 (21)	526 (29)	419 (23)
Xylinas et al.⁶⁸	Extravesical stapling	Med. 57.5	785	—	546 (70)	624 (79)	682 (87)	472 (60)	508 (65)	193 (25)	189 (24)	82 (10)	—	160 (20)	204 (26)	175 (22)
Yang et al.⁶⁹	Robotic	Mean 14.7	20	Mean 70.1 ± 9.9	6 (30)	0 (0)	19 (95)	12 (60)	12 (60)	—	—	—	0 (0)	3 (15)	4 (20)	1 (5)
Yoshino et al.⁷⁰	Extravesical stapling	Mean 15	23	Mean 66.7 (44–83)	15 (65)	0 (0)	9 (39)	9 (39)	10 (43)	—	—	—	0 (0)	4 (17)	2 (9)	2 (9)
Ziaee et al.⁷¹	Extravesical stapling	Mean 36.5	22	Mean 64.1 (52–83)	18 (82)	0 (0)	4 (18)	10 (45)	19 (86)	—	—	—	0 (0)	3 (14)	2 (9)	2 (9)

CIS = carcinoma in situ; DSM = disease-specific mortality.

Table 2.

Patient Characteristics of Studies Included in the Transurethral Group

Author	Distal ureter, Mx	Follow-up, months	Pts, n	Age, years ± SD (range)	Male, n (%)	Open, n (%)	G3/HG, n (%)	Stage T2–T4, n (%)	Renal or pelvis tumor, n (%)	Prev. Bca, n (%)	CIS, n (%)	N+, n (%)	+ve Margins, n (%)	IV Recur, n (%)	Other eecur, n (%)	DSM, n (%)
Agarwal et al.⁷	TCIUO with endoloop ligation	Med. 15.3	13	Mean 68.3 (45–88)	8 (62)	0 (0)	6 (46)	5 (38)	8 (62)	—	—	—	0 (0)	5 (38)	—	1 (8)
Araki et al.⁹	TCIUO	Med. 41	10	Mean 69 (49–83)	5 (50)	0 (0)	8 (80)	7 (70)	8 (80)	—	—	0 (0)	0 (0)	2 (20)	1 (10)	1 (10)
Chiang et al.¹³	TCIUO	Med. 26.7	110	Mean 65.2 ± 10.8	58 (53)	0 (0)	98 (89)	47 (43)	89 (81)	25 (23)	—	—	0 (0)	32 (29)	22 (20)	9 (8)
Cormio et al.¹⁵	TCIUO	Mean 39.8	13	Mean 68.2 (43–87)	8 (62)	13 (100)	9 (69)	8 (62)	6 (46)	2 (15)	—	2 (15)	0 (0)	4 (31)	0 (0)	—
Cormio et al.¹⁶	TCIUO	Med. 31.1	10	Mean 64.7 (56–80)	7 (70)	10 (100)	7 (70)	3 (30)	6 (60)	—	—	0 (0)	0 (0)	2 (20)	0 (0)	0 (0)
Fragkoulis et al.²⁰	Pluck	>60	186	Med. 68.7	123 (66)	186 (100)	130 (70)	102 (55)	125 (67)	0 (0)	—	22 (12)	—	50 (27)	—	47 (25)
Geavlete et al.²¹	Pluck	Med. 44	72	Mean 57.5	—	72 (100)	—	—	—	—	—	—	0 (0)	17 (24)	—	9 (13)
Geavlete et al.²²	Pluck with bipolar vaporization	Mean 14	42	—	—	42 (100)	—	16 (38)	34 (81)	—	—	—	0 (0)	6 (14)	2 (5)	2 (5)
