# Laparoscopic Nephroureterectomy and Management of the Distal Ureter: A Review of Current Techniques and Outcomes

Authors: Davis P. Viprakasit; Amanda M. Macejko; Robert B. Nadler
Journal: Advances in Urology
 (2009)

---

## Abstract

Laparoscopic nephroureterectomy (LNU) is becoming an increasingly common alternative treatment for transitional cell carcinoma (TCC) of the renal pelvis and ureter due to decreased perioperative morbidity, shorter hospitalization, and comparable oncologic control with open nephroureterectomy (ONU). Mobilization of the kidney and proximal ureter may be performed through a transperitoneal, retroperitoneal, or hand-assisted approach. Each technique is associated with its own benefits and limitations, and the optimal approach is often dictated by surgeon preference. Our analysis of the literature reflects equivalent cancer control between LPN and OPN at intermediate follow-up with significantly improved perioperative morbidity following LPN. Several methods for bladder cuff excision have been advocated, however, no individual technique for management of the distal ureter proved superior. Overall, complete en-bloc resection with minimal disruption of the urinary tract should be optimized to maintain oncologic outcomes. Longer follow-up and prospective studies are needed to fully evaluate these techniques.


---

## Body

## 1. Introduction

Transitional cell carcinoma (TCC) of  the renal pelvis and ureter is a disease associated with high
propensity for tumor recurrence and progression. Open radical nephroureterectomy (ONU) with bladder cuff excision is the traditional standard treatment for most localized diseases of the upper urinary tract because of its
aggressive nature, as well as the difficulty encountered with surveillance of the upper tract urothelium [1]. To obtain adequate exposure, open excision of the distal ureter and bladder cuff requires either two skin incisions or an extended flank incision. This is associated with increased perioperative
morbidity and recovery time. First described by Clayman et al. in 1991 [2], laparoscopic radical nephroureterectomy (LNU) has shown significant advantages in terms of blood loss, postoperative pain and recovery time, as well as comparable short and intermediate-term oncologic outcomes
with the open treatment [3]. As more urologists are gaining increased
comfort with minimally invasive techniques, LNU exhibits a large growth in worldwide popularity [4]. However, the optimal laparoscopic approach for nephroureterectomy as well as the technique for addressing the bladder cuff is unclear. We present a review of the most recent literature detailing the perioperative and cancer control outcomes observed with the various methods of LNU and discuss
the reported variations on bladder cuff excision.


## 2. Laparoscopic Nephroureterectomy

### 2.1. Approach

A variety of
techniques have been utilized to perform mobilization of the kidney and proximal
ureter. These include conventional transperitoneal, conventional
retroperitoneal, hand-assisted transperitoneal, and hand-assisted
retroperitoneal approaches. The choice of laparoscopic approach is most
dependent on the comfort level and training of the surgeon. However, each
technique has its own potential advantages. Transperitoneal exposure offers the
largest working area and may be beneficial for extensive tumors or
lymphadenopathy. The retroperitoneal approach, however, involves decreased
bowel manipulation and potentially allows for earlier recovery of bowel
function. Additionally, this method may be favored in morbidly obese patients
with an obstructing pannus or in patients with a history of previous
transperitoneal surgeries [5].
Hand-assistance techniques allow for continued tactile sensation and may
lessen the learning curve required in laparoscopy [6]. Most of the experiences with LNU are
primarily reported as single-institutional retrospective series. To date, there
have been no prospective randomized studies that compare the different
techniques for LNU. However, data published in the laparoscopic radical
nephrectomy literature may be applicable. For example, a randomized,
prospective study comparing conventional transperitoneal, retroperitoneal, and
hand-assisted transperitoneal laparoscopic radical nephrectomy was recently
published [7]. The hand-assisted technique resulted in a significantly
shorter operative time but an increased risk of hernia formation; conversely, conventional
transperitoneal surgery was associated with significantly improved
perioperative morbidity. Desai et al. reported shorter operative times and
faster control of the renal vasculature with retroperitoneal approaches in a
prospective randomized comparison of conventional transperitoneal and
retroperitoneal laparoscopic radical nephrectomy but no significant differences
in other perioperative measures [5].


