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INTRODUCTION: Although laparoscopic nephroureterectomy is an accepted procedure for treatment of urothelial carcinoma of the renal pelvis or middle and proximal ureter, the way to perform the distal ureterectomy next to the perimeatic bladder mucosa is controversial. The purpose of this study was to test the efficacy of a technique that is designed to destroy the ureteral mucosa and the bladder perimeatic mucosa through thermal ablation.
METHODS: A total of 27 patients with urothelial neoplasm were treated. The mean size of the tumors was 3.2 cm (range, 0.3-6 cm). Urinary cytology was positive and none of the tumors were classified as low-grade malignancy. All patients had thermal ablation of the distal ureter and perimeatic bladder mucosa with a Bugbee electrode through a cystoscope. The electrode was introduced 6 cm into the distal ureteral lumen and then extracted by a continuous rotating movement, with a 40 watt electrocoagulation power administered at the rate of 3 seconds per cm. The perimeatal mucosa was fulgurated with the same electrode, and the laparoscopic nephroureterectomy was performed.
RESULTS: There were no intraoperative complications. The mean follow-up period was 5.2 years (range, 3 months to 14 years). Three patients died from the progression of their disease. Of the remaining 24 patients, 9 had urothelial neoplasm recurrences in the bladder; none were in the ureteral trunnion or perimeatal mucosa. The other 15 patients were asymptomatic and disease-free at their final evaluation.
CONCLUSION: Thermal ablation of the distal ureteral mucosa simplifies the technique of laparoscopic nephroureterectomy for renal pelvic carcinoma and decreases the risk of cancer cell dissemination.
KEYWORDS: Ureteral laparoscopic detachment; Laparoscopic nephroureterectomy; Renal pelvic carcinoma.
CORRESPONDENCE: Prof. José Gabriel Valdivia-Uría, MD, Urbanización Santa Fe, calle 4a, no 13, Cuarte de Huerva 50410, Zaragoza, Spain ().
CITATION: UroToday Int J. 2010 Apr;3(2). doi:10.3834/uij.1944-5784.2010.04.12
ABBREVIATIONS AND ACRONYMS: TUR, transurethral resection
It has been demonstrated that leaving the distal segment of the ureter during nephroureterectomy for the treatment of upper urinary tract urothelial carcinoma results in a high incidence of cancer recurrence in both the ureteral remnant and the perimeatal mucosa . Between 30% and 75% of patients risk cancer recurrence in the surplus ureter . Recurrence is higher in tumors with high grade and when the urinary cytology is positive (60%) than when cytology is negative (17%) [3,4]. Therefore, radical nephroureterectomy is indicated for patients with high-grade tumors.
Complete, en-block removal of the kidney, ureter, and a cuff of the perimeatal bladder wall is the primary oncological goal in the radical surgery of high-grade upper urinary tract urothelial carcinoma. The purpose is to avoid any risk of tumor dissemination due to possible urine leak through the retroperitoneal space.
In 1991, Clayman and colleagues  achieved the first laparoscopic nephroureterectomy for the treatment of upper urinary tract urothelial carcinoma. Four years later, they demonstrated that this technique did not increase the risk of dissemination or tumor recurrence .
Different techniques have been proposed to obtain ureteral detachment of the bladder in the simplest way. These techniques were grouped into 5 different types plus other added variants. The safest technique is an open-cast and en-block removal of the kidney, ureter, and cuff of the bladder wall, after the laparoscopic nephroureterectomy has been completed. Another more sophisticated technique involves the detachment and transvesical laparoscopic ligation of the ureter, which includes the placement of 1-3 trocars in the bladder. Additional easier methods are to staple and section the ureterovesical funnel with an Endo GiaTM instrument or similar system, and to seal and section the structures with a LigaSure AtlasTM or similar instrument. Other proposed methods of ureteral meatus resection, ureteral pluck, and ureteral stripping are rarely being used.
Each of these surgical techniques has advantages and disadvantages. They differ not only in the terminal approach to the ureter, but also in basic oncologic principles. Some of them fail to avoid urine leakage, which may spread malignant cells from the ureter itself or from the remaining bladder orifice after the resection . Upper urinary tract carcinomas are typically very aggressive tumors. For this reason, some urologists recommend ureteral fibrin sealant injection of the distal ureter during the pluck technique, by means of laparoscopic nephroureterectomy .