Gillan et al.²⁵	TCIUO	Med. 12	12	Mean 75.2 ± 7.2	8 (67)	0 (0)	4 (33)	6 (50)	0 (0)	—	—	—	1 (8)	2 (17)	0 (0)	—
Hayashi et al.²⁸	TCIUO	Med. 24.9	28	Mean 67 (51–81)	18 (64)	8 (29)	13 (46)	20 (71)	11 (39)	—	—	2 (7)	0 (0)	9 (32)	3 (11)	2 (7)
Hora et al.²⁹	Pluck	Mean 25.7	11	Mean 71 (54–81)	6 (55)	0 (0)	2 (18)	7 (64)	9 (82)	1 (9)	—	—	0 (0)	1 (9)	1 (9)	2 (18)
Kapoor et al.³³	Pluck or TCIUO	Med. 24.6	98	Mean 70.0 ± 11.0	—	15 (15)	58 (59)	51 (52)	57 (58)	—	12 (12)	3 (3)	10 (10)	23 (23)	69 (70)	—
Kurzer et al.³⁷	TCIUO	Med. 10	41	Mean 67	—	0 (0)	22 (54)	15 (37)	30 (73)	6 (15)	—	4 (10)	0 (0)	20 (49)	6 (15)	1 (2)
Landman et al.³⁹	Pluck following ureter stapling	Med. 9.6	16	Mean 65	13 (81)	1 (6)	5 (31)	4 (25)	—	—	—	—	0 (0)	2 (13)	3 (19)	—
Li et al.⁴⁰	TCIUO	Med. 30	91	Mean 65.4 (23–87)	35 (38)	67 (74)	56 (62)	50 (55)	37 (41)	0 (0)	—	—	0 (0)	16 (18)	10 (11)	9 (10)
Matin and Gill⁴⁴	Pluck	Med. 22	36	Med. 73 (53–91)	—	0 (0)	23 (64)	14 (39)	24 (67)	6 (17)	—	4 (11)	1 (3)	5 (14)	5 (14)	—
Pai et al.⁴⁹	TCIUO	Med. 58	46	Mean 67 ± 10.3	38 (83)	0 (0)	33 (72)	25 (54)	23 (50)	—	—	3 (7)	3 (7)	9 (20)	8 (17)	9 (20)
Salvador-Bayarri et al.⁵⁴	Pluck	Med. 44	58	Med 64 (40–89)	—	58 (100)	32 (55)	31 (53)	—	—	11 (19)	—	0 (0)	20 (34)	—	—
Sesmero et al.⁵⁵	TCIUO	Med. 22.2	14	Mean 59.5 (35–70)	11 (79)	3 (21)	9 (64)	4 (29)	12 (86)	—	—	—	0 (0)	1 (7)	1 (7)	0 (0)
Shalhav et al.⁵⁶	Pluck	Mean 24	25	Mean 69.7 (50–87)	14 (56)	0 (0)	13 (52)	13 (52)	—	—	—	0 (0)	0 (0)	3 (12)	5 (20)	3 (12)
Ubrig et al.⁶³	Pluck	Med. 33	17	Mean 63.4 (21–94)	—	—	8 (47)	6 (35)	16 (94)	6 (35)	—	1 (6)	0 (0)	5 (29)	1 (6)	3 (18)
Walton et al.⁶⁵	Pluck	Med. 46	90	Mean 67.1 ± 1.4	57 (63)	90 (100)	19 (21)	29 (32)	47 (52)	—	12 (13)	2 (2)	3 (3)	49 (54)	—	16 (18)
Wolf et al.⁶⁶	Pluck or TCIUO	Med. 25.8	45	Mean 69.7 ± 10.5	0 (0)	—	—	—	—	—	—	—	4 (9)	26 (58)	—	—
Wong and Leveillee⁶⁷	TCIUO	Med. 8	14	—	—	0 (15)	—	—	—	—	—	—	0 (0)	2 (14)	0 (0)	0 (0)
Xylinas et al.⁶⁸	Pluck or TCIUO	Med. 57.5	85	—	54 (64)	13	49 (58)	35 (41)	70 (82)	22 (26)	16 (19)	3 (4)	—	29 (34)	18	15 (18)