### 2.2. Perioperative Outcomes

Rassweiler et al.
performed a literature review of published studies between 1991 and 2004 of LNU
and ONU, including nine comparative studies and 1365 overall patients [3]. As compared to ONU, LNU was associated with
a slightly longer operative time (277 versus 220 minutes), significantly lower
blood loss (241 versus 463 mL), and shorter hospital stays, but showed similar
complication rates (18% versus 21%).Table1 summarizes
the perioperative outcomes of 12 LNU studies published since 2005. The mean
operating time ranged from 165 to 395 minutes (mean 271) in the laparoscopic
group (n=465 patients), and 155 to 313 minutes (mean 237) in the open group
(n=268 patients). Significantly increased operative time with laparoscopy was
noted in three of eight comparative studies, all of which involved the
retroperitoneal approach. The blood loss averaged between 183 to 497 mL (mean
279) in the laparoscopic group as compared to a range of 296 to 558 mL (mean
402) in the open group. Significantly less blood loss after laparoscopy was
noted in four of eight comparative studies with a similar trend in three of the
remaining studies. The overall complication rate ranged from 0 to 37% (mean
18%) in the laparoscopy group and from 0 to 15% (mean 7%) in the open group.
The open conversion rate associated with laparoscopy ranged from 0 to 10%. The
absolute duration of hospital stays varied between institutions. Out of eight
comparative studies, hospitalization following laparoscopy was shorter in seven
series with a significant difference in five.Table 1
Perioperative characteristics of LPN versus ONU cases. CR, conventional retroperitoneal; CT, conventional
transperitoneal; HAT, hand-assisted transperitoneal; NL, not listed; ONU, open nephroureterectomy.
AuthorSurgeryNumberHigh grade (%)OR duration (min)Blood loss (min)Conversion (%)Complication (%)Hospital daysMuntener et al. [8]CT3931 (80)3123004 (10)12 (31)4Schatteman et al.
[9]CT10048 (48)1922347 (7)19 (19)10Rouprêt
et al. [10]CT208 (40)1652751 (5)3 (15)4ONU2619 (73)155338—4 (15)9Okegawa
et al. [11]CR256 (24)2992581 (4)4 (16)11ONU237 (30)313403—3 (13)13Tsujihata
et al. [12]CR255 (20)3063220 (0)0 (0)2ONU2412 (50)271558—0 (0)4Taweemonkongsap  et al.  [13]CR3113 (42)2592890 (0)2 (6)9.3ONU2919 (66)191314—2 (7)8.7Chung et al. [14]HAT3916 (41)2331830 (0)5 (13)7ONU3615 (42)220422—3 (8)9Raman  et al. [15]HAT3815 (40)2441910 (0)4 (11)5ONU5219 (37)243478—2 (4)7Wolf  et al. [16]HAT5326 (49)2793301 (2)20 (37)4Cannon  et al. [17]HAT34NL3172520 (0)9 (26)8Chung  et al. [18]HAR2511 (44)2522120 (0)3 (12)6.5ONU4117 (41)212408—3 (7)9Nakashima
et al. [19]HAR3618  (50)3954971 (3)11 (31)18.8ONU3713 (35)289296—2 (5)19.1


