Cystectomy with Prostate Sparing for Bladder Cancer in 100 Patients: 10-year Experience

0022-5347/02/1686-2413/0 THE JOURNAL OF UROLOGY® Copyright © 2002 by AMERICAN UROLOGICAL ASSOCIATION, INC.®

Vol. 168, 2413–2417, December 2002 Printed in U.S.A.

DOI: 10.1097/01.ju.0000036521.21034.ec

CYSTECTOMY WITH PROSTATE SPARING FOR BLADDER CANCER IN 100 PATIENTS: 10-YEAR EXPERIENCE GUY VALLANCIEN,* HAZEM ABOU EL FETTOUH, XAVIER CATHELINEAU, HERVE BAUMERT, ¨ LLE FROMONT AND BERTRAND GUILLONNEAU GAE From the Departments of Urology and Pathology, Institut Montsouris and the Universite Pierre et Marie Curie, Paris, France

ABSTRACT

Purpose: To minimize the risk of incontinence and impotence without compromising oncological outcome, we performed prostate sparing surgery during radical cystectomy for bladder cancer. Materials and Methods: Since 1992, 100 patients with a mean age of 64 years (range 48 to 82) underwent cystectomy for bladder transitional cell carcinoma with prostate sparing based on normal digital rectal examination of the prostate, normal prostate specific antigen (PSA), percent free PSA greater than 15 and normal transrectal ultrasound of the prostate. Prostate biopsies to exclude prostate cancer were performed on patients with an abnormal digital rectal examination, high PSA, percent free PSA less than 15 or hypoechoic lesions on ultrasound. Surgery consisted of transurethral resection of the prostate with analysis of frozen section of the prostatic urethra and transitional prostate and cystectomy with reconstruction by a Z ileal bladder anastomosed to the prostatic capsule after confirmation of the absence of prostate or bladder cancer on frozen sections of the surgical capsule specimens. Patients were followed closely with imaging and laboratory studies every 6 months and annually for 3 years thereafter. Results: Perioperative death occurred in 1 patient due to septicemia, 20 patients (20%) died of cancer and 6 (6%) died of nonrelated cancer causes. Mean followup 38 months (range 2 to 111). Postoperative pathological stage was PT0 in 2 cases, PtaT1 in 22, PT2 in 48, PT 3 in 28 and N⫹ in 13. The 5-year actuarial global survival according to pathological stage was pTaT1N0 in 96% of cases, pT2N0 in 83%, pT3N0 in 71% and N⫹ in 54% (p ⫽ 0.0001). The 5-year actuarial cancer specific survival was PT0, Ta T1 in 90% of cases, PT2 in 73%, PT3 in 63% and N– in 8%. The cancer specific survival according to pathological grade was 100% for well differentiated tumors (grade I), 76% for moderately differentiated tumors (grade II) and 47% for poorly differentiated tumors (grade III) (p ⫽ 0.003). Local recurrence was pTaT1N0 in 1 of 22 cases (4.5%), pT2N0 in 2 of 40 (5%), pT3N0 in 2 of 23 (8.5%) and N⫹ in 0 of 13 (0%). Prostate cancer was diagnosed in 3 patients (2 errors in the diagnosis and 1 cancer de novo within 5 years of followup). At 1-year followup 86 of 88 patients (97%) are fully continent (no pad) during the day, and 84 (95%) void 1 to 2 times a night to stay dry. Of 61 patients with previously adequate sexual function 50 (82%) maintained potency with retrograde ejaculation secondary to transurethral resection, 6 (10%) have partial potency and 5 (8.1%) are impotent. Conclusions: Cystectomy with prostate sparing for bladder cancer is feasible and offers promising functional results with no additional oncological risk. Careful selection of patients is mandatory. KEY WORDS: cystectomy, prostate, bladder neoplasms

