# Laparoscopic Nephroureterectomy: The Distal Ureteral Dilemma

Authors: Shalom J. Srirangam; Ben van Cleynenbreugel; Hein van Poppel
Journal: Advances in Urology
 (2009)

---

## Abstract

Transitional cell carcinoma affecting the upper urinary tract, though uncommon, constitutes a serious urologic disease. Radical nephroureterectomy remains the treatment of choice but has undergone numerous modifications over the years. Although the standard technique has not been defined, the laparoscopic approach has gained in popularity in the last two decades. The most appropriate oncological management of the distal ureteral and bladder cuff has been a subject of much debate. The aim of the nephroureterectomy procedure is to remove the entire ipsilateral upper tract in continuity while avoiding extravesical transfer of tumor-containing urine during bladder surgery. A myriad of technical modifications have been described. In this article, we review the literature and present an overview of the options for dealing with the lower ureter during radical nephroureterectomy.


---

## Body

## 1. Management of The Distal Ureter

The risk of tumor recurrence within the residual ureteral
stump/periureteral meatal region in cases of incomplete upper tract removal is
often cited as between 30 and 64% [10–12]. Total
excision of the entire ureter, including the distal ureter with its intramural
portion, the ipsilateral ureteral orifice and bladder cuff is
mandatory and represents a distinct portion of the case, whether an open
or laparoscopic approach to the kidney is used. Ideally, this is achieved by
removal of an en bloc, “closed
system” specimen following controlled occlusion of the ureteral orifice.
Continuity of the specimen, though desirable, may be conceded to aid ease of
extraction as long as the distal ureter is ligated and divided at tumor-free
location. The key issue is to avoid extravesical urine contact and adherence to
these principles will reduce risk of spillage or seeding of tumor cells.The following techniques, along with some minor variations, have been advocated in order to accomplish distal ureteral removal:(i)
“pluck” technique,(ii)
intussusception technique,(iii)
pure laparoscopy,(iv)
open resection.


## 2. Transurethral Resection of Ureteral Orifice (“Pluck” Technique)

This involves the transurethral disarticulation of the intramural ureter along with the ureteral
orifice (UO) using a standard resectoscope loop or Collin’s knife, usually
prior to performing the laparoscopic nephrectomy. The UO is resected deep into
extravesical fat allowing subsequent “plucking” of the entire ureter from
above. Though the original intention was to decrease morbidity by avoiding a
second lower abdominal incision during open surgery, this is a less compelling
argument with laparoscopic surgery as specimen extraction mandates a larger
incision.Following UO resection, the patient is put in the flank position for LNU. The kidney is mobilized along with the ureter down to the level of the pelvic brim. Gentle traction on the
ureter should result in the removal of the entire length of ureter down to the
level of the detached distal ureter. An indwelling Foley catheter is left in
the bladder for at least 7 days. The major concern related to this technique is
the risk of tumor cell spillage into the retroperitoneum with subsequent
seeding and local recurrence.A number of authors have published small retrospective series employing the pluck technique and report no local disease recurrences [13–15]. Palou et al.
reported no local recurrences after an average followup of 20 months in 31
patients with mainly high grade upper tract TCC [13]. In a large multicenter, five-institution study comprising 116 patients who underwent LNU, no
difference in local recurrence was noted between the  various techniques of
distal ureteral removal at a median followup time of 25 months [14]. Geavlete et al. recently reported   on 100 ONU patients from a single center, the majority of
whom (72 cases) had undergone a pluck transurethral detachment with coagulation
of the resected area [16]. The remainder (28 cases) were managed by ureteral stripping. No local recurrences were reported after a mean followup of 44
months.Nevertheless, the propensity for urological malignancies, including TCC, to seed is well
recognized [17]. Not surprisingly, therefore, local recurrence following a pluck nephroureterectomy has been noted on many occasions, often occurring
early and with tragic consequences [18–22]. Ko et al.
reported on 51 patients undergoing LNU with the distal ureter being managed by
either the open (n = 30) or the pluck technique (n = 20) [23]. The transurethral pluck was restricted to TCC located in the calices, renal pelvis, and ureter proximal to the pelvic brim and produced recurrence rates similar to those in an open fashion. Of note,
however, is that five patients had an unplanned incomplete ureterectomy and
four had tumor recurrences (three in
the form of metastatic disease).Furthermore, utilizing the pluck technique is likely to permit continued urine extravasation from the cancer-bearing ureter [24, 25].
Additionally, due to the absence of an identifiable marker within the detached
distal ureter, confirmation of complete specimen removal is not possible,
raising the theoretical possibility of local recurrence in any remaining
portion of ureter [24].


