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Radical Cystectomy for Bladder Cancer Today—A Homogeneous Series Without Neoadjuvant Therapy

From the Departments of Urology and Pathology, University of Bern, Switzerland.

Address reprint requests to Stephan Madersbacher, MD, Department of Urology, University of Bern, Anna-Seiler Haus, CH-3010 Bern, Switzerland; email: madersbacher{at}hotmail.com.

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Purpose: To investigate the effect of pelvic lymph node dissection and radical cystectomy for transitional cell cancer of the bladder on recurrence-free and overall survival, pelvic recurrences, and metastatic patterns in a homogeneous group.

Patients and Methods: A consecutive series of patients undergoing pelvic lymphadenectomy and radical cystectomy between 1985 and 2000 was analyzed. All patients were staged N0, M0 preoperatively, and no patient received neoadjuvant radio/chemotherapy. Pathologic characteristics based on the 1997 tumor-node-metastasis system, recurrence-free/overall survival, and metastatic patterns were determined.

Results: Five hundred seven patients (age 66 ± 12 years) with a mean follow-up time of 45 months (range, 0.1 to 176 months) were analyzed. Five-year recurrence-free and overall survival were, respectively, 73% and 62% for patients with organ-confined, lymph node-negative tumors (n = 217; pT2, pN0) and 56% and 49% for non-organ-confined, lymph node-negative tumors (n = 166; > pT2, pN0). Positive lymph nodes were found in 124 (24%) patients who had a 5-year recurrence-free (33%) or overall (26%) survival. Isolated local recurrences were observed in 3% of patients with organ-confined tumors ( pT2, pN0), 11% with non-organ-confined tumors (> pT2, pN0), and 13% with positive lymph nodes (any pT, pN+). Distant metastases developed in 25% of patients with organ-confined tumors, 37% with non-organ-confined tumors, and 51% with positive lymph nodes.

Conclusion: Despite negative preoperative staging, pelvic lymphadenectomy and cystectomy for bladder cancer reveal a high percentage of unsuspected nodal metastases (24%) that have a 25% chance for long-term survival. This procedure also ensures a low pelvic recurrence rate even in lymph node-positive patients, and patients with locally advanced cancer have a 56% probability of 5-year recurrence-free survival.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
PELVIC LYMPHADENECTOMY and radical cystectomy have been the cornerstone treatment for muscle-invasive bladder cancer during the last two decades.^1–3 Recently, advances in organ-preserving procedures for invasive bladder cancer such as extensive transurethral resection, chemo- and radiotherapy, and combined multimodal regimens have been popularized.^4–6 The latter therapy particularly challenges the role of radical surgery.^4–6 The primary impetus for a bladder-sparing approach is the improved quality of life associated with retaining the native bladder.^4–6 Organ-preserving procedures have been frequently compared with older, inhomogeneous cystectomy series with a 40% 5-year survival for organ-confined disease and only a 20% survival for more advanced stages.^7,8 This does not necessarily reflect what can be expected from radical surgery today. Although a randomized trial would be best for a direct comparison of organ-preserving approaches with radical cystectomy, such a study would be difficult to perform. In the absence of randomized trials, the outcome of a contemporary cystectomy series with equally good preoperative diagnostic workup provides valuable information.

We therefore assessed the outcome of a consecutive series of patients who had a complete preoperative workup, including chest x-ray, computed tomography (CT) scan of the pelvis, ultrasonography of the liver, bone scan, and an intravenous (IV) urography. All patients in this series were preoperatively staged N0, M0; no patient received neoadjuvant radio- or chemotherapy; and all patients subsequently underwent standard pelvic lymphadenectomy and radical cystectomy. We determined recurrence-free and overall survival, metastatic patterns, and the rate of pelvic recurrences in this homogeneous series.