Radical cystectomy has been the cornerstone for treatment of muscle invasive bladder cancer as well as recurrent refractory cases of superficial transitional cell carcinoma. Other forms of therapy such as external beam radiation therapy and chemotherapy have been tried at many centers to preserve the bladder and functional results but they too have morbidity1, 2 and less tumor control3, 4 compared to surgery.5 However, radical cystectomy is highly morbid, as it results in many changes in quality of life including sexual and social function. Sexual dysfunction is especially important to younger patients, and maintaining good urinary control and good sexual function is crucial for acceptance of this surgery by them. Partial cystectomy has been tried at many centers in an attempt to reduce the functional complications but local recurrence is high.6 Since 1992 we have been using a modi-

fied technique of radical cystectomy in which the prostate is spared in select patients with bladder cancer. We describe this technique and present our results in 100 successive patients. MATERIALS AND METHODS

Since 1992, 165 males and 44 females with bladder cancer were candidates for cystectomy at our institution. Of the male patients 57 (39%), were not candidates for prostate sparing due to associated prostate cancer, transitional cell carcinoma of the prostatic urethra or bladder tumor invading the prostate. The remaining 108 patients (66%) met the clinical selection criteria for prostate sparing surgery. Eight patients were excluded from the prostate sparing procedure intraoperatively because of carcinoma in situ in the frozen section of the prostatic urethra (4), transitional cell carcinoma of the prostate (2), and prostate cancer in the transurethral resection specimens sent for frozen section (2). Based on our selection criteria 100 patients (92%) with a

Accepted for publication June 28, 2002. Presented at annual meeting of American Urological Association, Orlando, Florida, May 25–30, 2002. * Requests for reprints: Department of Urology, Institut Mutualiste Montsouris, 42, Boulevard Jourdan, 75674 Paris cedex–France. 2413

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mean age of 64 years (range 48 to 82) underwent the procedure. The pathological characters are presented in the table. Patients were evaluated preoperatively by complete physical examination, urianalysis, complete blood count, chest x-ray and 1 or more imaging studies of the abdomen, including computerized tomography (CT), excretory urography, ultrasonography and transrectal ultrasonography (7.5 MHz. probe). All patients had a normal digital rectal examination, prostate specific antigen (PSA) less than 4 ng./ml. (mean 2.0 ⫾ 2 ng./ml.) and no hypoechoic areas of the prostate. With the introduction of percent free PSA for evaluation of prostate cancer an inclusion criterion was free PSA greater than 15%. Patients with palpable nodule(s) in the prostate, high PSA, low percent free PSA (less than 15%) or hypoechoic area on transrectal ultrasound underwent prostatic biopsy to exclude prostate cancer. Patients with negative biopsies were then candidates for the prostate sparing surgery. The surgical technique begins with transurethral resection of the prostate extending from the bladder neck to the verumontanum with care to preserve the prostatic capsule intact. (The procedure was performed under the same anesthetic in 85% of the patients and a few days before cystectomy in 15% during our initial experience.) Specimens of the mucosa of prostatic urethra and the remaining part of the transitional gland are sent for frozen section examination in separate containers. Chips are examined microscopically to make sure that there is no transitional cell carcinoma involvement of the prostatic urethra and transitional prostate, and to exclude cancer prostate as well. A midline or Pfannenstiel incision is made according to surgeon preference, and pelvic lymph node dissection is performed and sent for frozen section. The vas deferens are bilaterally identified, isolated and preserved. The ureters are identified and transected bilaterally at their entry to the bladder. The distal end of the ureters are sent for frozen section to ensure a good safety margin from the tumor. The vas deferens is traced deeply to reach the anterior surface of the seminal vesicles. Mild traction on the Foley catheter allows identification of the prostatovesical junction anteriorly (fig. 1). We incise the anterior surface of the prostate 3 to 5 mm. distal to the junction, complete the incision posteriorly to separate the bladder completely and close the bladder aperture immediately. In cases of bladder tumor at the trigone or the bladder neck 5 mm. beyond the distal end of the tumor are usually enough for a good safety margin. The surgical specimen is then inspected and sent for frozen section of the prostatic capsule to confirm negative surgical margin. In cases of tumors close to the bladder neck the external surface of the bladder at the tumor site is also sent for frozen section as this area is close to the spared seminal vesicles. A 40 cm. ileal segment is isolated and detubularized except for 3 cm. at both ends. The detubularized loop is remodeled in a Z fashion and the ureters are implanted at the nondetubularized ends (fig. 2). Ureteral stents are placed. The prostatoileal anastomosis is performed in a continuous fashion posteriorly and with interrupted stitches anteriorly. At the end of the procedure the pouch is inflated to detect any