TCIUO = transurethral circumferential incision of the ureteral orifice.

No prospective studies on distal ureter management at time of nephroureterectomy are available, with only retrospective comparative studies and retrospective case series. As all studies were retrospective in nature, level of evidence was low. Overall, RoB was considered low in 12 studies, moderate in 13 studies, and high in the remaining 41 studies.

Comparison of baseline cancer demographics found significantly higher rates of G3/high grade and ≥T2 disease, node-positive disease, and CIS disease in the BCE group (Table 3). In addition, a significantly higher proportion of patients in the BCE group had previous bladder cancer (Table 3). Patients in the transurethral management group were more likely to have disease confined to the kidney and renal pelvis (Table 3). The data did not include information on prior endoscopic intervention for biopsy or a tubal prosthesis, that is, stent, before definitive nephroureterectomy.

Table 3.

Distal Ureteral Techniques Used Within the Bladder Cuff Excision and Transurethral Groups

Bladder cuff excision group
Open
Intravesical excision
Extravesical excision
Minimally invasive
Laparoscopic extravesical excision
Robot-assisted extravesical excision
Laparoscopic excision via transvesical ports
Extravesical bladder tenting
With endoscopic stapling
With ligasure
Transurethral group
Pluck
Transurethral resection of ureteral orifice
With or without early ureter ligation/clipping/stapling
Bipolar vaporization of ureteral orifice
Transurethral circumferential excision of ureteral orifice
Using Collins knife
With or without early ureter ligation/stapling

Distal ureteral management

Table 3 summarizes the primary techniques and variations utilized in each group. Distal ureter management in the BCE group studies was variable, using techniques ranging from traditional open intravesical, to completely minimally invasive, or extravesical tenting approaches. Within the BCE group, 4437 patients had a traditional open BCE, using either an intravesical (cystotomy) or extravesical approach. The remaining 1693 patients had a completely minimally invasive approach, with either robotic or laparoscopic BCE or extravesical tenting.

The transurethral detachment techniques were all variations on two main approaches: transurethral resection of the ureteral orifice, that is, the “Pluck” technique or transurethral circumferential incision of the ureteral orifice (TCIUO). The Pluck technique was performed through transurethral resection or bipolar vaporization of the UO, and in some studies, synchronous ligation, clipping, or stapling of the ureter were performed before transurethral management of the UO. TCIUO was performed using a Collins knife in all studies, with or without ureteral ligation or stapling.

Outcomes of distal ureteral management

For the primary and secondary outcome measurements, most available information concerned the number of patients with an event at time of follow-up. There was little time-to-event data, including hazard ratios, p-values, and multivariate adjustment. Therefore, the main analysis is based on a comparison of the overall percentage of patients with an event during follow-up. Data from each study were combined to obtain an overall estimate and compared using a Pearson chi-square test. Cumulative patient characteristics are shown in Table 4.

Table 4.

Cumulative Analysis of Distal Ureter Technique Patient Characteristics and Outcomes

Variable	Bladder cuff excision	Endoscopic management	p	Odds ratio (95% CI)
Sex (male)	3148/4944 (63.7)	463/805 (57.5)	0.0008^*	1.29 (1.11, 1.51)
Open surgery	3941/6130 (64.3)	578/1121 (51.6)	<0.00001^*	1.69 (1.49, 1.92)
G3/High grade	3991/5729 (69.7)	601/1010 (59.8)	<0.00001^*	1.54 (1.34, 1.77)
Stage ≥T2	3191/5992 (53.3)	498/1052 (47.3)	0.0004^*	1.27 (1.11, 1.45)
Renal pelvis tumor	3130/5446 (57.5)	612/953 (64.2)	0.0001^*	0.75 (0.65, 0.87)
Previous bladder cancer	954/4193 (22.8)	68/590 (11.5)	<0.00001^*	2.26 (1.74, 2.94)
CIS	907/3782 (24.0)	51/331 (15.4)	0.0005^*	1.73 (1.27, 2.36)
N1 disease	419/4678 (9.0)	46/685 (6.7)	0.05	1.37 (1.00, 1.87)
Positive surgical margins	100/3208 (3.1)	22/912 (2.4)	0.27	1.30 (0.82, 2.08)
Intravesical recurrence	1447/6130 (23.6)	340/1183 (28.7)	0.0002^*	0.77 (0.67, 0.88)
Local/Distant recurrence	1093/6112 (17.9)	155/719 (21.6)	0.02^*	0.79 (0.66, 0.96)
DSM	854/5089 (16.8)	129/905 (14.3)	0.06	1.21 (0.99, 1.48)

Significant p < 0.05.

Primary outcome measure

Intravesical recurrence was reported by all included studies in both groups. During follow-up, intravesical recurrence was significantly lower in the BCE group patients, 23.6%, vs the transurethral management group, 28.7% (p = 0.0002*, OR 0.77, 95% CI 0.67, 0.88).

Secondary outcome measures

In the BCE group, other recurrence (local or systemic) and DSM was reported in 98% and 90% of included studies, respectively, while in the transurethral group, these variables were published in 76% and 72%, respectively. Other recurrence was significantly lower in the BCE vs the transurethral group, 17.9% vs 21.6%, respectively (p = 0.02*, OR 0.79, 95% CI 0.66, 0.96). No difference between the two groups was seen for DSM (BCE 16.8% vs transurethral 14.3%, p = 0.06, OR 1.21, 95% CI 0.99, 1.48).

Positive surgical margins were reported in 92% and 92% of studies in the BCE and transurethral groups, respectively. There was no significant difference in positive margins between the BCE and transurethral groups: 3.1% vs 2.4% (p = 0.27, OR 1.30, 95% CI 0.82, 2.08).

