To describe a purely laparoscopic nephroureterectomy approach that avoids the disadvantages of transurethral bladder cuff excision and open/laparoscopic distal ureterectomy using the EndoGIA.
A standard transperitoneal laparoscopic nephrectomy is carried out through three or four ports in the flank. The ureter is dissected caudally into the pelvis. Two additional (5- and 10-mm) trocars are placed in the ipsilateral lower abdomen. Caudal ureteral dissection continues until the detrusor muscle fibers at the ureterovesical junction are identified. A 1-cm area of bladder adventitia around the ureterovesical junction is cleared. The ureter is retracted upward and laterally, tenting up the bladder wall. The bladder cuff is excised using a 10-mm LigaSure Atlas and detached from the bladder. A 6-cm lower-quadrant incision is used to remove the specimen in an Endocatch bag. An indwelling 16F Foley catheter is then placed.
Thirteen adult patients with suspected upper-tract transitional cell carcinoma underwent this surgical technique (operative time: 170–270
The described procedure adheres strictly to oncologic principles (removal of the affected renal unit without opening the urinary tract), and circumvents the need for transurethral/intraureteral instrumentation and patient repositioning.
Keywords: Distal ureterectomy, Laparoscopy, Nephroureterectomy, Transitional cell carcinoma.
Nephroureterectomy with the removal of the bladder cuff is the standard care for patients with upper-tract transitional cell carcinoma (TCC). Several methods of securing the distal ureter and bladder cuff have been suggested since Clayman et al.'s  first description of laparoscopic nephroureterectomy in 1991, but the best way to manage the distal ureter remains in dispute  and . We present our technique of a purely laparoscopic nephroureterectomy (LNU) performed entirely through laparoscopic ports, avoiding the disadvantages of transurethral bladder cuff excision and open/laparoscopic distal ureterectomy using the EndoGIA (i.e., breach of the urinary tract, transurethral and/or intraureteral manipulation, possible viable tumor cell entrapment between the EndoGIA clips rows with possible tumor dissemination, and intraoperative patient repositioning).
First, a standard laparoscopic transperitoneal nephrectomy in a full flank position is performed. Three ports are used: one 10-mm trocar is placed by the Hasson technique supraumbilically, one 5-mm port is placed in the midclavicular line in the ipsilateral upper quadrant, and one 12-mm trocar is placed above the first one in the midline between the xyphoid and the first port. An optional fourth 5-mm trocar may be inserted above the former trocar on the right side and in the anterior axillary line on the left side (Fig. 1). After mobilization of the colon, the ureter is identified and clipped without trans-section to prevent inadvertent urine spillage. The renal artery and vein are dissected and divided, and the kidney is circumferentially mobilized, sparing the adrenal. The ureter is then dissected caudally into the pelvis. An additional two (5- and 10-mm) trocars are placed in the lower abdomen (Fig. 1). After trans-section of the lateral umbilical ligament, dissection is continued caudally until the detrusor muscle fibers at the ureterovesical junction are identified. The ureter is then retracted superior and laterally, tenting up the bladder wall at the ureterovesical junction. A 1-cm area of bladder adventitia around the ureterovesical junction is cleared, and a bladder cuff is incised with the use of a 10-mm LigaSure Atlas (Valleylab, Tyco Healthcare UK Ltd, Gosport, UK; Fig. 2). The bladder wall from one side and kidney together with the ureter and bladder cuff from the other side remain sealed after incision and detachment (Fig. 3). Additional sutures on the bladder wall are not required. After detaching the specimen, the camera is moved to the 12-mm trocar, and an Endocatch II bag (15
Our postoperative follow-up was conducted according to established protocols of upper tract TCC .
Thirteen patients (10 males, 3 females; age range: 47–84 yr; mean: 64.5) with suspected upper-tract TCC underwent surgery using this technique. The operative time ranged between 170–270
LNU has been established as a safe and reproducible, mini-invasive technique for treating upper-tract TCC in medical centers worldwide , , , , and . Compared with the “open” technique, the laparoscopic approach has been shown to result in decreased blood loss, less postoperative pain, and shorter hospitalization , , and . LNU is also associated with a faster recovery time and return to normal activities  and . With LNU, special attention needs to be paid to fastidious management of the distal ureter, to avoid the high incidence of recurrences in the ureteral stump and perimeatal bladder mucosa that have been reported in patients treated with incomplete ureterectomy .