Pathological features Mean pt. age ⫾ SD % Pathological T stage (No.): pT0 pTaT1 ⫺ N0 ⫺ M0 T2 ⫺ N0 ⫺ M0 T3-N0-M0 N⫹ % Ca in situ (No.) % Pathological grade (No.): Well differentiated (G1) Moderately differentiated (G2) Poorly differentiated (G3)

63 ⫾ 8 years 2 (2) 22 (22) 40 (40) 23 (23) 13 (13) 22 (22) 9 (9) 26 (26) 65 (65)

leak. Ureteral catheters are left for 7 days and a urethral catheter is left for 9 days. Followup protocol consists of complete physical examination with digital rectal examination, urianalysis, complete blood analysis, PSA evaluation (total and free PSA), transrectal ultrasound of the prostate, chest x-ray and CT scan of the abdomen and pelvis every 6 months for 3 years. If these tests continue to be negative then yearly tests are performed for life. Continence is assessed by patients using mailed questionnaires. Patients are considered continent only when they do not use any pads. They were strictly instructed during the postoperative year 1 to wake up at night once or twice to empty the bladder to achieve nighttime continence. Potency is strictly defined as the ability to maintain an unassisted erection sufficient for intercourse. Partial potency is defined as the ability to achieve but not maintain erection long enough for satisfactory intercourse without the use of a device or medications. Patients unable to stimulate erection for completion of intercourse, as well as those using medications or devices to stimulate erection are considered impotent. In this study the 1997 TNM staging system was used.7 In 2 cases without bladder cancer in the surgical specimens preoperative stage was pT1 and pT2, respectively. Discrete variables were analyzed using Pearson’s chi-square test and continuous variables were analyzed with Student’s t test. Kaplan-Meier survival estimates with log-rank tests were used in all survival data analysis. RESULTS

The surgical procedure was completed successfully in all patients. Mean operative time was 25 minutes (range 15 to 42) for transurethral resection of the prostate and 165 minutes (117 to 287) for cystectomy and neobladder. Mean operative blood loss was 250 ml. (range 90 to 1,000) and only 2 patients required transfusion. One patient died perioperatively due to septicemia. Two patients had pulmonary embolism that was successfully diagnosed and managed with anticoagulation. In 2 patients postoperative urine leak from the prostatovesical anastomosis was diagnosed on ascending cystourethrography. One of these patients was treated conservatively with Foley catheter drainage for 1 month, while the other underwent reexploration and surgical repair of the prostatoileal anastomosis. Two patients had ureteral stenosis on 1 side which was managed endoscopically in 1 and with open surgery 1. Other complications included wound infections in 2 patients, wound dehiscence in 2 and bulbar urethral stricture that was managed successfully by visual internal urethrotomy in 1. No stenosis at the prostatovesical junction has been reported to date. Oncological results. Postoperative pathological stage of the surgical specimens was pT0 in 2 patients (2%), pTa pT1 N0 in 22 (22%), pT2N0 in 40 (40%), pT3N0 in 23 (23%) and N⫹ in 13 (13%). Tumor grade was well differentiated in 9% of cases, moderately differentiated in 26% and poorly differentiated in 65%. Carcinoma in situ was present in 22 patients (22%). Mean followup was 38 months (range 2 to 111) and median followup was 36 months. A total of 52 patients have been followed more than 2 years and 35 more than 3 years. Overall 26 patients died, including 20 (20%) of cancer and 6 (6%) of other causes. The 5-year actuarial global survival according to pathological stage was in 2 of 2 cases PT0 (100%), pTaT1N0 in 21 of 22 (96%), pT2N0 in 34 of 40 (85%), pT3N0 in 17 of 23 (74%) and N⫹ in 7 of 13 (54%). The 5-year actuarial survival with no evidence of disease was PT0 in 2 of 2 cases (100%), PTaT1 in 20 of 22 (90%), PT2N0 in 29 of 40 (73%), PT3N0 in 15 of 23 (65%) and N⫹ in 1 of 13 (8%) (p ⫽ 0.0001, fig. 3). The cancer specific survival according to pathological grade was 100%