### 2.3. Oncologic Outcomes

The highly aggressive
natural history of upper tract TCC, particularly with high-grade and high-stage
disease, likely contributes to its increased potential for recurrence and poor
prognosis irrespective of the surgical technique. However, there are many
concerns that technical aspects of LNU, particularly with regard to management
of the distal ureter and bladder cuff, may affect recurrence risks in the bladder,
locally, or as port-site metastases secondary to tumor seeding. Rassweiler et
al. noted no significant difference in bladder recurrence (24% versus 25%),
local recurrence (4% versus 6%) and distant metastases (15.5% versus 15.2%) in
eight LNU series and 11 ONU series [3]. The 2-year cancer specific survival rates
were also similar (75% versus 76%).Table2 summarizes
the short and intermediate oncologic outcomes of 14 LNU studies published since
2005. The most common method for bladder cuff excision was an open approach. At
a minimum median follow-up of at least 2 years, bladder recurrence after LNU
(n=488 patients) ranged from 10 to 55% (mean 30%) as compared to 15 to 55%
(mean 33%) in the ONU series (n=512 patients). Local recurrence in the
retroperitoneum was documented as 0 to 13% (mean 3.3%) in the laparoscopic
(n=588 patients) and 0 to 8% (mean 2.5%) in the open series (n=512 patients).
Distant metastases occurred in 0 to 18% (mean 9.5%) of patients undergoing LNU
(n=588 patients) as compared to 5 to 35% (mean 14.5%) in the open series (n=512
patients). In six series reporting 2-year disease-specific survival, the rates
ranged from 64 to 91% (mean 83%) in the laparoscopic series (n=274 patients) and
between 58 to 93% (mean 83.6%) after ONU (n=242 patients). In the five series
reporting 5-year survival rates, the outcomes ranged from 68 to 90% (mean 85%)
after LNU (n=202 patients) and 62 to 86% (mean 75%) in the ONU groups (n=191
patients). There was no significant difference between LNU and ONU survival
rates in the 10 comparative studies. However, absolute comparisons between the
surgical approaches are difficult as the percentage of patients with high-grade
disease and the follow-up period varied considerably, reflecting a large
limitation with the retrospective nature of these studies. In addition, the inclusion
of patients with a prior or concomitant history of bladder cancer may affect
the oncologic outcome of treating upper tract TCC. In the 14 LNU studies, only
7 addressed this parameter in defining their patient characteristics. The 4
comparative studies including such patients and the 1 study which excluded
patients with bladder TCC did not show a significant difference between ONU and
LNU groups. However, it is unclear if the underlying biology and tumor
aggressiveness in patients with both upper and lower tract TCC differ
from patients with isolated upper tract TCC; inclusion of such patients in
studies with already relatively low numbers further complicates comparisons of treatment
approach.Table 2
Oncologic outcomes of LPN versus ONU
cases. CR, conventional retroperitoneal; CT,
conventional transperitoneal; HAR, hand-assisted retroperitoneal; HAT,
hand-assisted transperitoneal; LND, lymph node dissection; LS, laparoscopic
stapling; NL, not listed; ONU, open nephroureterectomy; SD, surgeon discretion; TURUO,
transurethral resection; TV, transvesical.
AuthorSurgeryNFollow up (mo)History of bladder tumor specifiedBladder cuff surgeryPath stage (Ta,Tis,T1/T2, T3,T4)Path grade (1/2/3)LNDUrothelial recurrence (%)Local recurrence (%)Port-site recurrence (%)Distal recurrence (%)Disease-specific survival (@ year)Muntener et al. [8]CT3974YesOpen (19), LS (13), other (5)22/15/2NL8LG/31HGNo16 (41)2 (5)0 (0)7 (18)68 (5)Schatteman et al. [9]CT/CR95/520NoOpen (55), Other (45)54/4624/28/4820% of casesNL13 (13)3 (3)16 (16)88 (2)Rouprêt  et al. [10]CT2069NoOpen15/511/1512LG/8HGSD2 (10)0 (0)0 (0)2 (10)90 (5)ONU26787LG/19HG4 (15)0 (0)9 (35)62 (5)Okegawa  et al. [11]CR2524YesOpen14/119/142/17/6No5 (20)0 (0)0 (0)2 (8)91 (2)ONU23291/15/74 (17)0 (0)3 (13)89 (2)Tsujihata  et al. [12]CR2522NoOpen12/1315/65/15/5No7 (28)0 (0)0 (0)0 (0)64 (2)ONU24220/11/128 (33)0 (0)2 (8)58 (2)Manabe  et al. [20]CR5814ExcludedOpen28/3070/964/31/23No19 (33)1 (2)1 (2)10 (17)85 (2)ONU1662815/87/6463 (38)2 (1)33 (20)87 (2)Taweemonkongsap  et al. [13]CR3126YesOpen16/1518LG/13HGSD9 (29)2 (6)0 (0)3 (10)86 (2)ONU292813/1610LG/19HG13 (45)1 (3)2 (7)93 (2)Chung  et al. [14]HAT3948NoOpen18/211/22/16SD17 (44)1 (3)0 (0)6 (15)90 (5)ONU366017/191/20/1513 (36)3 (8)4 (11)86 (5)Raman  et al. [15]HAT3832YesOpen (30),27/923LG/15HGNo11 (29)1 (3)0 (0)2 (6)81 (5)ONU5251TURUO (8)41/1133LG/19HG18 (35)0 (0)6 (11)77 (5)Wolf  et al. [16]HAT5325YesTURUO (23), TV (22), Open (6), LS
(2)38/1518/9/26SD(55)(8)0 (0)(16)80 (3)Cannon  et al. [17]HAT3414NoOpen17/18NLNo8 (24)0 (0)0 (0)2 (6)NLHsueh  et al. [21]HAR6638NoOpen35/311/25/38No13 (20)2 (3)0 (0)6 (9)80 (5)ONU775443/333/39/3419 (25)2 (3)12 (16)75 (5)Chung  et al. [18]HAR2532NoOpen13/121/13/11No9 (36)3 (12)0 (0)2 (8)92 (3)ONU416218/231/23/1713 (32)3 (7)5 (12)92 (3)Nakashima  et al. [19]HAR3523YesOpen22 ≤ T2,13T317 ≤ G2,18G3No12 (34)1 (3)0 (0)3 (9)89 (2)ONU385626 ≤ T2,11T324 ≤ G2,13G321 (55)1 (3)2 (5)91 (2)