Discussion

Summary of results

While the standard of care for UTUC is radical nephroureterectomy, current guidelines do not specify the ideal technique for management of the distal ureter.³ We performed a systematic review and cumulative analysis of the literature to assess contemporary (2000–2017) oncologic outcomes for UTUC patients undergoing nephroureterectomy with either BCE or transurethral distal ureter management.

We found that patients who underwent BCE had significantly higher rates of high grade (69.7% vs 59.8%; p < 0.0001) and staged (53.3% vs 47.3%; p = 0.0004) disease compared to the transurethral group, including higher rates of CIS (24% vs 15.4%; p = 0.0005). Despite having more advanced disease, results have shown significantly lower bladder recurrence rate (23.6% vs 28.7%; p = 0.0002) and distant recurrences (17.9% vs 21.6%, p = 0.02). There was no difference between the two groups regarding positive surgical margins (3.1% vs 2.4%; p = 0.27) or DSM (16.8% vs 14.3%, p = 0.06).

Comparison to the literature

The two largest studies within this systematic review came from two multicenter collaborations, by Kapoor and colleagues³³ and Xylinas and colleagues.⁶⁸ Both studies subdivided distal ureter techniques into intravesical BCE, extravesical tenting of the ureter without opening the bladder at another location, and transurethral techniques. The transurethral groups in both studies were comparatively small, representing only 12.0% (98/820) and 3.2% (85/2681) of patients, respectively. The Kapoor study found inferior recurrence-free survival for patients undergoing transurethral distal ureter management vs intravesical BCE (HR 1.488, p = 0.0424).³³ Similarly, Xylinas and colleagues reported higher intravesical recurrence rates in patients undergoing transurethral management (HR 1.74, p = 0.01). The results from both these reports are reflected in the higher intravesical recurrence rate seen in the transurethral group within this study.

Mortality

The population-based study by Lughezzani et al.⁵ analyzed the U.S. National Cancer Institute's Surveillance, Epidemiology, and End Results (SEER) database, comparing patients who underwent nephroureterectomy with or without BCE for DSM. The authors found 1.25- to 1.45-fold greater DSM when BCE was not performed in patient with pT3–4 N0/x or pT(any) N1–3 disease.

This increase in DSM was not seen in this review, and may be due, in part, to the wide variations in follow-up between the various included studies. However, taking this into consideration, the mortality rates of those studies with longer follow-ups for BCE vs transurethral treatment were compared: >36 months: 20.47% vs 19.45%; p = 0.06, OR 1.07, 95% CI 0.84, 1.35, >48 months follow-up: 22.5% vs 22.4%; p = 0.98, OR 0.1, 95% CI 0.76, 1.33, and for those with >60 months follow-up: 21.7% vs 25.3%; p = 0.62, OR 0.82, 95% CI 0.38, 1.78. With longer follow-up, it appears that DSM rates favor the BCE group.

In the short-term, the DSM rates are higher in the BCE group and may arise for a number of reasons. These results are interesting, particularly as local and systemic recurrences were lower in this same cohort. As previously discussed, the BCE group had higher disease burden vs the transurethral group. Furthermore, all included studies were retrospective, and the timing of patient mortality was not included in the studies. It is also unclear about the proportion of patients who underwent adjuvant or neoadjuvant chemotherapy before surgery. It is possible that those with the highest disease burden included in the BCE group died early in the follow-up, which would explain the higher early mortality, with similar mortality displayed on long-term follow-up. Some of these patients may have been unfit, denying the use of adjuvant chemotherapy following surgery.

Strengths and limitations of review

This systematic review comprehensively investigates the currently available contemporary (all articles published after 2000) literature and gives the best evidence regarding distal ureter management at time of nephroureterectomy to date. However, despite this, the quality of the evidence obtained was low. Studies were retrospective with no well-designed prospective studies with low RoB. Heterogeneity in study design, populations, and incomplete reporting of patient characteristics and outcome data limited the analyses that could be performed. Follow-up also varied from study to study, ranging from less than 1 year to greater than 5 years.

Finally, there was technique discrepancy in method of BCE within the group. A combination of open intra- and extravesical BCE was used along with minimally invasive techniques, including extravesical tenting and ligation. There is debate as to whether this extravesical tenting of the bladder followed by stapling, Ligasure or similar ligation of the UO and bladder cuff are equivalent to formal BCE. Indeed, larger cohort studies, including Kapoor and colleagues³³ and Xylinas and colleagues,⁶⁸ included these as a separate group. While Kapoor found significantly higher intravesical recurrence rates in the extravesical tenting group, no difference was seen in the Xylinas and colleagues cohort.