CYSTECTOMY WITH PROSTATE SPARING FOR BLADDER CANCER

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FIG. 1. A, limited dissection sparing prostate capsule and seminal vesicles with no control of deep dorsal vein plexus. B, prostatic capsule (PC) after transurethral resection of the prostate and cystectomy with preserved vas (VD) and seminal vesicles (SV). DVC, deep dorsal vein complex. PP, puboprostatic ligament.

including 3 of 22 (13%) pTaT1N0, 11 of 40 (27.5%) pT2N0, 8 of 23 (34%) pT3N0 and 9 of 13 (70%) N⫹ (p ⫽ 0.01). Mean time ⫾ SD to metastatic disease was 20 ⫾ 17 month. Transitional cell carcinoma recurred in the prostatic fossa in 1 patient with pT1 and 1 with pT2 disease (neither had carcinoma in situ) and was managed with transurethral resection. Three patients had prostate cancer. In 1 patient prostate cancer was not detected on the frozen section at the time of operation. Another patient had a PSA of 14 ng./ml. which was attributed to prior transurethral resection of the bladder 2 weeks before surgery. This patient was treated with sequential hormone therapy. In the remaining patient prostate cancer developed 5 years postoperatively and was detected during followup prostate biopsies. This patient underwent transrectal focused ultrasound. Functional results. Good satisfactory daytime and nighttime continence was achieved. At 1 year postoperatively 86 of 88 patients (97%) were completely continent (no pad) immediately after catheter removal and remain continent during the day. Nighttime continence has been achieved by 84 of 88 patients (95%) with a wake-up average of 1 to 3 times a night. Of the 2 who are incontinent 1 uses a penile clamp and 1 uses a condom catheter. No patient had urinary retention required or self-catheterization as the anastomosis between the prostate capsule and neobladder remains large. Of 61 patients with adequate sexual function before surgery 5 (8.1%) are impotent, 6 (10%) reported decreased potency and 50 (82%) maintained potency status, although they have retrograde ejaculation due to transurethral resection. The remaining 39 patients did not answer the questions concerning sexual activity. DISCUSSION

FIG. 2. Reconstruction of neobladder

for well differentiated, 76% for moderately differentiated tumors and 47% for poorly differentiated tumors (p ⫽ 0.006, fig. 4). Local pelvic recurrence developed in 5 cases, including 1 of 22 (4.5%) pTaT1N0 2 of 40 (5%) pT2N0 and 2 of 23 (8.5%) pT3N0 (p ⫽ 0.1). Distant metastasis developed in 31 cases,

The treatment of choice for muscle invasive bladder cancer and refractory cases of superficial high grade bladder cancer is radical cystectomy. During radical cystectomy prostate seminal vesicles and vas deferens are removed. During deep pelvic dissection the pelvic nerves are usually damaged or injured and the external sphincter to a lesser extent. The technique we use to spare the prostate and seminal vesicles in patients with bladder cancer involves several risks, including prostate cancer, carcinoma in situ of the prostatic urethra, transitional cell cancer of the prostatic duct or glands and prostatic invasion by bladder cancer. Prostate cancer risk Kabalin et al reported a 38% incidence of occult prostate cancer in cystoprostatectomy specimens but only 1.9% of these specimens had tumor volume exceeding 0.1 cc.8 Their study was performed before the PSA era