At present, there are no controlled studies that demonstrate the superiority of one laparoscopic nephroureterectomy technique over another , although some techniques appear more invasive than others. All authors seem to agree that nephroureterectomies should be performed without any expression maneuver, and that the pieces should be extracted in block and protected in a specimen retrieval pouch. These procedures may contribute to the fact that free-margin and local recurrence rates after laparoscopic surgery are similar to those following conventional open surgery; some studies reveal identical disease-free survival following either technique [9,10].
When treating high-grade malignances of the pyelocalyceal system or tumors situated in the upper and middle sections of the ureter, it is very important to perform a complete excision in block with a bladder cuff even though the distal ureter is not affected. This procedure was described by Skinner in 1978 , and it continues to be the basis of a fundamental oncologic rule. The excision of the distal ureter is a prophylactic but obligatory maneuver to prevent neoplasm appearance in these areas. The neoplasms are especially susceptible to cancer recurrence because of the multifocality of urothelial disease.
The risk of disseminating malignant neoplasm cells cannot be forgotten when a large bladder perforation with a partially or fully occluded urothelial detachment is deliberately created, or when laparoscopic trocars are used in the bladder (sometimes with urothelial neoplasm inside). Accidental perforation of the urinary tract also puts the patient at risk.
The present authors describe a technique for treatment of urothelial carcinoma that they have been using for 15 years. The technique is designed to destroy the ureteral mucosa and the bladder perimeatic mucosa through thermal ablation. The authors hypothesize that this procedure creates an oncologic prophylaxis against future neoplasm outbreaks, avoids the risk of urinary leakage with possible tumor spread, and shortens both surgical and postoperative times. The purpose of the present retrospective study was to test the long-term efficacy of this technique.
A total of 27 patients with urothelial neoplasm were treated with the same procedure between 1994 and 2009. There were 17 male and 10 female patients. Their mean age was 67.4 years (range, 35-82 years).
The neoplasm was in the pyelocalyceal cavity (n = 18), the lumbar or iliac ureter (n = 5), and simultaneously in the renal pelvis and lumbar or iliac ureter (n = 4). It was on the right side for 14 patients and the left side for 13 patients. At the time of surgery, 6 patients had bladder urothelial neoplasm antecedents and 3 patients had simultaneous bladder neoplasms. The mean size of the tumors was 3.2 cm (range, 0.3-6 cm). The tumor was multifocal in 11 patients. In all patients, urinary cytology was positive and none of the tumors were classified as low-grade malignancy.
All patients were informed about their disease and the modification of the laparoscopic procedure. An informed consent was obtained.
All patients had general anesthesia. They were initially placed in a Lloyd Davies position. Cystourethroscopy was performed with a 22 Ch cystoscope (Karl Storz, Tuttlingen, Germany). In the course of this exploration, when a bladder neoplasm was detected it was treated (following selective biopsy) by electrocoagulation with the Bugbee electrode or by transurethral resection (TUR). A 26 Ch resectoscope was used if the neoplasm had a large volume.
The Bugbee 6 Fr electrode (Richard Wolf Knittlingen, Germany) was used for thermal ablation of the ureter. The electrode was placed 6 cm inside the affected ureter. It was then withdrawn approximately 1 cm every 3-4 seconds while the electrocoagulation pedal (Erbe 350, Tuebingen, Germany) was activated. The device was preprogrammed to a power of 60-80 watts.
Two technical details are important. First, the electrode should be continuously turned between the fingers while it is withdrawn, in order to prevent its distal end from becoming affixed to the ureteral wall. The surgeon should never try to reintroduce the electrode into the ureter, because it could accidentally puncture the ureteral wall and generate uncontrolled lesions in neighboring structures. Second, during the process of ureteral mucosa thermal ablation, the constant output of necrotic and detached ureteral mucosa is checked. Blood flow is observed with many bubbles into the bladder through the ureteral meatus (Figure 1).