### 2.1. Pluck Technique Modifications

Various modifications on the pluck theme have been
described in an attempt to minimize tumor spillage. Tan et al. advocated
completion of the laparoscopic nephrectomy first with the clipping of the
ureter to prevent distal migration, followed by transurethral Collin’s knife
mobilization of the distal ureter and bladder cuff [8].
Recently, a novel technique has been described involving an initial partial circumscribing of the
bladder cuff with a Collin’s knife with a 1 cm margin around the ipsilateral
ureteral orifice [26]. A preformed PDS Endoloop (Ethicon, Sommerville, NJ, USA) is then passed through the
cystoscope to ligate and occlude the ureteral orifice. The bladder cuff is then
completely circumscribed down to perivesical fat and subsequently removed en
bloc following kidney mobilization. The Endoloop also acts as a marker
ensuring complete specimen removal. A similar procedure has been described
using a transurethrally placed 5-mm laparoscopic hem-o-lok clip on the ureteral
stump, as an alternative to the Endoloop, to ensure a closed system [27]. Both
these studies report no pelvic tumor recurrences in the short term [26, 27].


### 2.2. Ureteral Unroofing

The ureteralunroofing technique has been described
and popularized by the Washington University
group [28]. This can only be employed in transperitoneal LNU and briefly comprises cystoscopic incision of the entire anterior length of the intramural ureter;
electrocautery to the cut edges and floor of the intramural ureter; placement
of a 7.5 F occlusion ureteral balloon catheter in the renal pelvis to prevent
urine spillage; laparoscopic dissection of the kidney and ipsilateral ureter
down to the level of the bladder and specimen detachment following placement of
an Endo-GIA stapler on the bladder cuff. This technique has the theoretical advantage
of minimizing urine leakage while maintaining a truly minimally invasive
approach and promoting ureteral identification intraoperatively. It is
contraindicated in the presence of active ureteral or bladder TCC. Other
potential disadvantages include requirement of fluoroscopy, risk of injury to
the contralateral ureteral orifice as the stapler is applied “blindly” and
longer operating times [8]. Employment of the stapler device has produced hypothetical concerns relating to stone formation, tumor recurrence within
urothelium trapped in the staple line, and the inability to visualize this area
satisfactorily during subsequent surveillance cystoscopic inspections. These
complications have not been reported to be a clinical problem. The same
investigators compared LNU in 25 patients (using the unroofing technique) and
ONU performed in 17 cases with a mean
followup of 24 months and 43 months, respectively [29].
LNU took twice as long as ONU, but was associated with less pain, fewer complications, a shorter
hospital stay, and quicker convalescence. Although there was no statistically
significant difference in the disease-specific survival rate and proportion of
bladder tumor recurrences, concerningly, there were 3 retroperitoneal
recurrences in the LNU group. Whether this is due to surgical technique or the
high tumor grade in these patients in unclear from the study.


### 2.3. Pluck Technique in HALNU

HALNU offers distinct advantages when considering
how best to manage the distal ureter. Firstly, the requirement of a longer
incision to facilitate a hand port will allow improved access to the bladder
and distal ureter, offering the surgeon the option of either an extravesical
approach, open transvesical cystotomy, or detaching the ureter using a
transurethral technique [30].
In addition, the operator can facilitate dissection and resection by providing
gentle countertraction on the distal ureter. Tumor spillage can be prevented by
occlusion of the distal ureter by a clip or the surgeon’s hand. Alternatives to
the endoscopic management of the distal ureter during HALNU have been reported.
Gonzalez et al. described a technique implementing insertion of a laparoscopic
trochar, followed by introduction of a 24 F nephroscope allowing an endoscopic
Collin’s knife incision of the bladder cuff [31].
This is performed subsequent to dissection of the kidney and ureter, and after clips have been placed on the lower ureter. Alternatively, a similar technique may be performed without the
need for a bladder port or patient repositioning [32]. Placement of the patient in a modified dorsal lithotomy position will permit introduction of a
transurethral resectoscope to perform the bladder cuff incision. The
oncological sequalae of this same group of patients was recently published, and
none of the 49 patients had developed a pelvic recurrence after a mean followup
period of 10.6 months [33]. Notably, the authors emphasized early ligation of
ureter but did not routinely close the bladder. Vardi et al. reported a novel
modification to this technique by inserting a flexible cystoscope per urethra
and a 5 F electrode (ACMI, Norwalk, Conn, USA) to incise a circumferential 2-cm cuff of bladder around the UO using cutting and coagulating current [34]. Patient repositioning after the nephrectomy is avoided and the bladder opening is not closed. No pelvic recurrences were noted in their small group of patients after a mean followup of 31 months.In summary, therefore, pluck techniques are
contraindicated in the presence of lower ureteral tumor and widespread urinary
tract carcinoma in situ. Coexistent bladder TCC should preclude the situation,
where the bladder is left “open” with potential exposure of the perivesical
tissues to malignant-cell laden urine. Patients with previous pelvic
irradiation and active inflammatory conditions of the bladder are probably not
ideal candidates for endoscopic procedures. Blind pulling of the ureter is
discouraged to minimize ureteral tearing and the possibility of residual
tissue. While retrospective studies have not confirmed the superiority of the
open over the pluck method, the oncologically safe practice of maintaining a “closed” system is preferred and retroperitoneal exposure to potentially tumor cell-laden urine for any duration
of time, in our opinion, is best avoided.


