JOURNAL OF ENDOUROLOGY Volume 21, Number 9, September 2007 © Mary Ann Liebert, Inc. DOI: 10.1089/end.2006.0306
Oncologic Outcomes of Extravesical Stapling of Distal Ureter in Laparoscopic Nephroureterectomy FREDERICO R. ROMERO, M.D., EDWARD M. SCHAEFFER, M.D., MICHAEL MUNTENER, M.D., BRUCE TROCK, M.D., LOUIS R. KAVOUSSI, M.D.,* and THOMAS W. JARRETT, M.D.†
ABSTRACT Purpose: To evaluate the safety and oncologic efficacy of extravesical laparoscopic stapling of the distal ureter and bladder cuff during nephroureterectomy for pelvicaliceal transitional-cell carcinoma (TCC). Patients and Methods: Patients with primary pelvicaliceal TCC and no history of TCC of the bladder or ureter who underwent extravesical laparoscopic control of the bladder cuff were compared with a similar group of patients submitted to the open transvesical approach. Operative results and oncologic outcomes were compared. Results: Operative time, estimate blood loss, length of hospital stay, rate of positive margins, and postoperative complications were not statistically different in the two groups of patients. With an average of almost 4 years of follow-up, the laparoscopic approach to the bladder cuff was associated with an increase in the overall rate of recurrence and a shorter recurrence-free survival, although these differences were not statistically significant. Rates of local and bladder recurrence and distant metastases were similar. Conclusions: Laparoscopic stapling of the bladder cuff has oncologic efficacy and outcomes similar to those of the open transvesical approach. However, the laparoscopic procedure may carry a higher risk of recurrence and a shorter recurrence-free interval than the open transvesical approach.
transvesical open excision during laparoscopic NU for uppertract TCC.
INTRODUCTION
T
HE STANDARD TREATMENT for transitional cell carcinoma (TCC) of the upper urinary tract is nephroureterectomy (NU) with excision of a bladder cuff.1,2 Laparoscopic NU was developed to reduce the morbidity of the procedure compared with the open approach by reducing the incisional trauma but maintaining the principles of surgical oncology.1–3 The most controversial issue in laparoscopic NU is the management of the distal ureter.3,4 There are several approaches, often combining features of endoscopic, laparoscopic, and open management.5-9 Few studies have compared these methods and assessed the statistical significance of any differences.4,10 With the main objective of evaluating the safety and oncologic efficacy of extravesical laparoscopic stapling of the distal ureter and bladder cuff, we compared a group of patients undergoing this approach with those having the traditional
PATIENTS AND METHODS All 12 patients who underwent laparoscopic NU for pathologically confirmed TCC of the upper urinary tract between August 1993 and August 2005 at our institution were reviewed. Patients with primary pelvicaliceal TCC who had been submitted to extravesical laparoscopic control of the bladder cuff by one of two authors (LRK or TWJ) were selected as the group to be analyzed. Patients with a history of or concurrent TCC of the bladder were excluded from this study. A cohort of 12 patients matched by age, body mass index (BMI), tumor size and location, multifocality, associated carcinoma in situ (CIS), histologic grade, and pathologic stage who underwent an open
The James Buchanan Brady Urological Institute, The Johns Hopkins Medical Institutions, Baltimore, Maryland. *Current address: Department of Urology, North Shore-LIJ Health System, Long Island, New York. †Current address: Department of Urology, The George Washington University Medical Center, Washington, DC.
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ROMERO ET AL. TABLE 1. CHARACTERISTICS
OF
PATIENTS
Laparoscopic approach (N 12)
Mean age (years) (range) Mean tumor size (cm) (range) BMI (kg/m2) (range) CIS present (%) Multifocality (%) Histologic grade high low (%) Pathologic T stage Cis-1 2–4
65.6 3.50 24.6 5 5 10
68.3 3.43 24.2 6 4 10
3 (30.0) 7 (70.0)
transvesical approach to the distal ureter by the same surgeons was selected as the control group (Table 1). The operative techniques were described previously in an initial series of patients.1 Operative results and oncologic outcomes in the two groups were compared. Fisher’s exact test was used to determine the statistical significance of associations between categorical variables, while the Wilcoxon signed-rank test was used for continuous variables. Kaplan-Meier curves were generated for cancer-specific and recurrence-free survival. The log-rank test was used to generate P values for these variables. Statistically significant differences were considered to be present at P 0.05.
