Transurethral Approach to the Distal Ureter in Nephroureterectomy: Transurethral Extraction vs. Pluck Technique with Long-Term Follow-Up

European Urology European Urology 46 (2004) 741 747 Transurethral Approach to the Distal Ureter in Nephroureterectomy: Transurethral Extraction vs. Pluck Technique with Long-Term Follow-Up Burkhard Ubrig*, Michael Boenig, Michael Waldner, Stephan Roth Department of Urology, Klinik für Urologie und Kinderurologie, University of Witten/Herdecke, HELIOS Klinikum Wuppertal, Heusnerstr. 40, D-42283 Wuppertal, Germany Accepted 8 July 2004 Available online 28 July 2004 Abstract Objectives: We retrospectively compared two techniques of transurethral management of the lower ureter in nephroureterectomy. Patients and Methods: From August 1992 to December 2003, 34 patients underwent either transurethral detachment of the intramural ureter and cephalad extraction ( pluck ; Group 1, N = 18) or transection of the ureter with subsequent transurethral extraction (Group 2, N = 16). Choice of technique was left to the operating surgeon. All patients with upper tract urothelial carcinoma (TCC) were regularly followed by cystoscopy and abdominal ultrasound. Results: Of the 34 patients, 29 had upper tract TCC. Mean follow-up in these was 44 months (range: 1 129), with 24 (83.8%) over 24 months. On follow-up, 14 bladder tumors (all superficial) occurred in 7 patients (24.1%), but in no case on the scar of the excised ureteral orifice. No extravesical recurrences in the former ureteral bed were found. Of the 29 with upper tract TCC, 19 (65.5%) are alive without disease (median 45 months, range: 6 129), 5 (17.2%) have died with no evidence of disease (median 34 months, range: 20 58), and 4 (13.8%) have died from progressive disease (median 18 months, range: 1 33); 1 patient was lost to follow-up at 34 months with no evidence of disease. Differences between techniques with regard to blood loss, operative time, complications, and oncologic outcome were not significant. Conclusion: Both techniques proved technically and oncologically safe. Bladder tumor recurrence rate was in the range reported for classic nephroureterectomy. No extravesical tumor recurrence in the former ureteral bed or on the scar of the resected ureteral orifice occurred. # 2004 Elsevier B.V. All rights reserved. Keywords: Ureter; Transitional cell carcinoma; Reflux nephropathy; Ureterectomy 1. Introduction Nephroureterectomy is performed for transitional cell carcinoma (TCC) of the upper urinary tract and for some benign conditions such as reflux nephropathy or renal tuberculosis. It includes removal of the kidney and the complete ureter, including a cuff of bladder mucosa around the targeted ureteral orifice. If the distal * Corresponding author. Tel. +49 202 8960; Fax: +49 202 8963404. E-mail address: bubrig@wuppertal.helios-kliniken.de (B. Ubrig). ureter is not resected in upper tract TCC, tumor will recur in the ureteral stump in 19 30% [1]. Classic open nephroureterectomy requires one long abdominal incision or in the case of lumbar nephrectomy a second lower abdominal incision to approach the distal ureter, which is out of reach from a flank incision. Additionally, one or two cystotomies are required [2]. A transurethral approach [3,4] first described by McDonald et al. [5], obviates the lower abdominal incision and may lessen operative time and patient discomfort. 0302-2838/$ see front matter # 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.eururo.2004.07.008