	PATIENTS AND METHODS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Patients
Between 1985 and 2000, 647 patients underwent radical cystectomy at our institution. To analyze a homogeneous study population, only patients with primary transitional cell cancer (TCC) of the bladder who underwent radical cystectomy with intent to cure were included. Therefore, the following groups of patients were excluded: those with non-TCC malignancy or benign diseases of the urinary bladder (n = 53), those who had received neoadjuvant radio- or chemotherapy (n = 35), patients for whom such treatment would have only palliative indication (n = 16), gynecologic cancer patients (n = 22), and those patients with inadequate follow-up information (n = 14). The final study population comprised 507 patients, or 78% of those who underwent cystectomy between 1985 and 2000 at our institution. All 507 patients reported on here were preoperatively staged N0, M0 on the basis of CT scan, iv-urography, ultrasonography of the liver, and nuclear bone scans.

Indications for Cystectomy and Surgical Technique
Indications for radical cystectomy have not changed during the study period; they were muscle-invasive bladder cancer (> pT1) or multifocal pT1, G3 at initial diagnosis combined with multifocal carcinoma-in-situ. A solitary pT1, G3 lesion at first presentation or small, unifocal, superficially invasive TCC were not indications for primary cystectomy. These patients received a second transurethral resection and, in general, one or two cycles of Calmette-Guérin bacillus (BCG) immunotherapy for 6 weeks and were reassessed 6 weeks after the last BCG course. In the case of early recurrent carcinoma-in-situ or pT1G3, patients underwent radical cystectomy.

Lymphadenectomy. Pelvic lymphadenectomy was performed in all patients according to standard protocol as recently described.⁹ In brief, standard pelvic lymphadenectomy involves meticulous removal of all lymphatic and connective tissue within the following boundaries: laterally, genitofemoral nerve; distally, femoral canal; proximally, crossing of the ureter with the common iliac artery; inferiorly, side wall of the obturator muscle and floor of the obturator fossa down to the internal iliac vessels at the level of superior and inferior vesical arteries; and medially, side wall of the bladder. Presacral lymph nodes were not routinely removed, but lymphatic tissue along the medial portion of internal iliac vessels was routinely removed.

Radical cystectomy. In male patients, after the dorsolateral bladder pedicles containing superior and inferior vesical vessels along the hypogastric arteries had been divided, the endopelvic fascia is incised along the dorsolateral side of the prostate and Santorini’s plexus is ligated. The ureters are divided where they cross iliac vessels. This allows en bloc removal of the distal ureters and paraureteral lymphatic vessels, together with the cystectomy specimen. The dorsomedial pedicle is resected along the pararectal-presacral plane on the tumor-bearing side and on the opposite side along the dorsolateral wall of the seminal vesicle until the base of the prostate is reached. Santorini’s plexus is then divided over the ventral aspect of the prostate, and the membranous urethra is transected as close as possible to the apex of the prostate by dissecting it from the doughnut-shaped apex in an ascending way. In patients undergoing orthotopic bladder substitution (59% of patients in this study), we attempted to spare the neurovascular bundle on the contralateral tumor side, which had no effect on the pelvic recurrence rate. In female patients, unless an orthotopic bladder substitution is performed, the procedure usually involves en bloc resection of the uterus together with most of the anterior wall of the vagina and the entire urethra.¹⁰

Pathology
Cystectomy and lymphadenectomy specimens were analyzed according to a standard protocol. Pathologic staging of bladder tumor and lymph nodes was performed according to the 1997 tumor-node-metastasis classification by the International Union Against Cancer and the American Joint Committee on Cancer.¹¹ Pathologic subgroups were defined as organ-confined ( pT2, pN0), non-organ-confined (>pT2, pN0), and lymph node-positive (any pT, pN+).

Follow-Up
Patients were followed according to a prospective protocol and were seen at 3 and 6 months after surgery and thereafter at 6-month intervals until 5 years after surgery. Thereafter, they were seen annually, either at our institution or by urologists in private practice.