Nonetheless, this represents the existing evidence, based on a thorough, high-standard protocol-driven systematic review and analysis of the results.

Implications for practice and research

Although renal pelvic cancer is more common than distal ureteral disease, this study has found significantly more centers performing BCE as opposed to transurethral distal ureteral procedures. This emphasizes that although the evidence is not yet established, clinical intuition or practice has led to more surgeons moving away from transurethral management of the distal end at nephroureterectomy. Nonetheless, generally, this review found that BCE has better oncologic outcomes despite having more advanced disease. However, no difference in DSM was noted.

BCE had more advanced disease but better oncologic outcomes compared to transurethral management. We postulate that in patients with matching disease status, BCE will have better oncologic outcomes and potentially lower mortality.

Although this review is composed of low-grade evidence studies, it does highlight the current uncertainty and lack of high-level evidence in current guidelines regarding the optimum distal ureter technique at nephroureterectomy. There is a pressing need for further prospective, randomized studies to investigate the optimum distal ureter technique. Anecdotally, the increasing need for transurethral confirmation of urothelial carcinoma and the potential effects of manipulation and seeding from the upper tracts remains unquantified and must be documented as part of any future study.

Until such a trial is conducted, based on the evidence provided, we recommend that at time of nephroureterectomy, preference is given to BCE management of the distal ureter.

Conclusions

In this cumulative analysis, patients with BCE distal ureter management had more advanced disease burden compared to the transurethral group. Despite this, there was statistically lower bladder recurrences and local or distant recurrences. Further prospective research in this area should be encouraged to identify gold standard distal ureter management. Until then, we recommend BCE be considered the default technique with nephroureterectomy procedures.

Footnotes

Acknowledgment

The authors thank Dr. Isra Ashi for her support.

Author Disclosure Statement

No competing financial interests exist.

Abbreviations Used

References

Eylert

, Hounsome

, Verne

, Bahl

, Jefferies

, Persad

. Prognosis is deteriorating for upper tract urothelial cancer: Data for England 1985–2010. BJU Int, 2013; 112:E107–E113.

Azemar

, Comperat

, Richard

, Cussenot

, Roupret

. Bladder recurrence after surgery for upper urinary tract urothelial cell carcinoma: Frequency, risk factors, and surveillance. Urol Oncol, 2011; 29:130–136.

Roupret

, Babjuk

, Comperat

, et al. European Association of Urology guidelines on upper urinary tract urothelial carcinoma: 2017 Update. Eur Urol, 2018; 73:111–122.

Macejko

, Pazona

, Loeb

, Kimm

, Nadler

. Management of distal ureter in laparoscopic nephroureterectomy—A comprehensive review of techniques. Urology, 2008; 72:974–981.

Lughezzani

, Sun

, Perrotte

, 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; 57:956–962.

Aboumohamed

, Krane

, Hemal

. Oncologic outcomes following robot-assisted laparoscopic nephroureterectomy with bladder cuff excision for upper tract urothelial carcinoma. J Urol, 2015; 194:1561–1566.

Agarwal

, Khaira

, Clarke

, Tong

. Modified transurethral technique for the management of distal ureter during laparoscopic assisted nephroureterectomy. Urology, 2008; 71:740–743.

Ambani

, Weizer

, Wolf

Jr ., He

, Miller

, Montgomery

JS.

Matched comparison of robotic vs laparoscopic nephroureterectomy: An initial experience. Urology, 2014; 83:345–349.

Araki

, Lam

, Fetzer

, Clair

, Wong

. Tumor recurrence incidence following hand-assisted laparoscopic nephroureterectomy. JSLS, 2007; 11:449–452.

10.

Badani

, Rothberg

, Bergman

, et al. Robot-assisted nephroureterectomy and bladder cuff excision without patient or robot repositioning: Description of modified port placement and technique. J Laparoendosc Adv Surg Tech A, 2014; 24:647–650.

11.

Cannon

Jr ., Averch

, Colen

, Morrisroe

, Durrani

, Hrebinko

RL.

Hand-assisted laparoscopic nephroureterectomy with open cystotomy for removal of the distal ureter and bladder cuff. J Endourol, 2005; 19:973–975.

12.

Chen

, Ye

, Zhou

, et al. Clipping the extremity of ureter prior to nephroureterectomy is effective in preventing subsequent bladder recurrence after upper urinary tract urothelial carcinoma. Chin Med J (Engl), 2012; 125:3821–3826.

13.

