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Year : 2019  |  Volume : 30  |  Issue : 6  |  Page : 250-254

How safe could open extravesical bladder cuff resection guarantee complete removal of ipsilateral ureteral orifice?

Department of Urology, National Cheng Kung University Hospital, Tainan, Taiwan

Date of Submission19-Jun-2019
Date of Decision10-Sep-2019
Date of Acceptance09-Oct-2019
Date of Web Publication23-Dec-2019

Correspondence Address:
Dr. Yao-Lin Kao
Department of Urology, College of Medicine, National Cheng Kung University, No. 138, Sheng Li Road, Tainan 701
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/UROS.UROS_40_19

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Objectives: The aim of this study is to report our 8-year experience in terms of the success rate of complete bladder buff resection procedures bladder cuff resection (BCR) and further oncological outcomes in patients under open extravesical BCR for the management of primary upper tract urothelial carcinoma (UTUC). Materials and Methods: We retrospectively reviewed patients with primary UTUC who undergone laparoscopic nephroureterectomy and open extravesical BCR in our center. Complete BCR procedures were not defined by any ureteral orifice remnant noted in postoperative cystoscopy surveillance. The rate of complete BCR procedures was calculated. Patients were divided into residual ureteral orifice group (RUO) and nonRUO group (NRUO) and the intravesical and local recurrences and distant metastasis were analyzed and compared across the two groups. Results: A total of 105 patients were reviewed. After operation, 67 of them (63.8%) had ipsilateral strict criteria of complete BCR procedures defined on cystoscopy. Shorter mean operative time was noted in the RUO group comparing to the NRUO group (145 ± 73 vs. 192 ± 107 min, P = 0.03). Bladder recurrence was significantly higher in the RUO group (RUO vs. NRUO: 59.7% vs. 26%, P = 0.001) during a median of 39.7 months follow-up. Most of the intravesical recurrences were superficial (94%) and more prone to be found near the RUO/scar in the RUO group rather than the NRUO group (59.7% vs. 26.3%, P = 0.04). The RUO group strongly predicted superficial intravesical recurrence (odds ratio: 4.04, 95% confidence interval: 1.57–10.37, P = 0.004). No significant difference was recorded in muscle invasive bladder tumor, local recurrence, contralateral urinary tract recurrence, or distal metastasis across the groups. Conclusions: Open extravesical BCR does not guarantee the complete removal of ipsilateral ureteral orifice. Increased risk of superficial intravesical recurrence is noted in patients with RUO.

Keywords: Bladder cuff resection, nephroureterectomy, upper urinary tract, ureteral orifice, urothelial cancer

How to cite this article:
Lin YC, Ou CH, Yang WH, Kao YL. How safe could open extravesical bladder cuff resection guarantee complete removal of ipsilateral ureteral orifice?. Urol Sci 2019;30:250-4

How to cite this URL:
Lin YC, Ou CH, Yang WH, Kao YL. How safe could open extravesical bladder cuff resection guarantee complete removal of ipsilateral ureteral orifice?. Urol Sci [serial online] 2019 [cited 2020 Nov 30];30:250-4. Available from: https://www.e-urol-sci.com/text.asp?2019/30/6/250/273879

  Introduction Top

Urothelial carcinoma existing in the upper urinary tract is relatively uncommon compared to bladder urothelial carcinoma. Cancer represents approximately 5% of all urothelial tumors.[1] The standard therapy for upper tract urothelial cancer (UTUC) has been nephroureterectomy with excision of bladder cuff due to the possibility of multifocal disease within the ipsilateral collecting system.[2] With the advance of the minimally invasive method, laparoscopic nephroureterectomy could provide similar oncological outcomes compared to traditional open technique.[3],[4]

Complete ureter and bladder cuff resection (BCR) also served as a core of the procedure, among others. If the distal ureter is not completely resected in patients with UTUC, there is a 30%–40% chance that the tumor will recur in ureteral stump with poor survival.[5],[6] Many techniques have been described for the management of distal ureter and bladder cuff which could be performed either in open or laparoscopic approach with or without transurethral add.[7],[8] Each technique has its individual advantages and disadvantages. The best way to manage the distal ureter is still debatable. However, there is some evidence suggesting that an open approach might be more reliable than complete laparoscopic approach.[7],[9]

The open BCR approach may be secured extravesically or transvesically. The extravesical approach performed under ureter tenting without cystostomy could provide excellent local control without violating bladder integrity to minimize the possibilities of tumor spillage, especially in the circumstance of active bladder urothelial carcinoma presentation.[10] However, the “blind” extravesical clipping does not always guarantee complete bladder cuff retrieval.[11] Residual ureteral orifice could occasionally be found during postoperative cystoscopy. Studies focusing on complete ipsilateral ureteral orifice removal are scarce.[12] Most studies only reported surgical margins, which were not the definitive surrogate of complete ipsilateral urinary tract removal.[13],[14] We reported our single-center 8-year experience in the rate of successful complete removal of ipsilateral ureteral orifice through open extravesical BCR technique and compared further oncological outcomes between patients with complete or incomplete ipsilateral ureteral orifice removal.