742 B. Ubrig et al. / European Urology 46 (2004) 741 747 In laparoscopic nephroureterectomy, the best way to manage the distal ureter is still in dispute [6 9], but transurethral management has been sucessfully applied [6,8]. Based on case reports, some authors have suggested that the transurethral approach in patients with upper tract TCC may be associated with higher recurrence rates of invasive bladder tumor extravesically and at the site of the excised ureteral orifice and with increased rates of progression [10 13]. However, most reports describe technical modifications of the procedure and do not provide thorough long-term oncologic followup. Owing to the rarity of upper tract TCC, only two reports have more than 20 patients [4 14]. The best method for the transurethral approach to the distal ureter in terms of efficiency and oncologic safety remains controversial. The many published modifications of the procedure orginally described may be subdivided into two categories. The pluck technique comprises primary transurethral detachment (either resection or excision) of the intramural ureter with a resectoscope and subsequent cephalad extraction ( plucking ) during nephrectomy [5,15]. In this technique urine possibly loaden with tumor cells continues to flow and might extravasate into the perivesical space until the kidney and ureter are removed. Nevertheless, this technique has predominated [4,15]. In the transurethral extraction technique, the ureter is transected above the iliac vessels during nephrectomy; subsequently, the ureteral orifice is excised transurethrally and the distal ureter extracted. During this transurethral extraction, the ureteral stump is either inverted [2,16] or compressed [17]. Comparisons of the two techniques have so far not been reported. In 1996, one of us (S.R.) published the first results of a modified technique for transurethral extraction [17]. We now compare intra- and perioperative data and long-term oncologic follow-up of this technique with primary ureteral detachment and cephalad extraction ( pluck technique). 2. Patients and methods We retrospectively analyzed the follow-up and outcome of all 34 patients that underwent either of two transurethral approaches to the lower ureter during nephroureterectomy (open surgical in 32, retroperitoneoscopic in 2) from August 1992 to December 2003. Patients had been assigned to technique by the operating surgeon (B.U., M.W., S.R.), but TCC of the lower ureter (below the ureteral crossing with the iliac vessels) had been an exclusion criterion. During this same time period, 79 patients underwent classic two-incision nephroureterectomy mainly for resident training or Table 1 Patient characteristics Variable because of tumor below the crossing of the ureter with the iliac vessels. The majority of patients (n = 29, 85.3%) had upper tract TCC (see Table 1). Among the other 5, 2 patients underwent surgery under suspicion of TCC and postoperative histology revealed Bellini duct carcinoma in 1 and renal cell carcinoma in the other, and 3 patients had benign conditions (reflux nephropathy in 2, ureteral stricture in 1). All patients were regularly followed by us or their outpatient clinics at 3 6 months intervals, including abdominal ultrasound and cystoscopy. The last follow-up evaluation, in December 2003, consisted of interview, physical examination, ultrasonography of the abdomen and urogenital tract, intravenous urography, and urethrocystoscopy in all surviving patients. Data of deceased patients were retrospectively gathered from the files. All patients with ultrasonographic or clinical suspicion of metastasis underwent abdominal CT. Data were analyzed with standard statistical software (SPSS 1, Version 12.0 for Windows 1, Munich, Germany). The x 2 -test was used to compare percentage frequencies, and 5-year disease-specific survival was calculated by the Kaplan Meier method with the log-rank test; p = 0.05 was considered significant. 