Chiang

, Luo

, Chen

, Kang

, Chuang

, Lee

. Is hand-assisted retroperitoneoscopic nephroureterectomy better than transurethral bladder cuff incision-assisted nephroureterectomy?. J Endourol, 2011; 25:1307–1313.

14.

Chung

, Chueh

, Lai

, et al. Long-term outcome of hand-assisted laparoscopic radical nephroureterectomy for upper-tract urothelial carcinoma: Comparison with open surgery. J Endourol, 2007; 21:595–599.

15.

Cormio

, Selvaggio

, Di Fino

, et al. Transurethral distal ureter balloon occlusion and detachment: A simple means of managing the distal ureter during radical nephroureterectomy. J Endourol, 2013; 27:139–142.

16.

Cormio

, Selvaggio

, Di Fino

, et al. Simultaneous radical nephroureterectomy and transurethral distal ureter balloon occlusion and detachment. World J Surg Oncol, 2014; 12:345.

17.

Eandi

, Nelson

, Wilson

, Josephson

. Oncologic outcomes for complete robot-assisted laparoscopic management of upper-tract transitional cell carcinoma. J Endourol, 2010; 24:969–975.

18.

Fang

, Xiong

, Li

, et al. Pattern and risk factors of intravesical recurrence after nephroureterectomy for upper tract urothelial carcinoma: A large Chinese center experience. J Formos Med Assoc, 2014; 113:820–827.

19.

Favaretto

, Shariat

, Chade

, et al. Comparison between laparoscopic and open radical nephroureterectomy in a contemporary group of patients: Are recurrence and disease-specific survival associated with surgical technique?. Eur Urol, 2010; 58:645–651.

20.

Fragkoulis

, Pappas

, Papadopoulos

, Stathouros

, Fragkoulis

, Ntoumas

. Transurethral resection versus open bladder cuff excision in patients undergoing nephroureterectomy for upper urinary tract carcinoma: Operative and oncological results. Arab J Urol, 2017; 15:64–67.

21.

Geavlete

, Georgescu

, Bancu

, Mirciulescu

. Endoscopic ureteral procedures for one-step nephroureterectomy: Experience in 100 cases. J Endourol, 2007; 21:1019–1024.

22.

Geavlete

, Multescu

, Geavlete

, Georgescu

, Moldoveanu

. Bipolar plasma vaporization—An innovative intramural ureter detachment method during nephroureterectomy. J Med Life, 2012; 5:153–156.

23.

Giannakopoulos

, Toufas

, Dimitriadis

, et al. Laparoscopic transvesical resection of an en bloc bladder cuff and distal ureter during nephroureterectomy. ScientificWorldJournal, 2012; 2012:658096.

24.

Gill

, Sung

, Hobart

, et al. Laparoscopic radical nephroureterectomy for upper tract transitional cell carcinoma: The Cleveland Clinic experience. J Urol, 2000; 164:1513–1522.

25.

Gillan

, Alexander

, Townell

, Nabi

. Laparoscopic en bloc resection of ureter with a cuff of bladder during radical nephroureterectomy for lower ureteric tumors: A matched-paired analysis. J Laparoendosc Adv Surg Tech A, 2013; 23:626–631.

26.

Hattori

, Yoshino

, Gotoh

, Katoh

, Kamihira

, Ono

. Laparoscopic nephroureterectomy for transitional cell carcinoma of renal pelvis and ureter: Nagoya experience. Urology, 2006; 67:701–705.

27.

Hattori

, Yoshino

, Komatsu

, Matsukawa

, Ono

, Gotoh

. Pure laparoscopic complete excision of distal ureter with a bladder cuff for upper tract urothelial carcinoma. World J Urol, 2009; 27:253–258.

28.

Hayashi

, Tanaka

, Okutani

. Modified pluck method in en bloc nephroureterectomy with bladder cuff for upper urothelial cancer. Int J Urol, 2005; 12:539–543.

29.

Hora

, Eret

, Urge

, et al. Antegrade mini-invasive nephroureterectomy: Laparoscopic nephrectomy, transurethral excision of ureterovesical junction and lower abdominal incision. Urol Int, 2009; 83:264–270.

30.

Hou

, Chang

, Chen

, Lin

, Tsui

. Does adequate bladder cuff excision impact outcomes in patients undergoing nephroureterectomy for upper tract urothelial carcinoma. Chang Gung Med J, 2011; 34:496–505.

31.

Hsueh

, Huang

, Chiu

, Shen

, Lee

. A comparison of the clinical outcome between open and hand-assisted laparoscopic nephroureterectomy for upper urinary tract transitional cell carcinoma. BJU Int, 2004; 94:798–801.

32.