### 2.4. Port-Site Metastases

One unique concern reported
following laparoscopic surgery is the occurrence of recurrent malignant disease
at the port-site [22]. To the best of our knowledge, there have
been 18 cases published in the literature of port-site metastases of upper
tract TCC after laparoscopy (Table 3). In seven cases, the diagnosis of TCC was
not suspected preoperatively which influenced the surgical technique.
Metastases occurred 3 to 15 months postoperatively (mean 6.8). These overall
experiences emphasize that general preventive measures should be undertaken at
the conclusion of the surgery including the use of an impermeable organ bag,
minimal tissue handling, and the avoidance of gross violation of the urinary
system until the specimen has been removed en bloc.Table 3
Port-site metastasis following LNU. CR, conventional retroperitoneal; CT,
conventional transperitoneal; HAT, hand-assisted transperitoneal; LNU,
laparoscopic nephroureterectomy; NL, not listed; TCC, transitional cell carcinoma;
TURBT, transurethral resection of bladder tumor.
AuthorSurgeryStageRetrieval bagMetastases locationTime to metastasis (mo)CommentsAhmed  et al. [23]CTpT3NoWidespread8Barrett
et al. [24]CTpT1NoWidespreadNLOtani et al. [25]CTpT3YesTrocar3Bag torn;
preoperative diagnosis of TCC not knownOng  et al. [26]CRpT1YesTrocar12Stent
perforation in proximal ureter noted at time of LNUChueh  et al. [27]HATpT2NLTrocar8Bilateral
LNU and TURBT performed in renal transplant patientMicali  et al. [28]CTpT3YesNL3Micali  et al. [28]CRpT3YesNL15Micali  et al. [28]HATpT3YesNL3Micali  et al. [28]CRpT1NoTrocar3Preoperative
diagnosis of TCC not knownMicali  et al. [28]CRpT1YesTrocarNLPreoperative
diagnosis of TCC not knownMicali  et al. [28]CRpT2YesTrocarNLPreoperative
diagnosis of TCC not knownMicali  et al. [28]CRNLYesTrocarNLPreoperative
diagnosis of TCC not knownMatsui  et al. [29]CRpT3NoTrocar6Squamous
cell carcinomaNaderi  et al. [30]CTpT2NoTrocar,
subcostal wound3Required conversion
to open surgery secondary to renal vein bleedingManabe  et al. [20]CRNLNLWidespreadNLUrine
extravasation secondary to urinary tract obstruction noted preopSchatteman
et al. [9]CTpT4NoWidespread5Preoperative
diagnosis of TCC not knownSchatteman
et al. [9]CTpT3NoWidespread8Preoperative
diagnosis of TCC not knownSchatteman
et al. [9]CTpT1YesWidespread11


## 2.1. Approach

A variety of
techniques have been utilized to perform mobilization of the kidney and proximal
ureter. These include conventional transperitoneal, conventional
retroperitoneal, hand-assisted transperitoneal, and hand-assisted
retroperitoneal approaches. The choice of laparoscopic approach is most
dependent on the comfort level and training of the surgeon. However, each
technique has its own potential advantages. Transperitoneal exposure offers the
largest working area and may be beneficial for extensive tumors or
lymphadenopathy. The retroperitoneal approach, however, involves decreased
bowel manipulation and potentially allows for earlier recovery of bowel
function. Additionally, this method may be favored in morbidly obese patients
with an obstructing pannus or in patients with a history of previous
transperitoneal surgeries [5].
Hand-assistance techniques allow for continued tactile sensation and may
lessen the learning curve required in laparoscopy [6]. Most of the experiences with LNU are
primarily reported as single-institutional retrospective series. To date, there
have been no prospective randomized studies that compare the different
techniques for LNU. However, data published in the laparoscopic radical
nephrectomy literature may be applicable. For example, a randomized,
prospective study comparing conventional transperitoneal, retroperitoneal, and
hand-assisted transperitoneal laparoscopic radical nephrectomy was recently
published [7]. The hand-assisted technique resulted in a significantly
shorter operative time but an increased risk of hernia formation; conversely, conventional
transperitoneal surgery was associated with significantly improved
perioperative morbidity. Desai et al. reported shorter operative times and
faster control of the renal vasculature with retroperitoneal approaches in a
prospective randomized comparison of conventional transperitoneal and
retroperitoneal laparoscopic radical nephrectomy but no significant differences
in other perioperative measures [5].