Statistics
Clinical and pathologic information concerning all patients undergoing radical cystectomy at our institution were entered prospectively into a departmental database. Outcomes were measured by time to clinical recurrence and overall survival. Patients who were still alive were censored at the date of the last follow-up visit. Kaplan-Meier curves were used to estimate the recurrence-free and overall survival of all patients and for subgroups classified according to pathologic stage. The log-rank test was used to compare overall survival and recurrence-free survival in subgroups of patients. Pearson’s ² test for associations was used to evaluate the association between pathologic variables. P values < .05 were considered statistically significant.

	RESULTS

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Patient Characteristics and Pathologic Staging
Among the 507 patients (400 men and 107 women; age 66 ± 12 years) analyzed, organ-confined tumors ( pT2, pN0) were present in 217 (43%): pTa/pTIS in 17, pT1 in 75, and pT2 in 125 patients (Table 1). Non-organ-confined tumors (> pT2, pN0) were found in 166 patients (33%): pT3 in 120 and pT4 in 46 patients (Table 1). Despite negative preoperative staging in all patients, final pathology demonstrated positive lymph nodes in 124 (24%) patients (Table 1). Incidence of lymph- node positivity increased from 3% in pT1 to 41% in pT4 tumors (Table 1). Positive lymph nodes were found in 28 patients (11%) with pathologic stages pT2 (n = 245) compared with 96 patients (37%) in those with higher pathologic stages (> pT2; n = 262; Table 1). The majority of tumors (483 of 507; 95%) were grade 3 TCC (Table 1).

Recurrence-free and overall survival of the entire cohort (n = 507) at 5 years were 62% and 59%, respectively, and 50% and 37% after 10 years (Fig 1). Recurrence-free and overall survival were closely correlated to tumor stage and lymph node status (Figs 2–4). The 5-year recurrence-free survival decreased from 76% in patients with pT1 tumors to 74% in those with pT2 tumors, 52% with pT3 tumors, and 36% with pT4 tumors (Fig 2). The recurrence-free survival of patients with pT1 and pT2 tumors was identical (P = .33); in contrast, differences between pT2 and pT3 tumors (P = .0005) as well as pT3 and pT4 tumors (P = .0018) were statistically significant. The 5-year overall survival decreased from 63% in patients with pT1 tumors to 32% in those with pT4 tumors (Fig 2). Parallel to recurrence-free survival, overall survival of patients with pT1 and pT2 tumors was identical (P = .51), yet overall survival of those with pT2 and pT3 (P < .001), as well as pT3 and pT4 tumors (P = .02), was different.

View larger version (11K): [in this window] [in a new window]   Fig 1. Recurrence-free (A) and overall survival (B) of the entire study group (n = 507).

View larger version (16K): [in this window] [in a new window]   Fig 2. Recurrence-free (A) and overall survival (B), stratified according to tumor stage irrespective of lymph node status.

View larger version (19K): [in this window] [in a new window]   Fig 4. Recurrence-free (A) and overall survival (B) in patients with organ-confined, non-organ-confined, and pN+ tumors.

View larger version (17K): [in this window] [in a new window]   Fig 3. Recurrence-free (A) and overall survival (B), stratified according to tumor stage in patients with pN0 tumors.

Local Versus Distant Failure
Bladder cancer recurrences were classified as either local or distant. Patients who had both local and distant recurrences were allocated to the latter group. Local recurrences were defined as those within the soft-tissue field of exenteration, and distant recurrences were classified as those outside this field.

Tumor progression was observed in 219 of 507 (43%) patients (Table 2). The median time to progression in these 219 patients was 16 months (range, 2 to 97 months). An isolated local recurrence was observed in 40 (8%) patients; distant metastases developed in 179 (35%) patients. Incidence of local and distant failure correlated closely to pathologic stage (Table 2). Whereas isolated local recurrences were seen in only 3% of patients with organ-confined tumors ( pT2, pN0), this percentage increased to 11% in those with non-organ-confined tumors (>pT2, pN0; table 2). Distant metastases developed in 25% of those with organ-confined tumors compared with 37% of those with non-organ-confined tumors (Table 2). Sixty-four percent of recurrences developed during the first year after surgery; 20% within the second year, and 9% within 3 to 5 years. Late TCC recurrences occurring 5 years or more after surgery were seen in 11 patients (5% of all recurrences): four patients developed local recurrences (including two with urethral recurrence), three patients developed upper urinary tract tumors, and four patients developed distant recurrence. These late recurrences (up to 8.1 years after surgery) emphasize the need for lifelong follow-up.