2.1. The pluck technique (Group 1; N = 18) With the patient in the lithotomy position, a 5 French ureteral catheter is inserted into the targeted ureter, and a resectoscope is introduced alongside into the bladder (see Fig. 1). With a hook electrode, the bladder mucosa is circumferentially incised 10 mm from the center of the ureteral orifice; this incision is then carried down to the level of the perivesical fat until the intramural ureter is completely detached. (The ureteral catheter facilitates preparation of the intramural ureter by straightening it and lifting up the ipsilateral hemitrigone.) After complete hemostasis, a transurethral catheter is inserted. The patient is repositioned into the lateral decubitus position for nephroureterectomy and, as the first step, the ureter is identified and ligated below the suspected distal border of the tumor to prevent further urinary extravasation into the perivesical space. After retroperitoneal nephrectomy is completed, the distal ureter is digitally mobilized gently between the tips of the index finger and thumb completely down to the ureterovesical junction and extracted. The ureter is checked for complete extraction by identifying the cutting edge of the bladder cuff at the distal No. No. of patients 34 Mean/median age (year) 63.4/64.1 Age range 21.8 94.3 Gender (men/women) 24/10 Right/left side 10/24 Mean/median follow-up (month) 37/46 Range 1 138 Nephrectomy Open (lumbar incision) 32 Laparoscopic (retroperitoneoscopic) 2 Histopathologic result Upper tract TCC 29 Bellini duct carcinoma 1 Renal cell carcinoma 1 Reflux nephropathy 2 Stricture (post diverticulitis) 1

B. Ubrig et al. / European Urology 46 (2004) 741 747 743 Fig. 1. Pluck technique (Group 1): The intramural ureter is circumferentially excised. A 5 French ureteral catheter may be inserted to facilitate excision of the orifice and later ureteral dissection. After repositioning, the ureter is first ligated below the tumor to prevent tumor cell spillage. The lower ureter is mobilized and, when the ureter is completely detached, it is plucked. Transurethral extraction (Group 2): During nephrectomy the ureter is first transected. The ureteral end with stylet inside of catheter is kinked and fixed with 2 ligatures. Under traction on the catheter the intramural ureter is excised, and the distal ureter is transurethrally extracted. ureteral end. A Foley catheter is left indwelling in this and the following technique, with cystography performed on day 5 7 before removal. 2.2. Transurethral extraction of the ureteral stump (Group 2; N = 16) The procedure has been described in detail elsewhere [17]. Briefly, after placement of a 5 French catheter into the targeted ureter, the patient is placed in the lateral decubitus position for nephrectomy. The ureter is identified early and transected below the suspected tumor between ligatures, about 3 cm above its crossing with the iliac vessels. The kidney with the proximal ureter is removed. The end of the ureteral catheter is then kinked (with the metal stylet of the catheter left indwelling) and secured to the ureteral stump with ligatures. Then the ureter is digitally dissected down to the ureterovesical junction until no lateral attachments remain. After wound closure the patient is repositioned into the lithotomy position. A resectoscope with a hook electrode is then introduced alongside the ureteral catheter. The catheter is held under constant gentle traction, compressing the ureter and causing it to bulge against the bladder wall behind the orifice (see Fig. 1). The bladder mucosa is incised around the ureteral orfice in a radius (about 1 cm) sufficient to allow the compressed ureter to pass through into the bladder, creating a cuff. Subsequently, the ureter is extracted transurethrally by traction on the ureteral catheter. In 4 cases the modified lithotomy position of Clayman et al. was used, which allows the surgeon and endoscopist to work simultaneously [2]. The 2 retroperitoneoscopic cases in this study were Group 2 patients (transurethral extraction): after meticulous laparoscopic ureterolysis, the ureter was transected from the extraction site of the kidney and the procedure smoothly completed as described above. 