RESULTS Operative time, estimate blood loss, length of hospital stay, rate of positive margins, and postoperative complications were not statistically different in the two groups. With an average of 46.8 37 months of follow-up, the overall rate of recurrence was twofold higher in the laparoscopic group, although this difference did not reach statistical significance. The rates of local and bladder recurrence were not different in the two groups. None of the patients presented with a recurrence at the ipsilateral ureteral orifice scar or a pelvic extravesical recurrence. In a Kaplan-Meier comparison of time to recurrence, patients treated laparoscopically had a shorter recurrence-free survival, with a log-rank P value of 0.092 (Fig. 1). The occurrence of metastases was statistically similar in both groups. There were no deaths from disease during the follow-up, although one patient in the laparoscopic group died without evidence of disease 19 months after surgery. Postoperative results and oncologic outcomes are summarized in Table 2.
DISCUSSION Traditional open NU involves either one large incision or two separate incisions. These incisions result in considerable patient morbidity and prolonged convalescence. Laparoscopic NU was developed with the goal of providing a less-invasive approach and to hasten patient recovery and shorten the time required to return to normal activity.1 No consensus has been reached with regard to which tech-
TUMORS Open approach (N 12)
(51–84) (1.1–5.5) (19.4–34.0) (41.7) (41.7) (83.3) 2(16.7)
(56–85) (0.8–5.3) (21.5–31.6) (50.0) (33.3) (83.3) 2 (16.7)
3 (25.0) 9 (75.0)
P value 0.453 0.836 0.564 0.293 0.299 0.409 0.353
nique is best for managing the distal ureter during laparoscopic NU.4 The classical open technique of securing the distal ureter and bladder cuff achieves the principles of surgical oncology and has withstood the test of time. This technique parallels distalureteral resection in standard open nephroureterectomy.3 The extravesical laparoscopic stapling technique avoids cystotomy and minimizes the risk of tumor spillage and pelvic recurrence, but it risks leaving behind distal-ureteral and bladder segments that carry a considerable risk of containing unrecognized CIS or tumor.3,4 Further, this technique may result in exposed linear staples within the bladder.4 Complete laparoscopic dissection and stapling is a valid approach in patients undergoing NU, but it is limited by the absence of long-term follow-up. In the present study, the laparoscopic approach to the bladder cuff was associated with an increase in the positive-margin and recurrence rates and a shorter recurrence-free interval. However, none of these results was statistically significant. Similar trends have been reported previously.4,10 In 2005, Matin and Gill10 reported a statistically higher positive-margin rate and a tendency toward inferior recurrence-free and overall survival with the laparoscopic extravesical stapling approach in comparison with cystoscopically secured detachment and liga-
1.0
0.8
Cum Hazard
Variable
AND
0.6
0.4
0.2
0.0 0
20 40 60 80 100 Time to first recurrence after NUx (months)
FIG. 1. Time to first recurrence after nephroureterectomy. Solid line open surgery; dotted line laparoscopic surgery.