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

This study supports the role of radical surgery for invasive bladder cancer with a recurrence-free survival at 5 years of 62% for the entire group and of 73% for patients with organ-confined, lymph node-negative tumors.^2,3,13,14 A local recurrence rate of 8% in the overall group and 3% in patients with the organ-confined cancers provides further argument for the radical surgical approach. Stein et al³ recently reported on the largest radical cystectomy series of 1,054 patients. Their study’s scope was analyses of cystectomies performed over a substantially longer period (1971 to 1997), including patients from the pre-CT era and those with neoadjuvant chemo- and/or radiotherapy (16%).³ In contrast, our focus was to analyze the outcome of a selected, well-defined group of patients, excluding all those with incomplete preoperative workup, neoadjuvant chemo- and/or radiotherapy, or possible metastatic disease. Similar to the current series, Stein et al³ excluded patients undergoing cystectomy for other (nonbladder) pelvic malignancies and non-TCC bladder cancer, as well as those who underwent salvage cystectomy.

The recurrence-free survival in Stein et al’s³ series was 68% and 66% at 5 and 10 years, respectively, higher than in the current series (62% and 50% at 5 and 10 years, respectively). Outcome of cystectomy depends overwhelmingly on tumor stage, and therefore, the results of different series are generally a reflection of patient bias.¹⁰ Differences seen in our series, compared with that of Stein et al,³ can, therefore, be attributed in part to the fact that 20% of their patients had stages pT0, pTa, and pTIS. In our series, only 4% of the patients belonged to this low-risk group. For individual pathologic stages, the differences in recurrence-free and overall survival were smaller, usually in the 10% range.³ A more restrictive indication for cystectomy for pT1 and some pT2 tumors in our series and distinct differences in pathologic staging might be confounding factors.¹⁵ This hypothesis is substantiated by an almost identical outcome of patients with a "clear cut pathology" that is, positive lymph nodes; In the Stein et al³ series, the 5-year recurrence-free survival of lymph node-positive patients was 35%, compared with 33% in our series.

The present homogeneous cystectomy series demonstrates what can be expected from this approach today. Comparisons of different series must be carefully made because of distinct selection criteria. Caution must be applied in particular when comparing radical cystectomy results with bladder-sparing approaches, which, for obvious reasons, are used to treat mostly patients with small, transurethrally resectable, first-occurring tumors. The tumors selected for radical cystectomy usually cover more advanced stages. Although the reported overall 5-year survival of 48% to 63% of bladder-sparing approaches is comparable to that for radical cystectomy, salvage cystectomy is eventually required in 34% to 45% of these cases, at a significantly higher morbidity than primary surgery.^5,6,16 This looks rather poor when taking into account that selected patients with a good prognosis are compared with cystectomy patients, who are included in all risk groups. Despite the absence of randomized, controlled trials, these data indicate that cystectomy remains the gold standard for invasive bladder cancer.

Pathologic stage and lymph node status are the most important predictors for outcome, which is also reflected in our results.^1–3,17,18 The difference in survival between muscle-invasive, organ-confined tumors (pT1 or pT2, according to the 1997 tumor-node-metastasis system) and extravesical tumors (pT3 or pT4) is noteworthy.¹³ In agreement with recent series,^3,13 the distinction between organ-confined and non-organ-confined tumors is clinically justified, and the difference between pT1 and pT2 tumors seems to be irrelevant for the oncological outcome.^3,13 In our series, recurrence-free and overall survival of patients with pT1 and pT2 tumors was identical.