3. Results Intra- and perioperative data stratified by group are summarized in Table 2. Three patients required conversion to open ureterectomy, 1 in Group 1 (5.5%) and 2 in Group 2 (18.8%). In 2 of these patients periureteral fibrosis (consequent to diverticulitis in 1 and open stone surgery in 1) rendered adequate mobilization of the lower ureter impossible through the loin incision. Table 2 Intra- and perioperative data stratified by technique Variable Group 1 ( pluck ) Group 2 (transurethral extraction) p-value No. of patients 18 16 Median age (range) 64.7 (51.3 94.3) 63.6 (21.8 78.8) 0.132 Conversion to open ureterectomy 1 2 0.233 Reasons for conversion Anchored pelvic ureter 1 1 0.932 Ureteral catheter loss 1 Total operative time (min) [Median (range)] 153 (95 290) 165 (115 245) 0.564 Nephrectomy 118 (63 205) 149 (90 225) 0.257 Endoscopy 34 (25 110) 30 (10 45) 0.824 Intra- and postoperative bleeding Estimated intraoperative blood loss (ml) 128 (40 300) 150 (10 350) 0.248 Hemoglobin difference (g/dl) a 1.4 (0 2.7) 2.4 (0 5.3) 0.166 Hematocrit difference (%) a 0.052 (0.002 0.074) 0.066 (0.015 0.139) 0.123 Blood transfusions Median Foley days 7 (5 12) 7 (4 9) 0.064 Perioperative complications 1 1 0.932 Type of complication cardiac decompensation pneumonia Median hospital days 11 (7 22) 10 (7 16) 0.277 a 1 day preoperative vs. 1 day postoperative

744 B. Ubrig et al. / European Urology 46 (2004) 741 747 Table 3 Baseline tumor characteristics of patients with upper tract TCC Variable Total Group 1 ( pluck ) Group 2 (transurethral extraction) p-value No. patients 29 17 12 No. patients min. 24 months follow-up 24 12 12 pta 12 8 4 0.460 pt1 9 3 6 0.064 pt2 pt3 7 5 2 0.430 pt4 1 1 0.393 Concomitant ptis 2 1 1 0.798 Multifocal tumor growth 7 6 1 0.393 pn+ 1 1 0.393 M+ 1 1 0.393 Grade 1 4 2 2 0.706 Grade 2 14 7 7 0.362 Grade 3 11 8 3 0.228 Location primary tumor Renal pelvis 27 16 11 Upper ureter 2 1 1 No. with bladder tumor before NU a 5 5 0.039 a NU = nephroureterectomy. In 1 patient in Group 2, the catheter became detached from the ureter because of inadequate fixation and ureterolysis before extraction. Open surgical ureterolysis was performed and the lower ureter was then easily removed in all 3 cases. Apart from the conversions, no intraoperative complications occurred. No significant intra- or perioperative bleeding arose in either group and blood transfusion was not required. Operative time and complications were not significantly different between the two groups (Table 2). Transient cardiac decompensation and pneumonia occurred in 1 patient each postoperatively, both related to patient-specific risk factors. The Foley catheter was usually removed on day 5 to 7 after cystographic exclusion of extravasation. In 2 patients (5.8%) cystography on day 7 demonstrated minor leakage, but this resolved spontaneously by day 10 and 12 with further catheter drainage. The tumor stage and grade in the 29 patients (85%) with upper tract TCC are summarized in Table 3. Their oncologic follow-up data, with a focus on bladder tumors, are outlined in Table 4. Bladder cancer occurred in 7 patients (24.1%) on follow-up, a total of 14 tumors, all superficial (pta, pt1); 5 of these 7 patients had a history of bladder cancer before nephroureterectomy. In no patient did tumor recur in Table 4 Follow-up results of patients with upper tract TCC Variable Total Group 1 ( pluck ) Group 2 (transurethral extraction) p-value No patients 29 17 12 Mean/median follow-up (months) 44/36 33/33 58/37 No. extravesical recurrence (ureteral bed) No. retroperitoneal recurrence renal hilum 1 0.393 No. progressive TCC 3 1 0.474 Bladder cancer Total no. patients with bladder cancer 8 6 2 0.269 No. with bladder tumor after NU a 7 5 2 0.430 Total no. bladder tumors treated after NU a 14 9 5 0.288 No. superficial 14 9 5 0.288 No. invasive No. bladder recurrence at excision Site of former ureteral orifice a NU = nephroureterectomy.

