Oncological Outcomes in Patients Treated with Radical Cystectomy for Bladder Cancer: Comparison Between Open,Laparoscopic,and Robot-Assisted Approaches

Abstract

Purpose:

To investigate oncological outcomes in patients with muscle-invasive bladder cancer who underwent open radical cystectomy (ORC), laparoscopic radical cystectomy (LRC), or robot-assisted radical cystectomy (RARC).

Patients and Methods:

A retrospective analysis was performed on 230 patients who underwent ORC (n = 150), LRC (n = 22), or RARC (n = 58) between September 2009 and June 2012. Perioperative outcomes were compared between the three surgical approaches. The influence of the type of surgical approach on recurrence-free survival (RFS), cancer-specific survival (CSS), and overall survival (OS) was analyzed using the Kaplan–Meier method, and differences were assessed with the log-rank test. Predictors of RFS, CSS, and OS were also analyzed with a Cox regression model.

Results:

The median patient age for ORC, LRC, and RARC groups was 68.0 (interquartile range [IQR]: 60.0–73.0), 65.0 (IQR: 62.8–74.0), and 61.5 (IQR: 54.8–72.0) years, respectively (p = 0.017), and the median follow-up duration was 27.9 (IQR: 14.7–47.9), 28.8 (IQR: 15.7–41.8), and 32.0 (IQR: 15.5–45.4) months, respectively (p = 0.955). There was no significant difference in RFS, CSS, and OS according to the surgical approach (p = 0.253, p = 0.431, and p = 0.527, respectively). Subgroup analysis revealed that RFS, CSS, and OS were not significantly different in both subgroups with stage ≤pT2 or ≥pT3. Multivariable Cox regression analyses showed that the surgical approach was not a significant predictor of RFS, CSS, and OS.

Conclusion:

Our findings indicate that the type of surgical approach is not associated with RFS, CSS, and OS in patients with bladder cancer.

Introduction

Radical cystectomy (RC) with pelvic lymphadenectomy is the curative treatment of choice for muscle-invasive bladder cancer.¹ While open radical cystectomy (ORC) has been the gold-standard procedure and is associated with a long life expectancy,^2,3 minimally invasive approaches such as laparoscopic radical cystectomy (LRC) and robot-assisted radical cystectomy (RARC) have been increasingly performed in the surgical management of bladder cancer. In recent years, several studies, including randomized controlled trials, have documented the surgical feasibility and potential benefits of LRC and RARC for muscle-invasive bladder cancer.^4

–11 LRC and RARC appear to offer advantages to patients in terms of overall lower perioperative complications, decreased pain, reduced scarring, shorter hospital stay, and faster recovery.

However, LRC and RARC are technically challenging procedures that require special laparoscopic skills of the surgeon and have a long learning curve,^12,13 while surgeons more readily overcome the difficult learning curve with RARC compared to LRC. Due to the lack of adequate comparative data and sufficient follow-up to demonstrate oncologic outcomes compared to ORC, there are still concerns regarding the introduction of LRC and RARC into surgical treatment for bladder cancer.

There are few studies and limited information comparing ORC, LRC, and RARC; thus, little is known about the comparative oncological outcomes between these three surgical approaches for bladder cancer. The purpose of this study was to compare short-term oncological outcomes in a consecutive series of patients with bladder urothelial carcinoma undergoing ORC, LRC, or RARC.

Patients and Methods

Between September 2009 and June 2012, 271 patients underwent RC at our institution. Patients with pathologic cell types other than urothelial cell carcinoma (n = 18) and those for whom RC had salvage or palliative indication (n = 23) were excluded. The final study population consisted of 230 patients. Among these patients, 150 (65.2%), 22 (9.6%), and 58 (25.2%) patients underwent ORC, LRC, and RARC, respectively. This retrospective study was approved by our institutional review board.

All patients underwent RC according to criteria consistent with guideline recommendations.¹ Each patient underwent thorough preoperative evaluation, including imaging of the chest, abdomen, and pelvis, for staging. None of the patients had evidence of distant metastasis at the time of surgery. The surgical technique of ORC, LRC, and RARC has been described previously.^14,15 Radical cystectomy included removal of the prostate and seminal vesicles in men and removal of the uterus, vagina, and bilateral ovaries in women. All urinary diversions were performed as open procedures (extracorporeal approach through a lower midline mini-incision in LRC and RARC).