## 2.1. Pluck Technique Modifications

Various modifications on the pluck theme have been
described in an attempt to minimize tumor spillage. Tan et al. advocated
completion of the laparoscopic nephrectomy first with the clipping of the
ureter to prevent distal migration, followed by transurethral Collin’s knife
mobilization of the distal ureter and bladder cuff [8].
Recently, a novel technique has been described involving an initial partial circumscribing of the
bladder cuff with a Collin’s knife with a 1 cm margin around the ipsilateral
ureteral orifice [26]. A preformed PDS Endoloop (Ethicon, Sommerville, NJ, USA) is then passed through the
cystoscope to ligate and occlude the ureteral orifice. The bladder cuff is then
completely circumscribed down to perivesical fat and subsequently removed en
bloc following kidney mobilization. The Endoloop also acts as a marker
ensuring complete specimen removal. A similar procedure has been described
using a transurethrally placed 5-mm laparoscopic hem-o-lok clip on the ureteral
stump, as an alternative to the Endoloop, to ensure a closed system [27]. Both
these studies report no pelvic tumor recurrences in the short term [26, 27].


## 2.2. Ureteral Unroofing

The ureteralunroofing technique has been described
and popularized by the Washington University
group [28]. This can only be employed in transperitoneal LNU and briefly comprises cystoscopic incision of the entire anterior length of the intramural ureter;
electrocautery to the cut edges and floor of the intramural ureter; placement
of a 7.5 F occlusion ureteral balloon catheter in the renal pelvis to prevent
urine spillage; laparoscopic dissection of the kidney and ipsilateral ureter
down to the level of the bladder and specimen detachment following placement of
an Endo-GIA stapler on the bladder cuff. This technique has the theoretical advantage
of minimizing urine leakage while maintaining a truly minimally invasive
approach and promoting ureteral identification intraoperatively. It is
contraindicated in the presence of active ureteral or bladder TCC. Other
potential disadvantages include requirement of fluoroscopy, risk of injury to
the contralateral ureteral orifice as the stapler is applied “blindly” and
longer operating times [8]. Employment of the stapler device has produced hypothetical concerns relating to stone formation, tumor recurrence within
urothelium trapped in the staple line, and the inability to visualize this area
satisfactorily during subsequent surveillance cystoscopic inspections. These
complications have not been reported to be a clinical problem. The same
investigators compared LNU in 25 patients (using the unroofing technique) and
ONU performed in 17 cases with a mean
followup of 24 months and 43 months, respectively [29].
LNU took twice as long as ONU, but was associated with less pain, fewer complications, a shorter
hospital stay, and quicker convalescence. Although there was no statistically
significant difference in the disease-specific survival rate and proportion of
bladder tumor recurrences, concerningly, there were 3 retroperitoneal
recurrences in the LNU group. Whether this is due to surgical technique or the
high tumor grade in these patients in unclear from the study.


## 2.3. Pluck Technique in HALNU

HALNU offers distinct advantages when considering
how best to manage the distal ureter. Firstly, the requirement of a longer
incision to facilitate a hand port will allow improved access to the bladder
and distal ureter, offering the surgeon the option of either an extravesical
approach, open transvesical cystotomy, or detaching the ureter using a
transurethral technique [30].
In addition, the operator can facilitate dissection and resection by providing
gentle countertraction on the distal ureter. Tumor spillage can be prevented by
occlusion of the distal ureter by a clip or the surgeon’s hand. Alternatives to
the endoscopic management of the distal ureter during HALNU have been reported.
Gonzalez et al. described a technique implementing insertion of a laparoscopic
trochar, followed by introduction of a 24 F nephroscope allowing an endoscopic
Collin’s knife incision of the bladder cuff [31].
This is performed subsequent to dissection of the kidney and ureter, and after clips have been placed on the lower ureter. Alternatively, a similar technique may be performed without the
need for a bladder port or patient repositioning [32]. Placement of the patient in a modified dorsal lithotomy position will permit introduction of a
transurethral resectoscope to perform the bladder cuff incision. The
oncological sequalae of this same group of patients was recently published, and
none of the 49 patients had developed a pelvic recurrence after a mean followup
period of 10.6 months [33]. Notably, the authors emphasized early ligation of
ureter but did not routinely close the bladder. Vardi et al. reported a novel
modification to this technique by inserting a flexible cystoscope per urethra
and a 5 F electrode (ACMI, Norwalk, Conn, USA) to incise a circumferential 2-cm cuff of bladder around the UO using cutting and coagulating current [34]. Patient repositioning after the nephrectomy is avoided and the bladder opening is not closed. No pelvic recurrences were noted in their small group of patients after a mean followup of 31 months.In summary, therefore, pluck techniques are
contraindicated in the presence of lower ureteral tumor and widespread urinary
tract carcinoma in situ. Coexistent bladder TCC should preclude the situation,
where the bladder is left “open” with potential exposure of the perivesical
tissues to malignant-cell laden urine. Patients with previous pelvic
irradiation and active inflammatory conditions of the bladder are probably not
ideal candidates for endoscopic procedures. Blind pulling of the ureter is
discouraged to minimize ureteral tearing and the possibility of residual
tissue. While retrospective studies have not confirmed the superiority of the
open over the pluck method, the oncologically safe practice of maintaining a “closed” system is preferred and retroperitoneal exposure to potentially tumor cell-laden urine for any duration
of time, in our opinion, is best avoided.