B. Ubrig et al. / European Urology 46 (2004) 741 747 745 Table 5 Progression in patients with upper tract TCC Patient age Primary tumor Outcome (months of follow-up) Group I ( pluck ) 59 renal pelvis (pt3 pnx, G3,R0) metastasis before surgery; palliative nephroureterectomy; DOD (1) 73 renal pelvis (pt4 pl1 pn0 G3 R0) recurrence in former renal hilum and systemic progression; DOD (6) 61 renal pelvis (pta, G2, pn0, R0) paraaortic nodes, pulmonary and hepatic metastasis; DOD (33) a Group II (transurethral extraction) 64 renal pelvis (pt3 G3 pn0 MO) local recurrence renal bed, paraaortic nodes, collar lymph nodes; DOD (30) a Biopsy proven metastasis of urothelial cancer; other malignancies excluded. the area of the former ureteral orifice, including 1 who had to undergo radical cystectomy for multifocal pt1 G3 bladder cancer. Four patients developed metastatic urothelial cancer and eventually died therefrom within 33 months of nephroureterectomy. In no case could progressive disease be linked to the minimally invasive extraction of the distal ureter. Detailed information on location of metastasis and survival time are given in Table 5. All 4 patients had undergone abdominal computed tomography (CT), and the imaging studies were reviewed for signs of extravesical recurrence in the former ureteral bed, but no such recurrence could be diagnosed. Another patient was last confirmed disease-free at 34 months and then lost to follow-up. For survival analysis he was classified as dead of disease. At the end of analysis, of the 29 patients treated for upper tract TCC, 19 (65.5%) were alive without disease after a median follow-up of 44.8 months (range: 6 129), 5 (17.2%) had died with no evidence of disease after a median 34 months (range: 20 58), and 4 (13.8%) had died of disease after a median 18 months (range: 1 33). Cause-specific mortality was calculated at 17.2% (5/29), including the 1 patient lost to followup after 34 months with no evidence of disease. decision of the responsible surgeon, generally patients in Group 1 ( pluck ) were older (Table 2). In this study, both techniques proved oncologically safe, as has been found by others (Fig. 2) [2,3,14 18]. A disease-specific survival rate of 82.7% with a mean follow-up of 44 months compares favorably to published results of classic nephroureterectomy and a recent large series of laparoscopic nephroureterectomy [1,6]. The rate of bladder tumor recurrences after endoscopic management of the distal ureter has been reported 19.3% in a total of 62 patients in four prior studies [2 4,18] and was 24.1% in ours. This is in the range of 21 30% reported after classic nephroureterectomy [1,4]. In a single report, Saika and coworkers recently found a significantly better bladder recurrence free rate with the classic technique at 3 years than with transurethral stripping (75.0% vs. 57.7% respectively) [18]. They had prospectively compared the outcome of 32 patients that underwent classic nephroureterectomy 4. Discussion During nephroureterectomy with a cuff of bladder mucosa, transurethral management of the distal ureter obviates open cystotomies and incision of the lower abdominal wall to approach the ureterovesical junction. It may thus save patient discomfort and surgical time [3]. Its technical modifications may be subdivided into two categories: the pluck [5,14,15] and transurethral extraction [17] techniques. To our knowledge, the present study is the first to compare these two techniques in a single-center experience with longterm oncologic follow-up of patients with upper-tract TCC. Although patients were assigned to technique by Fig. 2. Five-year disease-specific survival after nephroureterectomy in upper tract TCC with pluck vs. transurethral extraction technique (p = 0.7292).

746 B. Ubrig et al. / European Urology 46 (2004) 741 747 versus 28 with endoscopically assisted transurethral stripping. As in our study, all of the bladder recurrences were superficial and no tumor recurrence was found on the scar of resection [18]. Bladder recurrence after endoscopic management of the distal ureter should be studied in further prospective trials. Both techniques compared in our study are technically safe. Apart from conversions (3/34), no significant intra- or perioperative complications or bleeding occurred in this study, nor have any been reported by others [3,4,10,14 18]. Even more than in conventional resection, coagulation must be meticulous because postoperative irrigation will