As soon as the electrode tip began to appear in the bladder, the surgeon proceeded to electrocoagulate the ureteral meatus and its surrounding mucosa. This progressively expanded the diameter of the treated area (Figure 2). A 16 Ch Foley catheter was inserted in the bladder. The patient was then placed in a supine position with a slight lateral inclination, to proceed with the laparoscopic nephroureterectomy.
A pure laparoscopic technique was used for the first 13 cases. The remaining 14 patients had hand-assisted laparoscopy through a half-supraumbilical or infraumbilical mini-incision of about 6 cm. This change simplified the technique and provided more security. The entire specimen was bagged in a LapSac® (Cook Urological Inc, Spencer, Indiana, USA) and extracted through the same incision.
In hand-assisted laparoscopic nephroureterectomy, 3-4 trocars were used: 1 was placed pararectal at the height of the navel for optic viewing; 1 was subcostal; 1 was in the iliac fossa. The authors achieved the hand-assisted technique without the aid of a specific device for hand insertion. They used their hands forcefully and occluded the possible gas leak, temporarily using a Backhaus clamp at the skin corners.
In the first cases, the surgeons used 11 mm metal clips to occlude the renal artery, a white load Endo GiaTM stapler (Tyco Healthcare Group, Colorado, USA) for the renal vein, and a blue load for the juxtavesical ureter. However, for later cases, they used Hem-o-lok clips (WECK, Teleflex Medical, USA) for all of these structures.
At the end of the nephroureterectomy, the ureter was dissected at the juxtavesical portion. Its wall was a pale gray color from the previous electrocoagulation (Figure 3). Nevertheless, the surgeons always used double clips and cut the ureter at its entry to the bladder, far below the limit reached by thermal ablation.
The outcomes of operative time and complications were recorded. Follow-up evaluations consisted of urinary cystoscopy and urine cytology at 3, 6, and 12 months after the nephroureterectomy. If the evaluations were normal, they were repeated every year. Urography was conducted every 2 years.
There were no intraoperative complications from the laparoscopic nephroureterectomy procedure. The mean operative time for the 13 patients receiving the pure laparoscopic procedure was 320 minutes (range, 249-390 minutes). The mean operative time for the 14 patients receiving the hand-assisted laparoscopic surgery was 192 minutes (range, 169-216 minutes).
None of the patients had complications attributable to the use of the Bugbee electrode. In all cases, it was possible to remove the catheter on the 2nd or 3rd postoperative day.
The mean follow-up period was 5.2 years (range, 3 months to 14 years). During the monitoring, 3 patients died from the progression of their disease: 1 patient without bladder recurrence, 1 patient with multiple spread (both cases were initially at very advanced stages), and 1 patient with brain metastases.
Of the remaining 24 patients, 9 patients had urothelial neoplasm recurrences in the bladder; 2 of them were multifocal and recidivated. None of these recurrences were at the treated hemitrigone. The other 15 patients were asymptomatic and disease-free at their final evaluation.
Although open surgery appears to offer a better guarantee of favorable surgical outcome than laparoscopic surgery, this is not always the case. Sometimes, especially in obese patients, the surgeon does not have a good view of the deep pelvic space. The bladder cuff can become too large and its removal may compromise the function of the contralateral meatus or, more frequently, the removal may be incomplete.
Hattori et al  performed cystoscopy in patients with a previous nephroureterectomy due to an upper urinary tract neoplasm. The ipsilateral ureteral meatus was found intact in 7% of the patients whose nephroureterectomy was achieved by open surgery, and in 11% of patients whose nephroureterectomy was achieved by combined laparoscopy and open surgery. The ureteral meatus was intact in only 15% of patients who had laparascopy alone, indicating the least favorable outcome.
Transvesical laparoscopic detachment and ligation  is a difficult surgery that also carries the risk of spreading exfoliated neoplastic cells to the retrovesical space. This risk is due to the transurethral insertion of the ureteral catheter in the tumoral kidney. Moreover, insertion of trocars into the urothelial neoplastic bladder increases the risk of possible recurrence in the trocar channel. An antecedent of urothelial neoplasm is also possible. Some authors [15,16] who used up to 3 bladder trocars tried to minimize the risk of tumor spread by adding gas to distend the bladder (pneumovesicum). The laparoscopic bladder trocars inserted into these patients are still potentially dangerous due to urothelial instability. As an example, Agarwall et al  performed detachment and intravesical ligature of the ureter in 13 patients and found 5 bladder recurrences, 2 of which were close to the ureteral scar.