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CYSTECTOMY WITH PROSTATE SPARING FOR BLADDER CANCER

FIG. 3. Kaplan-Meier survival estimates by pathological stage

FIG. 4. Kaplan-Meier survival estimates by pathological grade

and patients were excluded from analysis based only on an abnormal digital rectal examination. Our patients were assessed carefully preoperatively to exclude the possibility of associated prostate cancer. Patients with an abnormal digital rectal examination, high PSA or percent free PSA less than 15% underwent prostatic needle biopsy. The prostate sparing procedure was not performed in 2 patients with positive biopsies for prostate cancer. Frozen section from the transurethral resection specimens were examined in all patients to exclude occult prostate cancer in the transitional zone. Once the surgical specimen was removed, it was sent for frozen section of the margin of the prostatic capsule to detect any occult prostatic cancer. The prostate sparing procedure was not done in 2 other patients with positive chips for prostate cancer. Our strict followup protocol of digital rectal examination, PSA and percent free PSA every 6 months leads to early detection of de novo prostate cancer so that patients can be treated successfully with different modalities such as external beam radiotherapy, brachytherapy, hormonal treatment or transrectal focused ultrasound. Urethral carcinoma in situ and prostatic transitional cell carcinoma risk. The incidence of transitional cell carcinoma in the prostate was also an additional risk in our patients. In a review of 350 men who underwent cystoprostatectomy for bladder transitional cell carcinoma Schellhammer et al reported that 12% had associated prostate transitional cell carcinoma.9 Hardeman and Soloway reported a 25% incidence of prostatic transitional cell carcinoma in 86 patients.10 Wood et al indicated that most of the transitional cell carci-

noma seen in cystoprostatectomy specimens was in the prostatic urethra.11 In our series the prostatic urethra as well as most of the prostatic transitional zone were completely removed by transurethral resection of the prostate and sent for frozen section to exclude any transitional cell carcinoma at those sites. Patients with tumor at the prostatic urethra were not considered candidates for the procedure. The prostate sparing procedure was not done in 4 patients with carcinoma in situ of the prostatic urethra and 2 with transitional cell carcinoma of the prostate. Lebret et al reported no urethral recurrence at 10 years in patients who underwent cystectomy when no tumor was found on frozen section in the prostatic urethra.12 Transitional cell carcinoma recurred in the prostatic fossa in 2 of our cases and was managed successfully with transurethral resection. However, we do not know how many cases could have been missed. Prostatic invasion with bladder cancer risk. In our series patients were properly examined with digital rectal examination and CT preoperatively. In patients at risk (tumor close to the bladder neck) at least a 5 mm. safety margin beyond the lower extent of the tumor was ensured. Frozen section of the prostatic capsule was also performed. In 1 case we had to recut the prostatic capsule after the initial positive frozen section to obtain a good safety margin. This patient has no signs of recurrence to date. Orthotopic bladder substitution was initially described to improve the quality of life and body image of patients after radical cystectomy.13, 14 Recent innovations in surgical techniques and the use of detubularized bowel segments resulted in various pouches with good compliance and capacity that protect the upper tract. The continence rate is variable in different series. Turner et al compared 3 different types of neobladder reservoirs, and reported daytime incontinence rates of 5% to 18% and nighttime incontinence rates of 13% to 27%.15 Hautmann et al reported a daytime continence rate of 83.7% and a nighttime continence rate of 66.3%,16 while the day and night continence rates reported by Hollowell et al were 93% and 86%, respectively.17 In our series we used 40 cm. of detubularized ileum to create a small neobladder, and our daytime continence rate was 97% and our nighttime continence rate was 95%. There were no cases of prostatoileal stricture due to the wide anastomosis between the prostatic capsule after transurethral resection of the prostate and ileum. Schover et al reported a high prevalence of sexual dysfunction in radical cystectomy population,18 and Hart et al noted a high level of social dysfunction in these men as a result of urinary and sexual dysfunction.19 With nerve sparing radical cystoprostatectomy Brendler et al reported a 64% potency rate with no increase in oncological risk.20 The prostate sparing surgery allowed us to preserve the neurovascular bundles described by Walsh and Donker21 at the posterolateral edge of the prostate and also preserve the external urethral sphincter. In our series 82% of patients maintained their potency status and only 8.1% lost sexual function. Colombo et al performed the same nerve sparing procedure on 8 patients and reported immediate daytime continence and preserved potency in all patients.22 However, their series included young adults (mean age 44 years) with good sexual function. A major difference between our technique and that of Colombo et al is control of the deep dorsal vein complex which branches, we did not believe was necessary in our series. Horenblas et al reported a similar operation on 10 males and 3 females with good oncological and functional outcome.23 All of the aforementioned studies report initial results of the technique with short-term followup. In our study mean followup was 38 months which is the critical period for cancer recurrence.