result in retroperitoneal fluid collection. By maintaining intravesical pressure low during resection, extravasation of irrigation fluid through the perforating defect will remain low and the defect will not be torn apart by undue bladder distension. Contraindications for both techniques are the presence of tumor in the distal ureter, a synchronous bladder tumor, and double ureter. Conditions that cause ureteral fixation to the iliac vessels or pelvis (e.g., prior surgery, irradiation, retroperitoneal fibrosis, pelvic arterial aneurysm) may render digital ureterolysis perilous, at least in open nephroureterectomy, and require conversion. This occurred in 2 of our patients. The pluck procedure is straightforward and easily learned. The ureter is extracted from the site of nephrectomy and is usually entirely under digital control. Other authors have proposed resection of the ureteral orifice instead [5,14,15]. However, in our view the circumferential excision down into the perivesical fat to detach the ureter from the bladder is more precise and avoids potential loss of resection chips into the perivesical space. After extraction, the surgeon must check the distal border of the extracted ureter. This will be greatly facilitated by having a clean-cut bladder cuff. Nevertheless, the pluck technique (Group 1) may lead to spillage of tumor cell loaded urine into the perivesical space after detachment of the intramural ureter and before nephroureterectomy is completed. All 4 recurrences in the former perivesical ureteral bed that have been reported after minimally invasive management of the distal ureter during nephroureterectomy were directly attributed to tumor cell spillage during the pluck technique [10,12,13]. The wide and deep resection of the intramural ureter used in these cases, instead of excision as proposed, might have promoted tumor cell seeding because the urine is directly ejected into the perivesical space until ureteral ligation during nephrectomy. Abercrombie et al. [15] have suggested meticulous coagulation of the ureteral orifice after detachment to prevent extravasation, but the efficacy of this has not been proved. Gill and coworkers excised the intramural ureter in a fashion similar to our technique and ligated the intramural ureter with an endoloop as a preparation for the pluck procedure in laparoscopic nephroureterectomy [6]. This method seems promising, but long-term results are pending. Generally, the risk of tumor cell seeding of urothelial cancer after perforating resection in the urinary tract does not seem to be very high as demonstrated by recent experience from conservative ureteroscopic and percutaneous surgery of upper tract TCC and the rarity of invasive bladder recurrence after perforating bladder tumor resections. Seeding might be more common with high grade disease [19,20]. In the transurethral extraction technique, the ureter is transected and ligated and no tumor cell loaded urine can extravasate. Local recurrence in the former ureteral bed has never been attributed to this method [4,18]. In this technique, before commencing transurethral extraction, meticulous digital or laparoscopic mobilization of the distal ureter down to the ureterovesical junction is essential; if too many strands are left above the junction, the catheter will have to be pulled forcefully later to tear them apart and inadvertent catheter loss may result. This occurred in one of our initial patients and has been reported by others [4]. No catheter loss has occurred since the following details have been respected: The use of a stylet-stabilized kinked catheter [17], instead of the classic invagination technique [2,16], will improve traction and minimize risk of loss. The procedure can be made more rapid by placing the patient in a modified dorsal lithotomy position, as suggested by Clayman et al. [2]. This will make repositioning unnecessary and, more importantly, allow control of the distal ureter from the abdominal cavity during extraction by the endoscopist. We used this modification successfully in 4 cases. It should not be attempted in the very obese. Jacobsen et al. reported urethral stricture after their transurethral extraction technique [16], but this may be related to their use of a conventional vein stripper alongside the resectoscope to control the ureter. In our series, transurethral extraction was always smooth and no strictures were noted on cystoscopic follow-up. 5. Conclusions In this comparison of the pluck and transurethral extraction techniques for management of the distal