  Materials and Methods Top

We retrospectively reviewed the database of our hospital on patients with primary unilateral UTUC receiving Hand-Assisted Retroperitoneoscopic Nephroureterectomy (HARN) and open extravesical BCR from December 2004 to March 2012. Most of HARN and open extravesical BCR were conducted by an experienced hand surgeon (CHO). All patients included received postoperative cystoscopic examinations and were followed up for at least 1 year. Patients were excluded for possible confounding effects on comparing oncological outcomes between patients with complete or incomplete BCR in any of the following conditions: distal metastasis or local lymph node metastasis suggested by image at initial presentation, prior history of bladder cancer, synchronous bladder cancer, and primary tumor over ureterovesical junction. Patients were also excluded if they received perioperative systemic/intravesical chemotherapy or radiotherapy.

The open extravesical BCR technique was performed through a Gibson incision after completing kidney proximal ureter mobilization. With gentle traction on the distal ureter, bladder cuff was transected through Metzenbaum in the most distal part approachable between two right angles clamping over the upper and lower margins of excision area in case of any possibilities of tumor spillage. We spared no efforts to dissect the intramural portion of the ureter as low as possible to excise the ipsilateral orifice completely. Then, the extravesical serosa was electrocauterized and closed with 2-O chromic catgut sutures. Formal lymphadenectomy was not routinely performed due to the absence of lymph node metastasis during initial diagnosis and controversy concerning benefits of lymphadenectomy.

All patients generally removed foley catheter on the 7th day after the operation. Cystoscopic surveillance was done every 3 months in the 1st year for patients whether of ipsilateral ureteral orifice or any evidence of bladder tumor recurrence. In the absence of urothelial cancer relapse within 1 year after surgery, the follow-up interval was extended. Yearly abdominal computerized tomography was usually performed for upper urinary tract follow-up and to rule out retroperitoneal relapse. Patients were divided into complete or incomplete BCR groups according to the absence or presence of residual orifice during follow-up cystoscopy, respectively [Supplementary Figure 1]. Small indentation or irregular surface in the corresponding ipsilateral ureteral orifice area was considered as remnant of ureteral orifice which was grouped into incomplete BCR group.

All data from the patients were reviewed through office charts and electro-medical records. Clinical parameters included age, sex, American Society of Anesthesiologists (ASA) class, body mass index (BMI), symptoms of hematuria, presence of end-stage renal diseases, and mean operative time. Histopathologic parameters such as tumor stage, size, and location and specimen weight were included. All tumors were graded according to the WHO grading system for urothelial carcinoma and staged according to the 2004 TNM classification by different pathologists. Tumor recurrence in the bladder was mostly noted by follow-up cystoscopy with further pathological confirmation. Specific attention was dedicated to recurrences near area of ipsilateral ureteral scar/residual orifice. Local recurrence was defined as recurrence in the ipsilateral retroperitoneal space or de novo regional lymph node presence. Contralateral urinary tract recurrence was diagnosed through image with pathological confirmation. Distant metastasis was defined as an indicator of tumor presence outside the urinary tract neither in ipsilateral retroperitoneum nor in regional lymph node after operation.

Categorical variables were compared using the Chi-square test. Continuous variables were analyzed using the Student's t-test. Multivariate logistic regression procedures were performed for binary data. Kaplan–Meier survival curves were used to acquire survival data. All statistical analyses were performed through SPSS Statistics for Windows, Version 17.0. Chicago: SPSS Inc.