## 3. Intussusception Technique

This technique, first described by McDonald in 1953, has undergone various subsequent modifications
around a central theme of ureteral ligation and removal either by stripping or
intussusception [35]. Principles of this technique include initial
catheterization of the ureter using either a ureteral catheter or a stone
basket ligation and division of the ureter as part of the renal mobilization,
securing of the distal ureter to the ureteral catheter/stone basket, transurethral
incision of the bladder cuff, followed by removal of the distal ureter by
gentle traction on the catheter via the urethra [8, 18]. The distal ureter
intussuscepts into the bladder and can either be removed transurethrally or via
a small lower midline incision and anterior cystotomy. A variety of technical
devices, including sutures, vein stripper, balloon catheter, and double
ligation, have been described in an attempt to improve ureteral excision of the
ureter [18, 36–38].Though its long-term safety during LNU has not been
investigated, even after 5 years’ followup, Clayman et al. reported no pelvic
tumor recurrences in 14 patients undergoing ureteral stripping during ONU [36]. This is confirmed in a literature review by Laguna and de la Rosette, who compared the stripping and pluck techniques [18]. While there were no reports of local disease recurrence in the stripping group, this technique was associated with a 10% complication rate (including retained ureters and catheter breakage) resulting
in an open conversion rate of between 9.5 and 12.5% in patients after difficult
extraction.Since the ureter is transected, it is contraindicated for ureteral tumors and primarily
confined to low-grade renal pelvic tumors. Additionally, any cause for pelvic fibrosis,
such as previous surgery or irradiation and retroperitoneal fibrosis, may
further increase the risk of retention of ureteral remnant. Bladder mucosa is
exposed to ureteral mucosa with the potential for seeding. Its main drawback is
its failure to guarantee adequate excision of the intramural ureter and bladder
cuff, potentially resulting in tumor recurrence, and is thus unlikely to gain
universal acceptance following LNU.


## 4. Pure Laparoscopic

A completely laparoscopic approach offers distinct advantages in terms
of blood loss, postoperative pain, recovery times, and equivalent short- and
intermediate-term oncologic efficacy. The kidney and ureter are mobilized in
the standard fashion and the distal ureter may be secured by one of 2 main techniques:(i)
laparoscopic extravesical stapling of
the distal ureter [28, 39];(ii)
transvesical laparoscopic detachment and ligation (Cleveland
approach) [40, 41].


### 4.1. Laparoscopic Stapling

This method is usually combined with a ureteral unroofing procedure. The
ureter is clipped early and dissected caudally until it diverges to merge with
the detrusor muscle fibers at the ureterovesical junction (UVJ). Gentle
traction on the ureter will tent up the wall of the bladder at the UVJ enabling
placement of a 12-mm laparoscopic GIA tissue stapler (Endo-GIA; Auto-Suture, Norwalk,
Conn, USA) or a large hem-o-lok clip. If desired, an ontable bladder fill with saline/indigo carmine
solution may be performed to exclude extravasation and/or a delayed cystogram
is obtained before catheter removal. A more recent trend has been to perform
stapling of the bladder cuff as the initial step, followed by a transurethral
resection of the ipsilateral UO till the staple line is reached
[8].Laparoscopic stapling has manifest advantages. It may help reduce
operative time and facilitates a minimally invasive procedure while maintaining
a “closed” urinary tract, thus preventing tumor spillage. There are, however,
numerous concerns related to staple usage. Deployment of the stapler may prove awkward in the restricted pelvic space. An error in judgment may result in either part of the intramural ureter
being left behind or inadvertent injury to the contralateral UO. In addition,
the stapled margin cannot be assessed histologically. The Nagoya group reported stone formation at the staple line in 3 (5.7%) of 53 patients at an average of 20 months
postoperatively [42]. Using a porcine model, Venkatesh et al. investigated the viability of bladder cells using 4 types of laparoscopic vascular and tissue stapler
devices [43]. Viable cells were noted within the staple line
in all cases and this could represent a potential risk for tumor
recurrence in patients.Romero et al. compared long-term safety and oncologic efficacy of extravesical
laparoscopic stapling (n = 12) with the traditional transvesical open excision
(n = 12) at nearly 4 years followup [44]. An increased positive margin rate (3 versus 0 patients) and local recurrence rate (2 versus 0 patients), and decreased
recurrence-free interval were noted in the laparoscopic stapled group compared
to the open group. However, none of these results was statistically significant
probably owing to the small numbers. A number of authors have compared the
various methods to distal ureteral excision and reported a higher incidence of
positive surgical margins (up to 25%) and local recurrence (up to 15%) in the
pure LNU with laparoscopic stapling cohort [25, 29, 45]. This highlights the
need for meticulous removal of the whole ureter, UO, and bladder cuff. Contraindications include presence of mid/lower ureteral
and bladder TCC.More recently, Tsivian et al. described a variation on the laparoscopic
stapling technique, using a 10-mm LigaSure Atlas (Valleylab, Tyco Healthcare UK Ltd, Gosport, UK)
[46]. The
bladder cuff was excised laparoscopically in an extravesical fashion using the
LigaSure, without the need for staples. There were 2 bladder recurrences
distant from the site of surgery but no reports of local recurrence in 13
patients followed up for nearly a year. Suturing of the bladder following LNU
may be performed by those skilled in this technique.