B. Ubrig et al. / European Urology 46 (2004) 741 747 747 ureter during nephroureterectomy, blood loss, operative time, complications, and long-term oncologic outcome were not significantly different and compared favorably to results of classic and laparoscopic nephroureterectomy. Bladder tumor recurrence rate was in the range reported for classic nephroureterectomy. No recurrences in the former ureteral bed or on the scar of resection in the bladder occurred in either technique on long-term follow-up. Because of literature reports of tumor cell seeding from spillage, the pluck procedure should be used cautiously and preferably the ureter should be distally sealed. The transurethral approach is easy and rapid and can also be used in laparoscopic surgery. References [1] Hall MC, Womack S, Sagalowsky AI, Carmody T, Erickstad MD, Roehrborn CG. Prognostic factors recurrence and survival in transitional cell carcinoma of the upper urinary tract: a 30-year experience in 252 patients. Urology 1998;52:594 601. [2] Clayman RV, Garske GL, Lange PH. Total nephroureterectomy with ureteral intussusception and transurethral ureteral detachment and pull-through. Urology 1983;21:482 6. [3] Angulo JC, Hontoria J, Sanchez-Chapado M. One-incision nephroureterectomy endoscopically assisted by transurethral ureteral stripping. Urology 1998;52:203 7. [4] Laguna MP, de la Rosette JJ. The endoscopic approach to the distal ureter in nephroureterectomy for upper urinary tract tumor. J Urol 2001;166:2017 22. [5] McDonald HP, Upchurch WE, Sturdevant CE. Nephro-ureterectomy: a new technique. J Urol 1952;67:804. [6] Gill IS, Sung GT, Hobart MG, Savage SJ, Meraney AM, Schweizer DK, et al. Laparoscopic radical nephroureterectomy for upper tract transitional cell carcinoma: the Cleveland Clinic experience. J Urol 2000;164:1513 22. [7] Salomon L, Hoznek A, Cicco A, Gasman D, Chopin DK, Abbou CC. Retroperitoneoscopic nephroureterectomy for renal pelvic tumors with a single iliac incision. J Urol 1999;161:541 4. [8] McDougall EM, Clayman RV, Elashry O. Laparoscopic nephroureterectomy for upper tract transitional cell cancer: the Washington University experience. J Urol 1995;154:975 9. [9] Yoshino Y, Ono Y, Hattori R, Gotoh M, Kamihira O, Ohshima S. Retroperitoneoscopic nephroureterectomy for transitional cell carcinoma of the renal pelvis and ureter: Nagoya experience. Urology 2003;61:533 8. [10] Hetherington JW, Ewing R, Philp NH. Modified nephroureterectomy: a risk of tumour implantation. Br J Urol 1986;58:368 70. [11] Jones DR, Moisey CU. A cautionary tale of the modified pluck nephroureterectomy. Br J Urol 1993;71:486. [12] Fernandez Gomez JM, Barmadah SE, Perez GJ, Rabade Rey CJ, Rodriguez Martinez JJ. Risk of tumor seeding after nephroureterectomy combined with endoscopic resection of the ureteral meatus. Arch Esp Urol 1998;51:829 31. [13] Arango O, Bielsa O, Carles J, Gelabert-Mas A. Massive tumor implantation in the endoscopic resected area in modified nephroureterectomy. J Urol 1997;157:1839. [14] Palou J, Caparros J, Orsola A, Xavier B, Vicente J. Transurethral resection of the intramural ureter as the first step of nephroureterectomy. J Urol 1995;154:43 4. [15] Abercrombie GF, Eardley I, Payne SR, Walmsley BH, Vinnicombe J. Modified nephro-ureterectomy: Long-term follow-up with particular reference to subsequent bladder tumours. Br J Urol 1988;61:198 200. [16] Jacobsen JD, Raffnsoe B, Olesen E, Kvist E. Stripping of the distal ureter in association with nephroureterectomy: evaluation of the method. Scand J Urol Nephrol 1994;28:45 7. [17] Roth S, van Ahlen H, Semjonow A, Hertle L. Modified ureteral stripping as an alternative to open surgical ureterectomy. J Urol 1996;155:1568 71. [18] Saika T, Nishiguchi J, Tsushima T, Nasu Y, Nagai A, Miyaji Y, et al., Okayama Urogenital Cancer Collaborating Group (OUCCG). Comparative study of ureteral stripping versus open ureterectomy for nephroureterectomy in patients with transitional carcinoma of the renal pelvis. Urology 2004;63:848 52. [19] Goel MC, Mahendra V, Roberts JG. Percutaneous management of renal pelvic urothelial tumors: long-term followup. J Urol 2003;169:925 30. [20] Mydlo JH, Weinstein R, Shah S, Solliday M, Macchia RJ. Long-term consequences from bladder perforation and/or violation in the presence of transitional cell carcinoma: results of a small series and a review of the literature. J Urol 1999;161:1128 32.