The technique of distal ureterectomy and bladder cuff excision has not yet been standardized . The five major approaches in current practice include an open technique, a transurethral resection of the ureteral orifice (“pluck” technique), an intussusception technique, a transvesical laparoscopic detachment and ligation technique, and laparoscopic stapling of the distal ureter and bladder cuff  and . Each technique has distinct advantages and disadvantages, and differs not only in technical approach, but in the observation of oncologic principles as well.
The drawbacks of the transvesical laparoscopic detachment and ligation technique include the risks of fluid extravasation with potential tumor cell exfoliation after insertion of the ureteral catheter into the tumor-bearing unit and of tumor seeding. The two intravesical ports may be real risk factors for the occurrence of port-site metastases if bladder tumors are present. Finally, the learning curve of this technique is a difficult one . The transurethral resection of the intramural ureter during the pluck technique exposes the extravesical space to potential seeding, recurrence at the resection area, and bladder carcinoma recurrence. . Indeed, Arango et al.  reported a case of tumor implantation at the endoscopic resection area, and some urologists have abandoned the technique altogether . Laguna et al.  in their review found bladder carcinoma recurrence of 19.3% and 24% for ureteral stripping and “pluck” technique, respectively. The complication rate for endoscopic ureteral removal was 10.3%. The intussusception technique is contraindicated for any tumor within the ureter. The open technique carries a risk of contralateral ureteric orifice compromise, because the contralateral trigone may be inadvertently included in a right-angle clamp or suture line . In addition, an open extravesical technique does not necessarily guarantee adequate excision of the entire ureter with the bladder cuff, particularly when performed blindly . This approach also may be difficult in obese patients. In a series by Hattori et al. , the ipsilateral ureteral orifices were identified in eight patients (15%) of the laparoscopic stapler group, in four (7%) open surgery patients, and in four (11%) combined laparoscopy patients. Although at 3-mo follow-up, no ureteral orifices were present on endoscopy in our series, our technique is indeed also “blind” and may leave some intact orifices. All four of these techniques require intraoperative patient repositioning, and may be associated with potential urethral complications and prolonged operating time.
The use of a laparoscopic stapler also has some disadvantages: (1) handling of the stapler is difficult in the restricted pelvic area, (2) the titanium staple lines have potential risk of stone formation  and , and (3) the oncologic safety of stapling has been questioned. Recently, Hattori et al.  reported that stone formation has occurred in 3 (5.7%) of 53 patients at an average of 20 mo postoperatively. The stones were removed during follow-up cystoscopy. Venkatesh et al.  have shown that deployment of a stapler resulted in viable cells within the staple lines at the ureterovesical junction and bladder wall in a porcine model. In a human series by Matin and Gill , the rate of recurrence in a group of patients whose surgery included the use of a laparoscopic stapling device was higher compared with the group in which the surgical method involved cystoscopically secured detachment and ligation. Suturing and knotting in this area are challenging for the average urologist and may be successfully performed only by a very experienced laparoscopist. Few laparoscopic urologists perform pure LNU with suture of the bladder.
The practice of excising a cuff of periureteral bladder tissue en bloc with the nephrouretectomy specimen reflects the hallmark of an oncologic principle . In this scenario, removal of the renal unit without opening the urinary system and, thus, preventing possible spillage of tumor cell is mandatory, as was recently emphasized again in a study by Herawi et al. . Our experience with the LigaSure Atlas device has been highly satisfactory. The LigaSure is a computer-controlled bipolar diathermy system designed to optimally seal vessels <7
Our purely laparoscopic technique allows precise excision of the complete bladder cuff without breach of the urinary system, thus preventing spillage and enabling the removal of the entire specimen en bloc.
We describe an entirely laparoscopic removal of the kidney, ureter, and bladder cuff by a procedure that strictly adheres to oncologic principles (removal of the affected renal unit without opening the urinary tract), and obviates the need for transurethral and intraureteral instrumentation as well as intraoperative repositioning of the patient.
Conflicts of interest
The authors have nothing to disclose.
-  R.V. Clayman, L.R. Kavoussi, R.S. Figenshau, P. Chandhoke, D.M. Albala. Laparoscopic nephroureterectomy: initial clinical case report. J Laparoendosc Surg. 1991;1:343-349 Crossref.
-  M.P. Laguna, J.J. de la Rosette. The endoscopic approach to the distal ureter in nephroureterectomy for upper urinary tract tumor. J Urol. 2001;166:2017-2022
-  L. Salomon, A. Hoznek, A. Cicco, D. Gasman, D.K. Chopin, C.C. Abbou. Retroperitoneoscopic nephroureterectomy for renal pelvic tumors with a single iliac incision. J Urol. 1999;161:541-544
-  S. Matin, I.S. Gill. Recurrence and survival following laparoscopic radical nephroureterectomy with various forms of bladder cuff control. J Urol. 2005;173:395-400 Crossref.