### 4.2. Transvesical Laparoscopic Detachment and Ligation

This novel technique of securing the distal ureter and bladder cuff using
transvesically placed laparoscopic ports was described by Gill et al. and is
almost exclusively employed by the Cleveland clinic group [40, 41]. In this modified “pluck” procedure, a transurethral
Collin’s knife incision of the bladder cuff is performed after placement of a
catheter into the affected ureter. Simultaneously, two 5-mm balloon-tipped
ports are inserted suprapubically into the bladder. The incised UO is tightly
snared using a 5-mm Endoloop (Ethicon, Cincinnati, Ohio, USA), preventing urine leakage from the ureter. Traction on the incised bladder cuff enables the mobilization of 3-4 cm of
distal ureter into the bladder. The entire ureter can then be pulled through cephalad
after radical nephrectomy and ureteral dissection. A bladder catheter is left
in situ for 1 week.The authors claim that the transvesical technique adheres to general oncological
principles of complete and controlled en bloc specimen extraction. The ureteral
catheter and Endoloop occlude the ureter, thereby reducing urine leakage. An
indwelling ureteral catheter may aid identification and mobilization of the
ureter during the laparoscopic procedure. Complete retrieval is confirmed by
visualization of the Endoloop. However, this may be a difficult technique to
master for most urologists and operating time is usually lengthened by 60–90 minutes
[24, 47].
Other criticism of this approach includes the potential for irrigation fluid
extravasation resulting in dilutional hyponatremia, the need for patient
repositioning, and the possibility of port-site metastases. Contraindications
include the presence of distal ureteral TCC or concomitant bladder tumors, prior
pelvic surgery or irradiation and obesity [45].LNU with the transvesical technique has been evaluated
against ONU in a retrospective series [41].
Gill et al. reported that 27 patients who had undergone the former procedure had statistically significant superior results compared to the latter (35 patents) technique with regards to
surgical time, blood loss, narcotic analgesia requirements, hospital stay,
convalescence, and complication rates. Bladder recurrence rates and cancer
specific survival were similar in both groups and no local retroperitoneal or
port-site recurrence were diagnosed in any patients. The same group reviewed
their outcomes in 60 patients following LNU, who had either had a laparoscopic
stapling (n = 12) or transvesical laparoscopic detachment of the distal ureter
(n = 36) [45]. Following a mean followup period of 23 months, positive
margins were more common in the former group (25 versus 2.8%) as were the rates
of bladder recurrences at the ipsilateral ureteral scar/orifice (41.7 versus
13.9%), retroperitoneal recurrence (8.3 versus 5.6%), and distant metastasis
(25 versus 8.3%). None of these differences was statistically significant and
definitive conclusions are difficult to derive from such small retrospective
series.Recently, Cheng et al. described a similar technique utilizing a pneumovesicum to secure
the UO and bladder cuff [48]. Following initial cystoscopy to exclude bladder tumors, three 5-mm PediPorts (Tyco) are inserted suprapubically into the
bladder. Following the establishment of a carbon dioxide pneumovesicum, the
ipsilateral UO is closed using a stitch and the bladder cuff is incised down to
fat using diathermy scissors. The bladder defect is closed using Polysorb
sutures before completion of a standard 5-port laparoscopic nephroureterectomy.
The authors report on a single case and propose that gas insufflation minimizes
tumor spillage/seeding and permits a superior endoscopic view, even in the
presence of bleeding, compared to liquid endoscopy as in the Cleveland  method.