, Yang

, Huang

, et al. Robot-assisted laparoscopic nephroureterectomy versus hand-assisted laparoscopic nephroureterectomy for upper urinary tract urothelial carcinoma: A matched comparison study. Biomed Res Int, 2015; 2015:918486.

33.

Kapoor

, Dason

, Allard

, et al. The impact of method of distal ureter management during radical nephroureterectomy on tumour recurrence. Can Urol Assoc J, 2014; 8:E845–E852.

34.

Kim

, Kim

, Yoon

. Hand-assisted retroperitoneoscopic nephroureterectomy with bladder cuffing after preperitoneal and retroperitoneal perivesical ballooning. Korean J Urol, 2014; 55:29–35.

35.

Klingler

, Lodde

, Pycha

, Remzi

, Janetschek

, Marberger

. Modified laparoscopic nephroureterectomy for treatment of upper urinary tract transitional cell cancer is not associated with an increased risk of tumour recurrence. Eur Urol, 2003; 44:442–447.

36.

Koda

, Mita

, Shigeta

, Usui

. Risk factors for intravesical recurrence following urothelial carcinoma of the upper urinary tract: No relationship to the mode of surgery. Jpn J Clin Oncol, 2007; 37:296–301.

37.

Kurzer

, Leveillee

, Bird

. 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; 175:63–67; discussion 7–8.

38.

Lambert

, Schachter

, Altamar

, et al. A sealed bladder cuff technique during laparoscopic nephroureterectomy utilizing the LigaSure electrosurgical device: Laboratory and clinical experience. J Endourol, 2010; 24:327–332.

39.

Landman

, Lev

, Bhayani

, et al. Comparison of hand assisted and standard laparoscopic radical nephroureterectomy for the management of localized transitional cell carcinoma. J Urol, 2002; 167:2387–2391.

40.

, Shen

, Li

, et al. Oncologic outcomes following three different approaches to the distal ureter and bladder cuff in nephroureterectomy for primary upper urinary tract urothelial carcinoma. Eur Urol, 2010; 57:963–969.

41.

Lim

, Shin

, Kim

, et al. Intermediate-term outcomes of robot-assisted laparoscopic nephroureterectomy in upper urinary tract urothelial carcinoma. Clin Genitourin Cancer, 2013; 11:515–521.

42.

Liu

, Fang

, Xiong

, et al. A novel and simple modification for management of distal ureter during laparoscopic nephroureterectomy without patient repositioning: A bulldog clamp technique and description of modified port placement. J Endourol, 2016; 30:195–200.

43.

Mak

, Ng

, Chan

, Yip

, Cheng

, Wong

. Pneumovesicum approach to en-bloc laparoscopic nephroureterectomy with bladder cuff excision for upper tract urothelial cancer: Midterm oncological results. J Endourol, 2011; 25:611–614.

44.

Matin

, Gill

. Recurrence and survival following laparoscopic radical nephroureterectomy with various forms of bladder cuff control. J Urol, 2005; 173:395–400.

45.

Nakashima

, Fujiyama

, Tokuda

, et al. Oncologic assessment of hand-assisted retroperitoneoscopic nephroureterectomy for urothelial tumors of the upper tract: Comparison with conventional open nephroureterectomy. J Endourol, 2007; 21:583–588.

46.

Oehlschlager

, Baldauf

, Wiessner

, Gellrich

, Hakenberg

, Wirth

. Bladder tumor recurrence after primary surgery for transitional cell carcinoma of the upper urinary tract. Urol Int, 2004; 73:209–211.

47.

Okegawa

, Odagane

, Ide

, Horie

, Nutahara

, Higashihara

. Oncological outcome of retroperitoneoscopic nephroureterectomy for upper urinary tract transitional cell carcinoma. Int J Urol, 2006; 13:493–497.

48.

, Yang

. Impact of earlier ureteral ligation on intravesical recurrence during hand-assisted retroperitoneoscopic nephroureterectomy. Urol Int, 2014; 92:68–73.

49.

Pai

, Hussain

, Hindley

, Emara

, Barber

. Long term outcomes of laparoscopic nephro-ureterectomy with transurethral circumferential excision of the ureteric orifice for urothelial carcinoma. J Endourol, 2017; 31:651–654.

50.

Ritch

, Kearns

, Mues

, et al. Comparison of distal ureteral management strategies during laparoscopic nephroureterectomy. J Endourol, 2011; 25:1149–1154.

51.

Romero

, Schaeffer

, Muntener

, Trock

, Kavoussi

, Jarrett

. Oncologic outcomes of extravesical stapling of distal ureter in laparoscopic nephroureterectomy. J Endourol, 2007; 21:1025–1027.