  Results Top

From December 2004 to March 2012, 105 patients with primary UTUC were included. After HARN combined with open-extra vesical BCR, 67 cases had residual ipsilateral ureteral orifice (RUO) were found during cystoscope follow-up and 38 cases had no residual ipsilateral ureteral orifice (NRUO). The clinical and pathological characteristics of the patients are shown in [Table 1]. There was no significant difference between groups for age, BMI, male-to-female ratios, ASA classes, symptoms of hematuria, and end-stage renal diseases. However, significant increase of operative time was noted in the NRUO group (RUO vs. NRUO: 150 ± 78 vs. 200 ± 115 min, P = 0.03). No contralateral ureter damage was noted in either of the two groups. Pathologic results of the specimens were similar in both groups in tumor stage, location, and size and specimen weight in both groups.
Table 1: Clinical and pathological characteristics of the patients with residual ureteral orifice and nonresidual ureteral orifice groups

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The oncological outcomes are shown in [Table 2]. Overall median of follow-up sample was 39.7 months. Recurrence rates were significantly increased in both bladder and areas near ipsilateral ureteral orifice/scar in the RUO group compared to the NRUO group (59.7% vs. 26.3% over bladder, P < 0.01; 34.3% vs. 10.5% near ipsilateral ureteral orifice/scar, P = 0.04). However, there was no difference in time to first intravesical recurrence between the RUO and NRUO groups (16.9 ± 18.7 months vs. 22.1 ± 21.6 months, P = 0.42). Most of the bladder recurrences were superficial in both the RUO and NRUO groups. No difference between the RUO and NRUO groups in muscle-invasive bladder tumor progression (3 of 67 vs. 1 of 38, P = 0.63), contralateral upper tract recurrence (3 of 67 vs. 1 of 38, P = 0.63), local recurrence (1 of 67 vs. 3 of 38, P = 0.10), or distal metastasis (1 of 67 vs. 1 of 38, P = 0.68). The presence of residual U. O was identified as a significant predictor of superficial bladder recurrence (odds ratio [OR]: 4.04, P < 0.01) in the multivariate analysis in our study [Table 3]. Bladder cancer recurrence-free survival instances are shown in [Figure 1]. There was a significant difference in bladder cancer recurrence-free rate in the RUO group compared to the NRUO group (P = 0.04).
Table 2: Oncological outcomes of the patients with residual ureteral orifice and nonresidual ureteral orifice groups

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Table 3: Multivariate analysis of prognostic factors for superficial bladder recurrence

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Figure 1: Recurrence-free rate curves show significant difference in patients with residual ureteral orifice versus those no residual ureteral orifice

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  Discussion Top

Ipsilateral BCR importance, including ureteral orifice, cannot be emphasized enough in surgery of UTUC.[15] To the best of our knowledge, this is the first article focusing on the rate of successful complete ureteral orifice removal with laparoscopic nephroureterectomy in conjunction with open-extravesical BCR. Only about one-third of patients had complete ureteral orifice removed in our practice which was confirmed by follow-up cystoscopic surveillance. Compared to the RUO group, the NRUO group was associated with a significantly longer total operative time (145 ± 73 vs. 192 ± 107 min, P = 0.01) which suggests additional effort and time is needed if complete BCR without residual orifice is bound to be achieved.

Few studies reported the clearance of ureteral orifice under open extravesical approach.[12],[14] Hattori et al.[12] reported about 11% of patients with remnant ureteral orifice after laparoscopic nephroureterectomy combined with open-extravesical BCR. Success of complete ureteral orifice removal in all patients from a small series took place in only 10 patient cases under open extravesical BCR, which was also reported by Ritch et al.[14] The judgment in complete ureteral orifice removal under cystoscopy might be subjective. However, these studies did not clearly describe the boundaries between complete or incomplete BCR procedures. High RUO after extravesical BCR as demonstrated in our studies may be the result of strict definition of complete ureteral orifice under cystoscopy for any subtle indentation or irregular surface were not allowed considering them as partial ureteral orifice removal. The overall 3-year intravesical recurrence-free rate was around 65% in our group which was comparable to the data reported from previous studies (59%–78%).[7],[8],[12],[16] Due to the close relationship between incomplete BCR and intravesical recurrence, significant flaws in surgical technique over distal ureter management is likely to be rare in our practice.

Routine bladder mobilization is not performed in our practice as traditional distal ureteral management principle.[17] However, Some authors suggested aggressive division and ligation of lateral pedicle including obliterated arteries and superior/middle/inferior vesical arteries for adequate access of the entire intramural ureter.[18] With the better exposure of intramural ureter, the higher rate of complete ureteral orifice removal is expected. Nevertheless, the risk of contralateral urinary tract compromise must be kept in mind.[9] Simultaneously, cystoscopy may be a reasonable option in these circumstances for confirmation of ipsilateral bladder cuff retrieval and contralateral urinary tract patency.