-  J.J. Rassweiler, M. Schulze, R. Marrero, T. Frede, J.P. Redorta, P. Bassi. Laparoscopic nephroureterectomy for upper urinary tract transitional cell carcinoma: is it better than open surgery?. Eur Urol. 2004;46:690-697 Crossref.
-  A.L. Shalhav, M.D. Dunn, A.J. Portis, A.M. Elbahnassy, E.M. McDougall, R.V. Clayman. Laparoscopic nephroureterectomy for upper tract transitional cell cancer: the Washington University experience. J Urol. 2000;163:1100-1104
-  S.A. McNeill, M. Chrisofos, D.A. Tolley. The long-term outcome after laparoscopic nephroureterectomy: a comparison with open nephroureterectomy. BJU Int. 2000;86:619-623
-  T.W. Jarrett, D.Y. Chan, J.A. Cadeddu, L.R. Kavoussi. Laparoscopic nephroureterectomy for the treatment of transitional cell carcinoma of the upper urinary tract. Urology. 2001;57:448-453 Crossref.
-  H.A. El Fettouh, J.J. Rassweiler, M. Schulze, et al. Laparoscopic radical nephroureterectomy: results of an international multicentric study. Eur Urol. 2002;42:447-452 Crossref.
-  G. Apul, A.K. Hemal, N.P. Gupta. Retroperitoneal laparoscopic radical nephrectomy and nephroureterectomy and comparison with open surgery. World J Urol. 2002;20:219-223
-  H.C. Klingler, M. Lodde, A. Pycha, M. Remzi, J. Janetschek, M. Marberger. Modified laparoscopic nephroureterectomy for treatment of upper urinary tract transitional cell cancer is not associated with an increased risk of tumour recurrence. Eur Urol. 2003;44:442-447 Crossref.
-  M. Tsujihata, N. Nonomura, A. Tsujimura, K. Yoshimura, Y. Miyagava, A. Okuyama. Laparoscopic nephroureterectomy for upper tract transitional cell carcinoma: comparison of laparoscopic and open surgery. Eur Urol. 2006;49:332-336 Abstract, Full-text, PDF, Crossref.
-  J.R. Steinberg, S.F. Matin. Laparoscopic radical nephroureterectomy: dilemma of the distal ureter. Curr Opin Urol. 2004;14:61-65 Crossref.
-  D.W. Strong, H.D. Pearce, E.S. Tank, C.V. Hodges. The ureteral stump after nephroureterectomy. J Urol. 1976;115:654-655
-  O. Arango, O. Bielsa, J. Carles, et al. Massive tumor implantation in the endoscopic resected area in modified nephroureterectomy. J Urol. 1997;157:1839
-  D.R. Jones, C.U. Moisey. A cautionary tale of the modified “pluck” nephroureterectomy. Br J Urol. 1999;71:486-487
-  R. Hattori, Y. Yoshino, M. Goton, M. Katon, O. Kamihira, Y. Ono. Laparoscopic nephroureterectomy for transitional cell carcinoma of renal pelvis and ureter: Nagoya experience. Urology. 2006;67:701-705 Crossref.
-  S.M. Baughman, W. Sexton, J.T. Bishoff. Multiple intravesical linear staples identified during surveillance cystoscopy after laparoscopic nephroureterectomy. Urology. 2003;62:351 Crossref.
-  R. Venkatesh, J. Rehman, J. Landman, et al. Determination of cell viability after laparoscopic tissue stapling in a porcine model. J Endourol. 2005;19:744-747 Crossref.
-  M. Herawi, J.T. Leppert, G.V. Thomas, J.B. DeKernion, J.I. Epstein. Implants of noninvasive papillary urothelial carcinoma in peritoneum and ileocolonic neobladder: support for “seed and soil” hypothesis of bladder recurrence. Urology. 2006;67:746-750 Crossref.
-  S. Sengupta, D.R. Webb. Use of a computer-controlled bipolar diathermy system in radical prostatectomies and other open urological surgery. ANZ J Surg. 2001;71:538-540 Crossref.
-  J.S. Kennedy, P.L. Stranahan, K.D. Taylor, J.G. Chandler. High-burst-strength, feedback-controlled bipolar vessel sealing. Surg Endosc. 1998;12:876-878 Crossref.
Department of Urologic Surgery, Wolfson Medical Center, Holon, and the Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
Presented at XXIst Congress of the European Association of Urology, Paris, France, 2006, April 5–8.
© 2006 European Association of Urology, Published by Elsevier B.V.