Positive lymph nodes were seen in 24% of our patients, a percentage comparable with other series.^3,9,17,18 Lymph node involvement has been said to be an unfavorable prognostic sign that reflects systemic disease in most cases, yet long-term survival is seen in 20% to 30% of patients, emphasizing that lymphadenectomy can be curative in a subset of patients.^{3,9,17,18–20} Patients with limited lymph node involvement and smaller-sized nodal metastases, as well as those without lymph node capsule perforation, have a better outcome.⁹ In this series, lymph node-positive patients who received postoperative adjuvant chemotherapy had a significantly longer overall survival than those without adjuvant chemotherapy. However, in the absence of a randomized trial, these data must be interpreted with caution. Even if enlarged nodes are found during surgery, cure is still possible, although less likely.²¹

Incidence of pelvic recurrences after radical cystectomy has decreased in recent years to an average of 10% (range, 4% to 18%).²² This is a result of earlier intervention, improved surgical technique, and better patient selection.²² The overall 7% local recurrence rate in our series is at the lower end of this range (Table 2). Whether our meticulous lymph node dissection contributed to this low local recurrence rate remains an open question, yet it is suggestive. Few studies have addressed in detail the effect of the primary tumor stage on the development of local recurrences.²³ In our series, 3% of patients with organ-confined ( pT2, pN0) disease developed a local recurrence, compared with 10% in patients with extravesical tumors (> pT2, pN0). The local recurrence rate of lymph node-positive patients correlated with the pathologic stage, as well (Table 3). Although only 7% of patients with a pT2N+ stage developed a local recurrence, this percentage increased to 22% of those with pT4N+ tumors.

Despite satisfactory local tumor control, the incidence of distant metastases was 25% in patients with organ-confined tumors and 37% in those with extravesical disease (see Table 2). In those with positive lymph nodes, 64% progressed and 80% of all recurrences were attributable to distant metastases. These data indicate that further improvements in local control would be of little survival benefit because the problem lies in reducing distant metastases. Although there has been a huge increase in the knowledge of molecular mechanisms for bladder cancer and the large number of markers investigated, this has not yet brought about a reliable discrimination between high- and low-risk patients on an individual basis. Markers are needed to allow for a better stratification, for example, for adjuvant chemotherapy protocols.

In summary, the outcome of this large, homogeneous group of patients with bladder cancer, treated uniformly by a meticulous pelvic lymphadenectomy and radical cystectomy, supports the role of radical surgery. Recurrence-free survival at 5 years was 73% for patients with organ-confined, lymph node-negative tumors. A low local recurrence rate (3%) in the group with organ-confined disease underlines the excellent local tumor control after radical surgery. Almost one of four patients had positive lymph nodes despite negative preoperative staging, and 25% of these lymph node-positive patients experienced long-term survival.

	REFERENCES

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
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9. Mills RD, Turner WH, Fleischmann A, et al: Pelvic lymph node metastases from bladder cancer: Outcome in 83 patients after radical cystectomy and pelvic lymphadenectomy. J Urol 166:19–23, 2001[CrossRef][Medline]

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11. Fleming ID, Cooper JS, Henson DE, et al (eds): AJCC Cancer Staging Manual (ed 5). Philadelphia, PA, Lippincott-Raven, 1997, pp 241–243

12. Sternberg CN, Parmar MKB: Neoadjuvant chemotherapy is not (yet) standard treatment for muscle-invasive bladder cancer. J Clin Oncol 19:S21–S26, 2001 (Sept 15 suppl)

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17. Vieweg J, Gschwend JE, Herr HW, et al: Pelvic lymph node dissection can be curative in patients with node positive bladder cancer. J Urol 161:449–454, 1999[CrossRef][Medline]

18. Leissner J, Hohenfellner R, Thüroff JW, et al: Lymphadenectomy in patients with transitional cell carcinoma of the urinary bladder; significance for staging and prognosis. Br J Urol 85:817–823, 2000

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23. Pollack A, Kagars GK, Cole CJ, et al: The relationship of local control to distant metastases in muscle invasive bladder cancer. J Urol 154:2059–2064, 1995[Medline]

Submitted May 14, 2002; accepted October 31, 2002.

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