Many other techniques in distal ureterectomy have their own benefits and shortcomings. Transvesicalor transurethral resection approach may offer precise distal ureteral and BCR methods. The violation of bladder integrity might raise the concern of cancer spillage, especially under conditions such as the presence of occult bladder tumor or distal ureteral tumor. Indeed, studies do report invasive tumor implantation over the bladder defect area after operation.[19],[20] Open extravesical approach still provided better ureteral orifice retrieval compared to laparoscopic stapling approach.[11],[14] Laparoscopic dissection with LigaSure BeRhad also reported good results without remnant ureteral orifice in small-case series.[21] Surgeons should choose the technique which they are familiar with to achieve the oncology principle of a UTUC surgery.

Significant higher bladder recurrence was noted in the RUO group compared to the NRUO group (59.7% vs. 26%), which was prone to be located in the remnant of ipsilateral ureteral orifice or scar (RUO vs. NRUO: 57.5% vs. 40%). This may be the effect of monoclonal tumor seeding from the upper urinary tract.[22],[23] Luckily, the majority of these subsequent bladder tumors recurrences were superficial lesions.[24] Ninety-four percent of intravesical recurrences in our series were found in superficial stages which can be treated by endoscopic transurethral resection with or without intravesical chemotherapy. The presence of remnant UO is a strong predictor for superficial intravesical recurrence (OR: 4.04, P = 0.004). This result, again, emphasizes the importance of complete BCR procedure.

There was no difference noted in progression to muscle-invasive bladder cancer between the RUO and NRUO groups (2.9% vs. 2.6%). No differences in local recurrences, contralateral upper tract recurrences, or distal metastasis in the RUO group compared to the NRUO group were detected. Our observations suggest that RUO urothelium followed by nephroureterectomy may have no adverse effect on disease-specific survival in patients with primary UTUC. The need for transurethral ureteral orifice excision and cauterization or not in patients with remnant ureteral orifice after BCR procedure depends on evidence to give a prudent clinical recommendation.

There are some limitations in our study: first, it is a retrospective design that many potential confounding factors may influence the clearance of ureteral orifice, except for strict definition on complete BCR procedure, the other bias might be trivial for no difference in tumor pathological stage, patient age, and BMI between our groups. Second, the information from the single-center with most of the surgery performed by 1 surgeon may not be representative; nevertheless, it suggests that even with the experienced hand, open extravesical BCR still cannot guarantee complete retrieval of ipsilateral ureteral orifice. Finally, patients are limited. A larger number of cases, especially with multicenter design, are needed to validate these findings.

  Conclusions Top

Open extravesical bladder cuff excision in the management of UTUC cannot guarantee the complete excision of the entire ipsilateral urinary tract including the ureteral orifice even in the surgeon's experienced hand. Superficial bladder recurrence, especially near the RUO, will increase if the excision is incomplete. Therefore, simultaneous cystoscopy confirmation for the presence of remnant ureteral orifice during operation may be needed.

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Conflicts of interest

There are no conflicts of interest.