## 4.1. Laparoscopic Stapling

This method is usually combined with a ureteral unroofing procedure. The
ureter is clipped early and dissected caudally until it diverges to merge with
the detrusor muscle fibers at the ureterovesical junction (UVJ). Gentle
traction on the ureter will tent up the wall of the bladder at the UVJ enabling
placement of a 12-mm laparoscopic GIA tissue stapler (Endo-GIA; Auto-Suture, Norwalk,
Conn, USA) or a large hem-o-lok clip. If desired, an ontable bladder fill with saline/indigo carmine
solution may be performed to exclude extravasation and/or a delayed cystogram
is obtained before catheter removal. A more recent trend has been to perform
stapling of the bladder cuff as the initial step, followed by a transurethral
resection of the ipsilateral UO till the staple line is reached
[8].Laparoscopic stapling has manifest advantages. It may help reduce
operative time and facilitates a minimally invasive procedure while maintaining
a “closed” urinary tract, thus preventing tumor spillage. There are, however,
numerous concerns related to staple usage. Deployment of the stapler may prove awkward in the restricted pelvic space. An error in judgment may result in either part of the intramural ureter
being left behind or inadvertent injury to the contralateral UO. In addition,
the stapled margin cannot be assessed histologically. The Nagoya group reported stone formation at the staple line in 3 (5.7%) of 53 patients at an average of 20 months
postoperatively [42]. Using a porcine model, Venkatesh et al. investigated the viability of bladder cells using 4 types of laparoscopic vascular and tissue stapler
devices [43]. Viable cells were noted within the staple line
in all cases and this could represent a potential risk for tumor
recurrence in patients.Romero et al. compared long-term safety and oncologic efficacy of extravesical
laparoscopic stapling (n = 12) with the traditional transvesical open excision
(n = 12) at nearly 4 years followup [44]. An increased positive margin rate (3 versus 0 patients) and local recurrence rate (2 versus 0 patients), and decreased
recurrence-free interval were noted in the laparoscopic stapled group compared
to the open group. However, none of these results was statistically significant
probably owing to the small numbers. A number of authors have compared the
various methods to distal ureteral excision and reported a higher incidence of
positive surgical margins (up to 25%) and local recurrence (up to 15%) in the
pure LNU with laparoscopic stapling cohort [25, 29, 45]. This highlights the
need for meticulous removal of the whole ureter, UO, and bladder cuff. Contraindications include presence of mid/lower ureteral
and bladder TCC.More recently, Tsivian et al. described a variation on the laparoscopic
stapling technique, using a 10-mm LigaSure Atlas (Valleylab, Tyco Healthcare UK Ltd, Gosport, UK)
[46]. The
bladder cuff was excised laparoscopically in an extravesical fashion using the
LigaSure, without the need for staples. There were 2 bladder recurrences
distant from the site of surgery but no reports of local recurrence in 13
patients followed up for nearly a year. Suturing of the bladder following LNU
may be performed by those skilled in this technique.


## 4.2. Transvesical Laparoscopic Detachment and Ligation

This novel technique of securing the distal ureter and bladder cuff using
transvesically placed laparoscopic ports was described by Gill et al. and is
almost exclusively employed by the Cleveland clinic group [40, 41]. In this modified “pluck” procedure, a transurethral
Collin’s knife incision of the bladder cuff is performed after placement of a
catheter into the affected ureter. Simultaneously, two 5-mm balloon-tipped
ports are inserted suprapubically into the bladder. The incised UO is tightly
snared using a 5-mm Endoloop (Ethicon, Cincinnati, Ohio, USA), preventing urine leakage from the ureter. Traction on the incised bladder cuff enables the mobilization of 3-4 cm of
distal ureter into the bladder. The entire ureter can then be pulled through cephalad
after radical nephrectomy and ureteral dissection. A bladder catheter is left
in situ for 1 week.The authors claim that the transvesical technique adheres to general oncological
principles of complete and controlled en bloc specimen extraction. The ureteral
catheter and Endoloop occlude the ureter, thereby reducing urine leakage. An
indwelling ureteral catheter may aid identification and mobilization of the
ureter during the laparoscopic procedure. Complete retrieval is confirmed by
visualization of the Endoloop. However, this may be a difficult technique to
master for most urologists and operating time is usually lengthened by 60–90 minutes
[24, 47].
Other criticism of this approach includes the potential for irrigation fluid
extravasation resulting in dilutional hyponatremia, the need for patient
repositioning, and the possibility of port-site metastases. Contraindications
include the presence of distal ureteral TCC or concomitant bladder tumors, prior
pelvic surgery or irradiation and obesity [45].LNU with the transvesical technique has been evaluated
against ONU in a retrospective series [41].
Gill et al. reported that 27 patients who had undergone the former procedure had statistically significant superior results compared to the latter (35 patents) technique with regards to
surgical time, blood loss, narcotic analgesia requirements, hospital stay,
convalescence, and complication rates. Bladder recurrence rates and cancer
specific survival were similar in both groups and no local retroperitoneal or
port-site recurrence were diagnosed in any patients. The same group reviewed
their outcomes in 60 patients following LNU, who had either had a laparoscopic
stapling (n = 12) or transvesical laparoscopic detachment of the distal ureter
(n = 36) [45]. Following a mean followup period of 23 months, positive
margins were more common in the former group (25 versus 2.8%) as were the rates
of bladder recurrences at the ipsilateral ureteral scar/orifice (41.7 versus
13.9%), retroperitoneal recurrence (8.3 versus 5.6%), and distant metastasis
(25 versus 8.3%). None of these differences was statistically significant and
definitive conclusions are difficult to derive from such small retrospective
series.Recently, Cheng et al. described a similar technique utilizing a pneumovesicum to secure
the UO and bladder cuff [48]. Following initial cystoscopy to exclude bladder tumors, three 5-mm PediPorts (Tyco) are inserted suprapubically into the
bladder. Following the establishment of a carbon dioxide pneumovesicum, the
ipsilateral UO is closed using a stitch and the bladder cuff is incised down to
fat using diathermy scissors. The bladder defect is closed using Polysorb
sutures before completion of a standard 5-port laparoscopic nephroureterectomy.
The authors report on a single case and propose that gas insufflation minimizes
tumor spillage/seeding and permits a superior endoscopic view, even in the
presence of bleeding, compared to liquid endoscopy as in the Cleveland  method.