CYSTECTOMY WITH PROSTATE SPARING FOR BLADDER CANCER CONCLUSIONS

In our experience cystectomy with prostate and seminal vesicle sparing in select patients with bladder cancer is feasible. This modified technique offers good functional results in regard to continence and potency with cancer control comparable to the standard procedure. Careful selection of patients is mandatory and the role of the pathologist is crucial. The best indication for this procedure remains PT2 tumor not located too close to the bladder neck. We need to confirm our results after longer followup. REFERENCES

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10. Hardeman, S. W. and Soloway, M. S.: Urethral recurrence following radical cystectomy. J Urol, 144: 666, 1990 11. Wood, D. P., Jr., Montie, J. E., Pontes, J. E., Medendorp, S. V. and Levin, H. S.: Transitional cell carcinoma of the prostate in cystoprostatectomy specimens removed for bladder cancer. J Urol, 141: 346, 1989 12. Lebret, T., Herve, J. M., Barre, P., Gaudez, F., Lugagne, P. M., Barbagelatta, M. et al: Urethral recurrence of transitional cell carcinoma of the bladder. Predictive value of preoperative latero-montanal biopsies and urethral frozen sections during prostatocystectomy. Eur Urol, 33: 170, 1998 13. Couvelaire, R.: Le reservoire ileal de substitution apres la cystectomie totale chez l’homme. J d’ Urol, 57: 408, 1951 14. Camey, M. and Le Duc, A.: L’enterocystoplastie apres cystoprostatectomy totale pour cancer de vessie. Ann Urol, 2: 114, 1979 15. Turner, W. H., Bitton, A. and Studer, U. E.: Reconstruction of the urinary tract after radical cystectomy: the case for continent urinary diversion. Urology, 49: 663, 1997 16. Hautmann, R. E., de Petriconi, R., Gottfried, H.-W., Kleinschmidt, K., Mattes, R. and Paiss, T.: The ileal neobladder: complications and functional results in 363 patients after 11 years of followup. J Urol, 161: 422, 1999 17. Hollowell, C. M. P., Christiano, A. P. and Steinberg, G. D.: Technique of Hautmann ileal neobladder with chimney modification: interim results in 50 patients. J Urol, 163: 47, 2000 18. Schover, L. R., Evans, R. and von Eschenbach, A. C.: Sexual rehabilitation and male radical cystectomy. J Urol, 136: 1015, 1986 19. Hart, S., Skinner, E. C., Meyerowitz, B. E., Boyd, S., Lieskovsky, G. and Skinner, D. G.: Quality of life after radical cystectomy for bladder cancer in patients with an ileal conduit or cutaneous or urethral Kock pouch. J Urol, 162: 77, 1999 20. Brendler, C. B., Steinberg, G. D., Marshall, F. F., Mostwin, J. L. and Walsh, P. C.: Local recurrence and survival following nerve-sparing radical cystoprostatectomy. J Urol, 144: 1137, 1990 21. Walsh, P. C. and Donker, P. J.: Impotence following radical prostatectomy: insight into etiology and prevention. J Urol, 128: 492, 1982 22. Colombo, R., Bertini, R., Salonia, A., Da Pozzo, L. F., Montorsi, F., Brausi, M. et al: Nerve and seminal sparing radical cystectomy with orthotopic urinary diversion for select patients with superficial bladder cancer: an innovative surgical approach. J Urol, 165: 51, 2001 23. Horenblas, S., Meinhardt, W., Ijzerman, W. and Moonen, L. F. M.: Sexuality preserving cystectomy and neobladder: initial results. J Urol, 166: 837, 2001