## 2.2. Perioperative Outcomes

Rassweiler et al.
performed a literature review of published studies between 1991 and 2004 of LNU
and ONU, including nine comparative studies and 1365 overall patients [3]. As compared to ONU, LNU was associated with
a slightly longer operative time (277 versus 220 minutes), significantly lower
blood loss (241 versus 463 mL), and shorter hospital stays, but showed similar
complication rates (18% versus 21%).Table1 summarizes
the perioperative outcomes of 12 LNU studies published since 2005. The mean
operating time ranged from 165 to 395 minutes (mean 271) in the laparoscopic
group (n=465 patients), and 155 to 313 minutes (mean 237) in the open group
(n=268 patients). Significantly increased operative time with laparoscopy was
noted in three of eight comparative studies, all of which involved the
retroperitoneal approach. The blood loss averaged between 183 to 497 mL (mean
279) in the laparoscopic group as compared to a range of 296 to 558 mL (mean
402) in the open group. Significantly less blood loss after laparoscopy was
noted in four of eight comparative studies with a similar trend in three of the
remaining studies. The overall complication rate ranged from 0 to 37% (mean
18%) in the laparoscopy group and from 0 to 15% (mean 7%) in the open group.
The open conversion rate associated with laparoscopy ranged from 0 to 10%. The
absolute duration of hospital stays varied between institutions. Out of eight
comparative studies, hospitalization following laparoscopy was shorter in seven
series with a significant difference in five.Table 1
Perioperative characteristics of LPN versus ONU cases. CR, conventional retroperitoneal; CT, conventional
transperitoneal; HAT, hand-assisted transperitoneal; NL, not listed; ONU, open nephroureterectomy.
AuthorSurgeryNumberHigh grade (%)OR duration (min)Blood loss (min)Conversion (%)Complication (%)Hospital daysMuntener et al. [8]CT3931 (80)3123004 (10)12 (31)4Schatteman et al.
[9]CT10048 (48)1922347 (7)19 (19)10Rouprêt
et al. [10]CT208 (40)1652751 (5)3 (15)4ONU2619 (73)155338—4 (15)9Okegawa
et al. [11]CR256 (24)2992581 (4)4 (16)11ONU237 (30)313403—3 (13)13Tsujihata
et al. [12]CR255 (20)3063220 (0)0 (0)2ONU2412 (50)271558—0 (0)4Taweemonkongsap  et al.  [13]CR3113 (42)2592890 (0)2 (6)9.3ONU2919 (66)191314—2 (7)8.7Chung et al. [14]HAT3916 (41)2331830 (0)5 (13)7ONU3615 (42)220422—3 (8)9Raman  et al. [15]HAT3815 (40)2441910 (0)4 (11)5ONU5219 (37)243478—2 (4)7Wolf  et al. [16]HAT5326 (49)2793301 (2)20 (37)4Cannon  et al. [17]HAT34NL3172520 (0)9 (26)8Chung  et al. [18]HAR2511 (44)2522120 (0)3 (12)6.5ONU4117 (41)212408—3 (7)9Nakashima
et al. [19]HAR3618  (50)3954971 (3)11 (31)18.8ONU3713 (35)289296—2 (5)19.1