52.

Roupret

, Hupertan

, Sanderson

, et al. Oncologic control after open or laparoscopic nephroureterectomy for upper urinary tract transitional cell carcinoma: A single center experience. Urology, 2007; 69:656–661.

53.

Saika

, Nishiguchi

, Tsushima

, et al. Comparative study of ureteral stripping versus open ureterectomy for nephroureterectomy in patients with transitional carcinoma of the renal pelvis. Urology, 2004; 63:848–852.

54.

Salvador-Bayarri

, Rodriguez-Villamil

, Imperatore

, Palou Redorta

, Villavicencio-Mavrich

, Vicente-Rodriguez

. Bladder neoplasms after nephroureterectomy: Does the surgery of the lower ureter, transurethral resection or open surgery, influence the evolution?. Eur Urol, 2002; 41:30–33.

55.

Sesmero

, Redondo

, Delgado

, Royo

, Tesedo

, Oceja

. Intravesical sealing of the distal ureter in nephroureterectomy. Arch Esp Urol, 2010; 63:223–229.

56.

Shalhav

, Dunn

, Portis

, Elbahnasy

, McDougall

, Clayman

. Laparoscopic nephroureterectomy for upper tract transitional cell cancer: The Washington University experience. J Urol, 2000; 163:1100–1104.

57.

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; 104:1505–1509.

58.

Simone

, Papalia

, Guaglianone

, et al. Laparoscopic versus open nephroureterectomy: Perioperative and oncologic outcomes from a randomised prospective study. Eur Urol, 2009; 56:520–526.

59.

Song

, Han

, Song

, Choo

, Ahn

, Hong

. Hand-assisted laparoscopic bladder cuff excision via the same hand port as that used for nephroureterectomy. World J Urol, 2015; 33:1459–1465.

60.

Taweemonkongsap

, Nualyong

, Amornvesukit

, 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.

61.

Tsivian

, Benjamin

, Sidi

. A sealed laparoscopic nephroureterectomy: A new technique. Eur Urol, 2007; 52:1015–1019.

62.

Tsujihata

, Nonomura

, Tsujimura

, Yoshimura

, Miyagawa

, Okuyama

. Laparoscopic nephroureterectomy for upper tract transitional cell carcinoma: Comparison of laparoscopic and open surgery. Eur Urol, 2006; 49:332–336.

63.

Ubrig

, Boenig

, Waldner

, Roth

. Transurethral approach to the distal ureter in nephroureterectomy: Transurethral extraction vs. “pluck” technique with long-term follow-up. Eur Urol, 2004; 46:741–747.

64.

Waldert

, Remzi

, Klingler

, Mueller

, Marberger

. 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.

65.

Walton

, Sherwood

, Parkinson

, et al. Comparative outcomes following endoscopic ureteral detachment and formal bladder cuff excision in open nephroureterectomy for upper urinary tract transitional cell carcinoma. J Urol, 2009; 181:532–539.

66.

Wolf

Jr ., Dash

, Hollenbeck

, Johnston

3rd , Madii

, Montgomery

JS.

Intermediate followup of hand assisted laparoscopic nephroureterectomy for urothelial carcinoma: Factors associated with outcomes. J Urol, 2005; 173:1102–1107.

67.

Wong

, Leveillee

. Hand-assisted laparoscopic nephroureterectomy with cystoscopic en bloc excision of the distal ureter and bladder cuff. J Endourol, 2002; 16:329–332; discussion 32–33.

68.

Xylinas

, Rink

, Cha

, et al. Impact of distal ureter management on oncologic outcomes following radical nephroureterectomy for upper tract urothelial carcinoma. Eur Urol, 2014; 65:210–217.

69.

Yang

, Chung

, Hung

, et al. Robot-assisted nephroureterectomy for upper tract urothelial carcinoma: The Taiwan Robot Urological Surgery Team (TRUST) experience. World J Surg Oncol, 2014; 12:219.

70.

Yoshino

, Ono

, Hattori

, Gotoh

, Kamihira

, Ohshima

. Retroperitoneoscopic nephroureterectomy for transitional cell carcinoma of the renal pelvis and ureter: Nagoya experience. Urology, 2003; 61:533–538.

71.

Ziaee

, Azizi

, Nouralizadeh

, Gooran

, Radfar

, Mirzaei

. Laparoscopic nephroureterectomy with concomitant open bladder cuff excision: A single center experience. Urol J, 2012; 9:652–656.