  References Top

Munoz JJ, Ellison LM. Upper tract urothelial neoplasms: Incidence and survival during the last 2 decades. J Urol 2000;164:1523-5.  Back to cited text no. 1
Kirkali Z, Tuzel E. Transitional cell carcinoma of the ureter and renal pelvis. Crit Rev Oncol Hematol 2003;47:155-69.  Back to cited text no. 2
Stewart GD, Humphries KJ, Cutress ML, Riddick AC, McNeill SA, Tolley DA, et al. Long-term comparative outcomes of open versus laparoscopic nephroureterectomy for upper urinary tract urothelial-cell carcinoma after a median follow-up of 13 years*. J Endourol 2011;25:1329-35.  Back to cited text no. 3
Miyazaki J, Nishiyama H, Fujimoto H, Ohyama C, Koie T, Hinotsu S, et al. Laparoscopic versus open nephroureterectomy in muscle-invasive upper tract urothelial carcinoma: Subanalysis of the multi-institutional national database of the Japanese urological association. J Endourol 2016;30:520-5.  Back to cited text no. 4
Strong DW, Pearse HD, Tank ES Jr., Hodges CV. The ureteral stump after nephroureterectomy. J Urol 1976;115:654-5.  Back to cited text no. 5
Kang M, Jeong CW, Kwak C, Kim HH, Ku JH. The characteristics of recurrent upper tract urothelial carcinoma after radical nephroureterectomy without bladder cuff excision. Yonsei Med J 2015;56:375-81.  Back to cited text no. 6
Kapoor A, Dason S, Allard CB, Shayegan B, Lacombe L, Rendon R, et al. The impact of method of distal ureter management during radical nephroureterectomy on tumour recurrence. Can Urol Assoc J 2014;8:E845-52.  Back to cited text no. 7
Li WM, Shen JT, Li CC, Ke HL, Wei YC, Wu WJ, et al. Oncologic outcomes following three different approaches to the distal ureter and bladder cuff in nephroureterectomy for primary upper urinary tract urothelial carcinoma. Eur Urol 2010;57:963-9.  Back to cited text no. 8
Stravodimos KG, Komninos C, Kural AR, Constantinides C. Distal ureterectomy techniques in laparoscopic and robot-assisted nephroureterectomy: Updated review. Urol Ann 2015;7:8-16.  Back to cited text no. 9
[PUBMED]  [Full text]  
Steinberg JR, Matin SF. Laparoscopic radical nephroureterectomy: Dilemma of the distal ureter. Curr Opin Urol 2004;14:61-5.  Back to cited text no. 10
Tsujihata M, Nonomura N, Tsujimura A, Yoshimura K, Miyagawa Y, Okuyama A, et al. Laparoscopic nephroureterectomy for upper tract transitional cell carcinoma: Comparison of laparoscopic and open surgery. Eur Urol 2006;49:332-6.  Back to cited text no. 11
Hattori R, Yoshino Y, Gotoh M, Katoh M, Kamihira O, Ono Y, et al. Laparoscopic nephroureterectomy for transitional cell carcinoma of renal pelvis and ureter: Nagoya experience. Urology 2006;67:701-5.  Back to cited text no. 12
Brown JA, Strup SE, Chenven E, Bagley D, Gomella LG. Hand-assisted laparoscopic nephroureterectomy: Analysis of distal ureterectomy technique, margin status, and surgical outcomes. Urology 2005;66:1192-6.  Back to cited text no. 13
Ritch CR, Kearns JT, Mues AC, Hruby GW, Benson MC, McKiernan JM, et al. Comparison of distal ureteral management strategies during laparoscopic nephroureterectomy. J Endourol 2011;25:1149-54.  Back to cited text no. 14
Rai BP, Shelley M, Coles B, Somani B, Nabi G. Surgical management for upper urinary tract transitional cell carcinoma (UUT-TCC): A systematic review. BJU Int 2012;110:1426-35.  Back to cited text no. 15
Xylinas E, Rink M, Cha EK, Clozel T, Lee RK, Fajkovic H, et al. Impact of distal ureter management on oncologic outcomes following radical nephroureterectomy for upper tract urothelial carcinoma. Eur Urol 2014;65:210-7.  Back to cited text no. 16
Hubosky SG, Michael D. Laparoscopic Nephroureterectomy. In: Fabrizio Graham SD, Keane TE, Glenn JF. editors. Glenn's Urologic Surgery. 7th ed. Philadelphia, PA: Lippincott Williams and Wilkins; 2010. p. 834-5.  Back to cited text no. 17
Smith AK, Matin SF, Jarrett TW. Urothelial Tumors of the Upper Urinary Tract and Ureter. In: Wein AJ, Kavoussi LR, Novick AC, Partin AW, Peters CA. editors. Campbell-Walsh urology. 11th ed. Philadelphia, PA: Saunders Elsevier; 2015. p. 1377-8.  Back to cited text no. 18
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.  Back to cited text no. 19
Hetherington JW, Ewing R, Philp NH. Modified nephroureterectomy: A risk of tumour implantation. Br J Urol 1986;58:368-70.  Back to cited text no. 20
Tsivian A, Benjamin S, Sidi AA. A sealed laparoscopic nephroureterectomy: A new technique. Eur Urol 2007;52:1015-9.  Back to cited text no. 21
Takahashi T, Kakehi Y, Mitsumori K, Akao T, Terachi T, Kato T, et al. Distinct microsatellite alterations in upper urinary tract tumors and subsequent bladder tumors. J Urol 2001;165:672-7.  Back to cited text no. 22
Catto JW, Hartmann A, Stoehr R, Bolderson E, Rehman I, Rosario DJ, et al. Multifocal urothelial cancers with the mutator phenotype are of monoclonal origin and require panurothelial treatment for tumor clearance. J Urol 2006;175:2323-30.  Back to cited text no. 23
Kang CH, Yu TJ, Hsieh HH, Yang JW, Shu K, Huang CC, et al. The development of bladder tumors and contralateral upper urinary tract tumors after primary transitional cell carcinoma of the upper urinary tract. Cancer 2003;98:1620-6.  Back to cited text no. 24


  [Figure 1]

  [Table 1], [Table 2], [Table 3]


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