## 2.3. Oncologic Outcomes

The highly aggressive
natural history of upper tract TCC, particularly with high-grade and high-stage
disease, likely contributes to its increased potential for recurrence and poor
prognosis irrespective of the surgical technique. However, there are many
concerns that technical aspects of LNU, particularly with regard to management
of the distal ureter and bladder cuff, may affect recurrence risks in the bladder,
locally, or as port-site metastases secondary to tumor seeding. Rassweiler et
al. noted no significant difference in bladder recurrence (24% versus 25%),
local recurrence (4% versus 6%) and distant metastases (15.5% versus 15.2%) in
eight LNU series and 11 ONU series [3]. The 2-year cancer specific survival rates
were also similar (75% versus 76%).Table2 summarizes
the short and intermediate oncologic outcomes of 14 LNU studies published since
2005. The most common method for bladder cuff excision was an open approach. At
a minimum median follow-up of at least 2 years, bladder recurrence after LNU
(n=488 patients) ranged from 10 to 55% (mean 30%) as compared to 15 to 55%
(mean 33%) in the ONU series (n=512 patients). Local recurrence in the
retroperitoneum was documented as 0 to 13% (mean 3.3%) in the laparoscopic
(n=588 patients) and 0 to 8% (mean 2.5%) in the open series (n=512 patients).
Distant metastases occurred in 0 to 18% (mean 9.5%) of patients undergoing LNU
(n=588 patients) as compared to 5 to 35% (mean 14.5%) in the open series (n=512
patients). In six series reporting 2-year disease-specific survival, the rates
ranged from 64 to 91% (mean 83%) in the laparoscopic series (n=274 patients) and
between 58 to 93% (mean 83.6%) after ONU (n=242 patients). In the five series
reporting 5-year survival rates, the outcomes ranged from 68 to 90% (mean 85%)
after LNU (n=202 patients) and 62 to 86% (mean 75%) in the ONU groups (n=191
patients). There was no significant difference between LNU and ONU survival
rates in the 10 comparative studies. However, absolute comparisons between the
surgical approaches are difficult as the percentage of patients with high-grade
disease and the follow-up period varied considerably, reflecting a large
limitation with the retrospective nature of these studies. In addition, the inclusion
of patients with a prior or concomitant history of bladder cancer may affect
the oncologic outcome of treating upper tract TCC. In the 14 LNU studies, only
7 addressed this parameter in defining their patient characteristics. The 4
comparative studies including such patients and the 1 study which excluded
patients with bladder TCC did not show a significant difference between ONU and
LNU groups. However, it is unclear if the underlying biology and tumor
aggressiveness in patients with both upper and lower tract TCC differ
from patients with isolated upper tract TCC; inclusion of such patients in
studies with already relatively low numbers further complicates comparisons of treatment
approach.Table 2
Oncologic outcomes of LPN versus ONU
cases. CR, conventional retroperitoneal; CT,
conventional transperitoneal; HAR, hand-assisted retroperitoneal; HAT,
hand-assisted transperitoneal; LND, lymph node dissection; LS, laparoscopic
stapling; NL, not listed; ONU, open nephroureterectomy; SD, surgeon discretion; TURUO,
transurethral resection; TV, transvesical.
AuthorSurgeryNFollow up (mo)History of bladder tumor specifiedBladder cuff surgeryPath stage (Ta,Tis,T1/T2, T3,T4)Path grade (1/2/3)LNDUrothelial recurrence (%)Local recurrence (%)Port-site recurrence (%)Distal recurrence (%)Disease-specific survival (@ year)Muntener et al. [8]CT3974YesOpen (19), LS (13), other (5)22/15/2NL8LG/31HGNo16 (41)2 (5)0 (0)7 (18)68 (5)Schatteman et al. [9]CT/CR95/520NoOpen (55), Other (45)54/4624/28/4820% of casesNL13 (13)3 (3)16 (16)88 (2)Rouprêt  et al. [10]CT2069NoOpen15/511/1512LG/8HGSD2 (10)0 (0)0 (0)2 (10)90 (5)ONU26787LG/19HG4 (15)0 (0)9 (35)62 (5)Okegawa  et al. [11]CR2524YesOpen14/119/142/17/6No5 (20)0 (0)0 (0)2 (8)91 (2)ONU23291/15/74 (17)0 (0)3 (13)89 (2)Tsujihata  et al. [12]CR2522NoOpen12/1315/65/15/5No7 (28)0 (0)0 (0)0 (0)64 (2)ONU24220/11/128 (33)0 (0)2 (8)58 (2)Manabe  et al. [20]CR5814ExcludedOpen28/3070/964/31/23No19 (33)1 (2)1 (2)10 (17)85 (2)ONU1662815/87/6463 (38)2 (1)33 (20)87 (2)Taweemonkongsap  et al. [13]CR3126YesOpen16/1518LG/13HGSD9 (29)2 (6)0 (0)3 (10)86 (2)ONU292813/1610LG/19HG13 (45)1 (3)2 (7)93 (2)Chung  et al. [14]HAT3948NoOpen18/211/22/16SD17 (44)1 (3)0 (0)6 (15)90 (5)ONU366017/191/20/1513 (36)3 (8)4 (11)86 (5)Raman  et al. [15]HAT3832YesOpen (30),27/923LG/15HGNo11 (29)1 (3)0 (0)2 (6)81 (5)ONU5251TURUO (8)41/1133LG/19HG18 (35)0 (0)6 (11)77 (5)Wolf  et al. [16]HAT5325YesTURUO (23), TV (22), Open (6), LS
(2)38/1518/9/26SD(55)(8)0 (0)(16)80 (3)Cannon  et al. [17]HAT3414NoOpen17/18NLNo8 (24)0 (0)0 (0)2 (6)NLHsueh  et al. [21]HAR6638NoOpen35/311/25/38No13 (20)2 (3)0 (0)6 (9)80 (5)ONU775443/333/39/3419 (25)2 (3)12 (16)75 (5)Chung  et al. [18]HAR2532NoOpen13/121/13/11No9 (36)3 (12)0 (0)2 (8)92 (3)ONU416218/231/23/1713 (32)3 (7)5 (12)92 (3)Nakashima  et al. [19]HAR3523YesOpen22 ≤ T2,13T317 ≤ G2,18G3No12 (34)1 (3)0 (0)3 (9)89 (2)ONU385626 ≤ T2,11T324 ≤ G2,13G321 (55)1 (3)2 (5)91 (2)