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EXTRAVESICAL STAPLING OF URETER TABLE 2. OPERATIVE DATA Laparoscopic approach (N 12)
Variable Mean operative time (min) Mean estimated blood loss (mL) Mean hospital stay (days) Positive margins (%) Complications (%) No. (%) with recurrence Total Local Bladder Metastases Mean follow-up (mos) (range)
292.9 400.0 3.8 3 (25.0) 3 (25.0) 8 (66.7) 2 (16.7) 6 (50.0) 3 (25.0) 54.5 (7–148)
tion for the management of the bladder cuff. However, in their study population, a bladder-tumor history was more common in the laparoscopic group, which by itself is associated with a higher risk of recurrence and poorer prognosis. In the same year, Brown et al4 found a higher rate of positive margins with the laparoscopic stapling procedure in comparison with different approaches to the lower ureter, but the patients who underwent laparoscopic stapling excision of the distal ureter had a higher incidence of distal-ureteral tumors than the other patients. Intraoperative frozen-section review can be used to avoid positive margins during the laparoscopic stapling procedure. In the case of a positive ureteral margin, open bladder-cuff excision should be performed. A strength of our study is the exclusion of patients with previous or synchronous ureteral and bladder TCC. Excluding such tumors prevented a higher rate of positive ureteral margins or local recurrences in the bladder or the ipsilateral orifice scar as a result of the natural history of these tumors. Although this group of patients is at lower risk for recurrence, analysis was performed in two cohorts with the same demographic and clinicopathologic characteristics, correlating the operative results and outcomes more strongly with the surgical approach used for the treatment of the distal ureter. We found that laparoscopic stapling of the bladder cuff has oncologic efficacy and outcomes similar to those of the open transvesical approach. The analyses are limited by the small sample size and retrospective nature of the study. Given these caveats, it is difficult to interpret the clinical significance of this result. The most conservative assessment would be to assume that the laparoscopic procedure may carry a higher risk of recurrence and a shorter recurrence-free interval in a larger cohort of patients with long-term follow-up, suggesting the need for additional studies.
REFERENCES 1. Jarrett TW, Chan DY, Cadeddu JA, et al. Laparoscopic nephroureterectomy for the treatment of transitional cell carcinoma of the upper urinary tract. Urology 2001;57:448.
Open approach (N 12)
P value
260.1 220.8 4.2 0 2 (16.7)
0.791 0.151 0.554 0.108 0.341
4 (33.3) 0 4 (33.3) 1 (8.3) 39.2 (8–84)
0.090 0.239 0.233 0.248 0.488
2. Gonzalez CM, Batler RA, Schoor RA, et al. A novel endoscopic approach towards resection of the distal ureter with surrounding bladder cuff during hand assisted laparoscopic nephroureterectomy. J Urol 2001;165:483. 3. Steinberg JR, Matin SF. Laparoscopic radical nephroureterectomy: Dilemma of the distal ureter. Curr Opin Urol 2004;14:61. 4. Brown JA, Strup SE, Chenven E, et al. Hand-assisted laparoscopic nephroureterectomy: Analysis of distal ureterectomy technique, margin status, and surgical outcomes. Urology 2005;66:1192. 5. El Fettouh HA, Rassweiler JJ, Schulze M, et al. Laparoscopic radical nephroureterectomy: Results of an international multicenter study. Eur Urol 2002;42:447. 6. Hsu THS, Hsu S. A novel open surgical approach to transvesical distal ureterectomy in nephroureterectomy. Int Urol Nephrol 2004;36:155. 7. McDonald DF. Intussusception ureterectomy: A method of removal of the ureteral stump at the time of nephrectomy without an additional incision. Surg Gynecol Obstet 1953;97:565. 8. Gill IS, Soble JJ, Miller SD, et al. A novel technique for management of the en bloc bladder cuff and distal ureter during laparoscopic nephroureterectomy. J Urol 1999;161:430. 9. McDonald HP, Upchurch WE, Sturdevant CE. Nephro-ureterectomy: A new technique. J Urol 1952;61:804. 10. Matin SF, Gill IS. Recurrence and survival following laparoscopic radical nephroureterectomy with various forms of bladder cuff control. J Urol 2005;173:395.
Address reprint requests to: Thomas W. Jarrett, M.D. Dept. of Urology The George Washington University Medical Center 2150 Pennsylvania Ave Washington, DC 20037 E-mail: tjarrett@mfa.gwu.edu
ABBREVIATIONS USED BMI body mass index; CIS carcinoma in situ; NU nephroureterectomy; TCC transitional-cell carcinoma.