## 5. Open Removal

The open technique (either
2-incision or extended single incision) forms the standard against which all
techniques are measured. Typically performed after nephrectomy, it can be
performed through a lower midline, modified Pfannenstiel, or Gibson incision.
The lower ureter is clipped, dissected free, and removed in continuity with the
bladder cuff. The bladder cuff may be secured extravesically (using a right
angle clamp) or via an anterior cystotomy. The en bloc specimen is delivered
through the same incision.In the review of 252 patients performed by Hall et al., 194 patients had undergone ONU with open
bladder cuff excision for TCC and showed excellent long-term local control
[6]. Klingler et al. reported outcomes at a mean followup period of 22 months in 19 patients who had an LNU with open bladder cuff excision versus 15 patients with
a standard ONU [49]. Only 1 patient in the LNU group, with a high-grade, locally infiltrative, lymph node positive final histology (pT3b pN2 G3 TCC) had
local recurrence. There was no significant difference in local recurrence rates
between the laparoscopic and open group.A recent multicenter retrospective Belgian study analyzed 100 patients following LNU for TCC [50]. Of these, 55 patients had an open excision of the distal ureter while the rest (45 patients) underwent a laparoscopic technique. Local recurrence was noted in
13 out of 100 cases of which 6 of 55 cases (11%) had open distal ureter
management and 7 of 45 (16%) laparoscopic handling of the distal ureter. The
investigators attribute the higher local recurrence rate to the larger
proportion of high grade disease being operated on.The open technique is not without its pitfalls. The “blind” extravesical clamping may compromise the contralateral UO and does not inevitably guarantee adequate bladder cuff
retrieval [51]. An anterior cystotomy must be avoided in the presence of active bladder TCC as it retains the potential to seed tumor into the extravesical
space. Furthermore early ligation/clipping of the ureter during the nephrectomy
part is advisable. Additionally, prior pelvic surgery or irradiation and
obesity may render the open procedure more challenging. Notwithstanding these
potential concerns, the open approach to distal ureteral removal is
oncologically sound and minimizes tumor spillage and therefore has withstood
the test of time [52]. An open incision is often required for specimen
extraction and adds little to overall morbidity, while providing visual
confirmation of complete upper tract resection. It also enables accurate
histological examination and reporting by the pathologist. Patient
repositioning is usually required but not always mandatory. At our institution,
this is the preferred method of dealing with the distal ureter following LNU. Table 1 summarizes the data from some of the studies
(all retrospective in design) comparing the different techniques of distal ureteral management and associated
outcomes.Table 1
Summary of perioperative results
and oncological outcomes for the different distal ureteral management
techniques from selected larger studies. (ND: no data; LOS: length of stay; f/u: mean followup).
f/unProcedure typeNumber of complications of distal ureter techniqueMedian LOS (days)Positive marginsBladder recurrence (%)Pelvic recurrence (no)No. of cancer-specific deathsPluck techniquePalou et al., 1995 [13]2031ONU1NDND3502Ubrig et al., 2004 [15]4418ONU111ND5005Geavlete et al., 2007
[16]4472ONU210ND2409Laguna and de la Rosette, 2001
(meta-analysis) [18]n/a129ONU/LNU3NDND244NDKo et al., 2007 [23]2219ONU/LNU07.302611Modification of
Pluck techniqueAgarwal et al., 2008 [26]1513LNU07.303801Ureteral
deroofingShalhav et al., 2000
[29]2424LNU26.1ND233NDPluck in HALNUWong and Leveillee, 2002 [32]814HALNUND2ND14NDNDLaparoscopic extravesical
ureteral staplingJarrett et al., 2001
[39]2425LNU0414802Laparoscopic
transvesical ureteral ligationGill et al., 2000 [41]1142LNU12.332402Open distal
ureteral excisionKlingler et al., 2003
[49]2219LNU08.10ND0NDTsujihata et al., 2006
[53]ND49ONU/LNU04ND3102Taweemonkongsap et al.,
2008 [54]2760ONU/LNU09ND3738