## 2.4. Port-Site Metastases

One unique concern reported
following laparoscopic surgery is the occurrence of recurrent malignant disease
at the port-site [22]. To the best of our knowledge, there have
been 18 cases published in the literature of port-site metastases of upper
tract TCC after laparoscopy (Table 3). In seven cases, the diagnosis of TCC was
not suspected preoperatively which influenced the surgical technique.
Metastases occurred 3 to 15 months postoperatively (mean 6.8). These overall
experiences emphasize that general preventive measures should be undertaken at
the conclusion of the surgery including the use of an impermeable organ bag,
minimal tissue handling, and the avoidance of gross violation of the urinary
system until the specimen has been removed en bloc.Table 3
Port-site metastasis following LNU. CR, conventional retroperitoneal; CT,
conventional transperitoneal; HAT, hand-assisted transperitoneal; LNU,
laparoscopic nephroureterectomy; NL, not listed; TCC, transitional cell carcinoma;
TURBT, transurethral resection of bladder tumor.
AuthorSurgeryStageRetrieval bagMetastases locationTime to metastasis (mo)CommentsAhmed  et al. [23]CTpT3NoWidespread8Barrett
et al. [24]CTpT1NoWidespreadNLOtani et al. [25]CTpT3YesTrocar3Bag torn;
preoperative diagnosis of TCC not knownOng  et al. [26]CRpT1YesTrocar12Stent
perforation in proximal ureter noted at time of LNUChueh  et al. [27]HATpT2NLTrocar8Bilateral
LNU and TURBT performed in renal transplant patientMicali  et al. [28]CTpT3YesNL3Micali  et al. [28]CRpT3YesNL15Micali  et al. [28]HATpT3YesNL3Micali  et al. [28]CRpT1NoTrocar3Preoperative
diagnosis of TCC not knownMicali  et al. [28]CRpT1YesTrocarNLPreoperative
diagnosis of TCC not knownMicali  et al. [28]CRpT2YesTrocarNLPreoperative
diagnosis of TCC not knownMicali  et al. [28]CRNLYesTrocarNLPreoperative
diagnosis of TCC not knownMatsui  et al. [29]CRpT3NoTrocar6Squamous
cell carcinomaNaderi  et al. [30]CTpT2NoTrocar,
subcostal wound3Required conversion
to open surgery secondary to renal vein bleedingManabe  et al. [20]CRNLNLWidespreadNLUrine
extravasation secondary to urinary tract obstruction noted preopSchatteman
et al. [9]CTpT4NoWidespread5Preoperative
diagnosis of TCC not knownSchatteman
et al. [9]CTpT3NoWidespread8Preoperative
diagnosis of TCC not knownSchatteman
et al. [9]CTpT1YesWidespread11


## 3. Bladder Cuff Excision

There is no consensus
as to the optimal technique to excise the distal ureter and ipsilateral bladder
cuff [1]. Definitive steps to minimize tumor seeding
and complete excision of the ureter are mandatory given the 30% to 64% tumor
recurrence rate reported following inadequate distal resections [31, 32]. As noted in Table 2, one of the most utilized
approaches involves an open approach. This may be accomplished transvesically
or extravesically via a lower midline, Pfannenstiel, or
Gibson incision, or by incorporation of the hand port incision following hand-assisted LNU. This technique is similarly employed during ONU and offers the surgeon
familiarity, direct visualization, and a simultaneous site for en bloc specimen
extraction. Awareness of the contralateral trigone and ureteral orifice location
should be undertaken as potential injury may occur during ipsilateral dissection
or bladder cuff closure [33].Alternatively, numerous
endoscopic approaches have been promoted. In 1952, McDonald et al. described
the first endoscopic method of bladder cuff excision, the “pluck” technique,
via transurethral resection of the ureteral orifice (TURUO) at the onset of
surgery [34]. Resection
of the orifice and intramural ureter, however, may require patient
repositioning and when performed at the onset of the procedure can expose the extravesical
space to potential tumor seeding. Several modifications have been described to
this technique in contemporary series, including delaying resection until after
kidney mobilization, performing transvesical endoscopy [35] or using transurethral cystoscopy with a Bugbee
electrode [36] or Collins knife for excision [37]. Ko et al. reviewed their experience
comparing open dissection (n=27 patients) with modified TURUO using a Collins
knife (n=19 patients) following nephroureterectomy [38]. At a mean follow-up of over 22 months, they
noted similar bladder recurrence rates (22.2% versus 26.3%) without evidence of
pelvic recurrence.The technique of
ureteral intussusception has also been described and involves endoscopic
extraction of the ligated ureter using a “stripping” method with the assistance
of a ureteral catheter [39]. However, this approach is contraindicated
with concomitant bladder or ureteral tumors and was noted to have an incomplete
excision rate of 18.7% in a large single institutional series of 32 patients [40].Gill et al. described
the method of cystoscopic detachment and ligation which incorporates intramural
ureteral dissection with a Collins knife aided by two transvesical laparoscopic
ports and an endoloop to ligate the ureteral lumen and minimize potential tumor
spillage [41]. While this method most closely echoes the
intentions of ONU, it is associated with a steep learning curve and long procedural
time [42].Laparoscopic stapling
of the distal ureter and bladder cuff with either cystoscopic unroofing or a
pure extravesical approach has also been utilized [43]. This technique, however, has been
associated with the potential risk of stone formation [44] or viable tumor cells within the
incorporated staple line [45]. A comparison of laparoscopic stapling (20%
of cohort) with cystoscopic detachment and ligation (60% of cohort) by Matin
and Gill was notable for a positive surgical margin rate of 25% versus 2.8% [46]. Hattori et al. reported their experience
between laparoscopic stapling and open bladder cuff excision [44]. They noted a significantly decreased
operative time with laparoscopic stapling with no significant difference in
bladder and extravesical recurrence-free rates and disease-specific survival at
3-year follow-up. Tsivian et al. detailed a modified technique for excising the
periurethral bladder cuff en bloc using a LigaSure Atlas device instead of a
stapler [47]. Similarly,
excision via harmonic scalpel has also been utilized [48]. Division of the bladder cuff using
hemostatic diathermy devices may address the potential concerns of viable tumor
cells and stone formation associated with laparoscopic stapling although
further study is needed.While there have been
no randomized prospective trials comparing the management of the distal ureter,
several groups have reported their retrospective results with several different
approaches. In a large multicenter
American and European study, Abou El Fettouh et al. noted that the local recurrence
rates and the development of metastases depended on pathologic tumor stage and
was irrespective of bladder cuff approach (open, TURUO, cystoscopic detachment
and ligation, laparoscopic stapling) [49]. In a
series of 55 patients undergoing hand-assisted transperitoneal LNU, Brown et al.
noted increased perioperative morbidity and complications with TURUO. However,
higher positive surgical margins were observed following laparoscopic stapling
(29%) or extravesical harmonic scalpel excision (10%) as compared to TURUO or
open techniques [50]. Additionally, in patients without active or
recent lower tract TCC, concerns exist regarding the increased potential risk
of local recurrence when the cystotomy is not primarily closed following
excision of the ureteral orifice and bladder neck as with many of the
endoscopic approaches. Brown et al. noted their sole pelvic recurrence occurred
in 1 of 7 patients without cystotomy closure, leading the authors to also
advocate routine bladder defect closure [50]. However, Kurzer et al. reported no local
recurrences in 49 patients treated with a modified TURUO technique and no
cystotomy closure at a median follow-up of 10 months [51].