Laparoscopic sectioning and stapling of the ureterovesical funnel with an EndoGiaTM or similar instrument has the potential drawback of stone formation on titanium clips that migrate inside the bladder . Tsivian et al  proposed sealing and cutting the ureterovesical funnel using the LigaSure AtlasTM. According to them, the heat produced by this device does not extend deeper than 2 mm. This opinion is not necessarily shared by surgeons who perform hand-assisted laparoscopy and feel the heat generated by these devices with their fingers. The heat applied to the bladder wall funnel (resulting from ureteral traction) could potentially affect the functionality of the contralateral ureteral meatus, because it is not easy to calculate the trigonal area captured by the branches of this device outside the bladder. This problem was already indicated by Skinner in 1978  in his description of open nephroureterectomy.
When TUR is performed to detach the ureteral meatus, the procedure of ureteral stripping leaves a wide communication between the bladder and the retroperitoneal space and the catheter needs to be in place for a long time. These procedures increase the risk of spreading tumor cells. In a review article, Laguna et al  found a bladder carcinoma recurrence rate of 19.3% after ureteral stripping, and a recurrence rate of 24% after transurethral resection of the intramural ureter. Vardi et al  detached the ureter with an electrode through a flexible cystoscope, at the end of hand-assisted laparoscopic nephroureterectomy. The authors acknowledged that although they performed ureter detachment after laparoscopic clipping, there was a potential risk of tumor spread because the bladder was left open.
With the technique proposed by the present authors, the hypothetical tumor cell dissemination out of the bladder is impossible and there is no risk of contralateral meatus thermal injury. The last 6 cm of the ureteral mucosa and the corresponding hemitrigone mucosa are not perforated and they undergo necrosis. The thermal ablation of the last 6 cm of ureteral mucosa makes it easy to see the pale gray portion of the ureteral wall that was previously electrocoagulated. It is then enough to double clip and cut its entry into the bladder, 3-4 cm below the limit reached by thermal ablation of the ureteral wall. This procedure allows the removal of the bladder catheter the day after surgery.
The present authors prefer to electrocoagulate the surrounding meatus of the bladder mucosa rather than resect it, so that they do not have to replace the cystoscope with a resectoscope. From a scientific point of view, they lose the opportunity of knowing if this mucosal area actually had atypical cells. However, if the endoscopic aspect is good, they reduce morbidity and surgical time by performing only the electrofulguration with the same Bugbee electrode.
The ureter cutting point is always below the area previously treated by endoscopic electrocoagulation. Moreover, the surgical procedure is highly simplified because it requires a cystoscope and a 6 Fr Bugbee electrode to catheterize the last 6 ureteral cm. Performing hand-assisted laparoscopic nephroureterectomy further simplifies the procedure and provides additional security. Finally, the parietal incision size is not larger than that required to remove the kidney and ureter in block .
Berger and Fergany  conducted a recent literature review and concluded that long-term follow-up studies after laparoscopic nephroureterectomy are still sparse . It was suggested that additional studies are needed to reinforce the multicenter study of El Fettouh et al . These authors reported the results of 116 patients who underwent laparoscopic nephroureterectomy, with a median follow-up of 25 months. Positive margins were identified in 4.5% of the patients, local recurrence in 1.7%, and bladder recurrence in 24%. The mean time to recurrence was 13.9 months. In the present study, although the number of patients is reduced when compared with the larger study, there was no local recurrence. However, there was a 33.3% recurrence of bladder cancer, possibly because the follow-up period extended to 14 years.
Although larger numbers of patients are needed to extract definitive conclusions, the results of the present study indicate that thermal ablation of the distal ureteral mucosa and the corresponding hemitrigonal mucosa simplifies laparoscopic nephroureterectomy. The procedure also decreases morbidity and provides security from the spread of malignant cells. This technique is contraindicated in cases of pelvic ureteral tumors, but it appears to provide successful results for other types of patients with upper urinary tract malignant urothelial neoplasm.
Conflict of Interest: None declared.
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