## 6. Open or Laparoscopic?

Given the uncommon nature of upper tract TCC, there is a scarcity of prospective randomized studies with
long-term followup comparing both modalities of nephroureterectomy. The “gold
standard” open surgery offers excellent access but at the expense of increased
patient morbidity. Since being first described in 1991 by Clayman et al.,
increasing surgical experience and equipment quality has seen LNU emerge as a
viable option with the express intention of minimizing surgical morbidity
without compromising oncology outcomes.Rassweiler et al. performed a meta-analysis comparing ONU and LNU, which included 1365 patients
from 85 studies [55]. LNU was associated with a slightly longer operating time (276.6 versus 220.1 minutes); significantly lower blood loss (240.9 versus
462.9 mL); decreased analgesia requirements and shorter hospital stay (not
statistically significant in all included studies). There appeared to be no
significant difference in complication rates, both minor (12.9 versus 14.1%)
and major (5.6 versus 8.3%) between LNU and ONU, respectively. In addition,
bladder recurrence, local recurrence, distant metastases, and actual
disease-free two-year survival rates (75.2 versus 76.2%) were similar. It is
worth noting that caution is suggested in interpreting the data from this
meta-analysis as the majority of studies were retrospective, nonrandomized, and
limited by short followup periods and  variable outcome measures.Further, recent smaller retrospective comparisons by McNeill et al.  (n = 67) [56], Tsujihata et al. (n = 49) [53],
Taweemonkongsap et al. (n = 60) [54], Rouprêt   et al. (n = 46) [57], and Manabe et al. (n = 224) [58] have
demonstrated parity between ONU and LNU when comparing oncological parameters
over a shorter followup period (1–3 years). In a
similar study, but with 7-year outcome data, LNU was noted to have a similar
local recurrence rate (8 versus 15.4%), bladder recurrence rate (28 versus 42%),
and 5-year metastases free survival rate (87.2 and 82.1%) compared to ONU [59].Port-site seeding following LNU remains a concern but is fortunately rare if appropriate surgical
techniques are adopted and have been mainly confined to individual case reports
[60, 61].Hand-assisted laparoscopic nephroureterectomy referred to as (HALNU) is often seen as a compromise between the open and laparoscopic technique. Arguments in its favor include a shorter learning
curve, facilitates tactile feedback and the eventual requirement of a longer
incision following LNU for specimen extraction. In a prospective, but nonrandomized
study with 27 subjects, patients undergoing an HALNU could expect a quicker
discharge from hospital, faster recovery, and fewer complications with an
equivalent intermediate-term oncologic outcome compared to the open approach [62].
On the other hand, HALNU took longer and was more expensive. Other studies
evaluating ONU and HALNU have confirmed an overall equivalence with regards to
cancer control in the short term [30, 63].Clearly, in the absence of prospective, randomized studies comparing ONU, LNU, and HALNU, it is
injudicious to draw robust conclusions  regarding the superiority of one
technique over the other. Nevertheless, though radical ONU still represents the
gold standard for upper tract TCC, laparoscopic nephroureterectomy appears to
offer the advantages of minimally invasive surgery without deteriorating the
oncological outcome in most cases.


## 7. Conclusion

TCC of the upper urinary
tract, though rare, constitutes a serious urological disease. Even though it is
curable in its early stages, there has been little improvement in disease-specific
survival in high-risk patients over the last three decades. Radical
nephroureterectomy, with en bloc removal of the entire ureteral length and cuff
of bladder, remains the procedure of choice, and the technique has undergone
numerous modifications in recent years. The integration of laparoscopy into
urological practice has seen LNU emerge as a viable option for the management
of upper tract TCC.Given the relative rarity
of the disease and a lack of robust multicenter effort, it is unlikely that the
issue of LNU versus ONU for upper tract TCC will be resolved in a prospective
randomized manner. Nevertheless, a multitude of small prospective studies with
intermediate followup have clearly demonstrated the benefits of minimally
invasive surgery (lesser morbidity, quicker recovery, better cosmesis)
associated with LNU, along with comparable oncological efficacy in the hands of
appropriately trained and experienced laparoscopic urologists. Long-term data
from these studies would be beneficial.The issue of the distal
ureteral remains unresolved, and number and complexity of available techniques
will undoubtedly continue to evolve. The existing data does not confirm the
overwhelming superiority of one technique over the other. Each method has its
distinct advantages and disadvantages and it is essential that the responsible
surgeon adopts a meticulous, safe, reproducible, and oncologically sound
technique.



---

*Source: 316807-2008-11-05.xml*