## 4. Role of Lymphadenectomy

Given its aggressive
nature, the presence of nodal involvement in TCC of the renal pelvis and ureter
is a poor prognostic factor and has shown limited response to adjuvant
therapies [52]. However, the role and utilization of
routine lymph node dissection (LND) in conjunction with either LNU or ONU is not
well established. This contrasts lower urinary tract TCC in which extended
pelvic LND is well supported in the literature for improved staging and
survival benefits [53]. One reason for the variable use of LND (Table 2) is that the standard template for regional lymph node involvement in upper
tract TCC has not been well delineated. In a recent review of 42 of 181
patients with upper tract TCC metastases, Kondo et al. noted that the location
of lymph node metastases depended on the laterality and level of the primary
tumor [54]. Based
on their findings, the authors advocated a relatively wide LND template,
particularly on the right side to include the paracaval, retrocaval, and
interaortocaval nodes. In a follow-up study, the authors noted an improved
cancer-specific survival in patients with advanced disease (stage pT3 or
higher) undergoing LND although no difference was noted when all pathologic
stages were considered [55]. Brausi et al. similarly reported an
improved disease-specific survival benefit in patients treated with ONU and LND
(81.6%) as compared to ONU alone (44.8%) [56]. However, the retrospective study may have
been influenced by a potential bias in patient selection for LND [57]. Additionally, regardless of the benefits of
LND, concerns remain regarding the technical challenge of laparoscopic
lymphadenectomy. Hattori et al. reported a significantly decreased number of
lymph nodes removed following LNU (8.2–11.6) as compared
to ONU (16.5) [44]. Busby
and Matin, however, reported their experience that removal of an equivalent
number of nodes could be performed with both laparoscopic and open approaches [58].


## 5. Future Developments

With the increased
popularity in robotic-assisted laparoscopy in urology, individual case reports
and small case series have recently described robotic-assisted LNU with either
retroperitoneal or transperitoneal approaches [59–62]. The improved dexterity, precision, and
control of robotic assistance may better facilitate handling of the distal
ureter and bladder cuff [60]. However, concerns with cost and the
potential need for patient repositioning and robot redocking may influence the
widespread utilization of robotics in treating upper tract TCC.


## 6. Conclusions

Following the increased
popularity of laparoscopy in urologic surgery, LNU has become a common treatment
for TCC of the renal pelvis and ureter with decreased perioperative morbidity,
shorter hospitalization, as well as comparable oncologic outcomes and survival
rates as with ONU. The optimal technique for mobilization of the kidney and
proximal ureter, as well as excision of the distal ureter and bladder cuff, is
still evolving and largely based on surgeon preference. The classic open
approach for distal ureter removal is most comparable to the established
principles of open oncologic surgery and simultaneously allows for intact en bloc
specimen removal. Regardless of technique used, minimal disruption of the
urinary tract should be maintained to decrease the risk of recurrences and
port-site metastases. The role of routine lymphadenectomy and the utilization
of robotic assistance in upper urinary tract TCC are still to be determined. Long-term
studies with prospective, randomized trials are necessary to fully evaluate the
outcomes of LNU in the management of this aggressive disease.



---

*Source: 721371-2009-01-08.xml*