Demographic, perioperative, and pathologic data were assessed, including age, gender, American Society of Anesthesiologists (ASA) scores, body mass index (BMI), clinical tumor stage, type of urinary diversion, total number of lymph nodes (LNs) removed, intraoperative receipt of transfusion, pathologic tumor stage, tumor grade, presence of carcinoma in situ (CIS) or lymphovascular invasion (LVI), positive surgical margin (PSM), LN involvement, and receipt of perioperative (neoadjuvant or adjuvant) chemotherapy. Clinical stage was assigned based on a combination of specimen pathology at transurethral resection of the bladder tumor and imaging studies. In this study, clinical T2 was defined as muscle-invasive bladder cancer at transurethral resection of the bladder tumor and/or tumor has grown into the muscle layer (but, not into the fatty tissue layer) at imaging study such as computed tomography scans for abdomen and pelvis. On the other hand, clinical T3 was defined as the tumor has grown through the muscle layer of the bladder and into the fatty tissue layer that surrounds it. Pathologic staging and tumor grading were determined using the 2010 TNM classification from the American Joint Committee on Cancer and the International Union against Cancer. Tumor grading was assessed based on the 2004 World Health Organization/International Society of Urologic Pathology consensusclassification.

Follow-up outcomes, including recurrence-free survival (RFS), cancer-specific survival (CSS), and overall survival (OS), were evaluated. While postoperative follow-up was not standardized due to the retrospective design of this study, in general, each patient was followed up according to recommendations and institutional protocols. Patients were followed every 3 months for the first 2 years, every 6 months for the next 2 years, and annually thereafter. Follow-up evaluations consisted of physical examinations with laboratory tests, chest radiography, and computed tomography scans for abdomen and pelvis. Bone scintigraphy scans were performed when clinically indicated. The RFS was defined as time from RC to local and/or metastatic recurrence, based on histologic or radiologic evidence. The CSS and OS were defined as time from RC to death due to bladder cancer and due to any cause, respectively.

Statistical analyses

Median and interquartile range (IQR) were used for the descriptions of quantitative variables, and frequency and percentage were used for qualitative variables. Descriptive statistics were obtained for demographic variables. Demographic, perioperative, and pathologic data were compared between three surgical approaches. Continuous variables were compared using the Kruskal–Wallis test and one-way analysis of variance, while categorical variables were compared using the chi-square test. Kaplan–Meier curves were constructed to illustrate RFS, CSS, and OS according to three surgical approaches. The influence of surgical approach on RFS, CSS, and OS in the entire study group and pathologic tumor stage subgroups was analyzed using the Kaplan–Meier method, and differences were assessed with the log-rank test. Multivariable Cox proportional hazard models were used to evaluate the association among RFS, CSS, OS, and risk factors of interest. A p-value <0.05 was considered statistically significant. Statistical analyses were performed using SPSS^® for Windows, version 21.0.

Results

Patient characteristics and preoperative variables for each group are provided in Table 1. The median patient age for ORC, LRC, and RARC groups was 68.0 (IQR: 60.0–73.0), 65.0 (IQR: 62.8–74.0), and 61.5 (IQR: 54.8–72.0) years, respectively (p = 0.017). The proportion of male to female patients, ASA score classification, clinical tumor staging, and histologic grading were similar among the three groups (p = 0.093, 0.104, 0.345, and 0.198, respectively).

Table 1.

Baseline Characteristics for the Open Radical Cystectomy, Laparoscopic Radical Cystectomy, and Robot-Assisted Radical Cystectomy

	ORC, n = 150	LRC, n = 22	RARC, n = 58	p
Age, years	68.0 (60.0–73.0)	65.0 (62.8–74.0)	61.5 (54.8–72.0)	0.017
Male sex, n (%)	123 (82.0)	20 (90.9)	54 (93.1)	0.093
Body mass index, kg/m²	23.9 (21.9–26.3)	23.3 (20.9–26.1)	22.8 (20.8–25.5)	0.240
Prior intravesical therapy, n (%)	28 (18.7)	2 (9.1)	11 (19.0)	0.440
ASA score group, n (%)				0.104
1	33 (22.0)	4 (18.2)	16 (27.6)
2	106 (70.7)	15 (68.2)	38 (65.5)
3	11 (7.3)	2 (9.1)	4 (6.9)
4	0 (0)	1 (4.5)	0 (0)
Clinical stage, n (%)				0.345
≤T2	72 (48.0)	10 (45.5)	34 (58.6)
≥T3	78 (52.0)	12 (54.5)	24 (41.4)
Clinical grade, n (%)				0.198
I	0 (0)	1 (4.5)	1 (1.7)
II	34 (22.7)	3 (13.6)	13 (22.4)
III	116 (77.3)	18 (81.8)	44 (75.9)
Neoadjuvant chemotherapy, n (%)	3 (2.0)	1 (4.5)	1 (1.7)	0.720

All values are given as median (interquartile range) unless otherwise indicated.

ASA = American Society of Anesthesiologists; LRC = laparoscopic radical cystectomy; ORC = open radical cystectomy; RARC = robot-assisted radical cystectomy.

Perioperative and pathologic variables are shown in Table 2. The proportion of patients undergoing conduit procedure in urinary diversion was 75.8%, 100%, and 41.4% for ORC, LRC, and RARC, respectively (p < 0.001). Patients undergoing ORC received more intraoperative allogenic blood transfusions than patients who underwent LRC or RARC (p < 0.001). The proportion of patients with pathologic stage ≥pT3 in ORC, LRC, and RARC groups was 53.3%, 45.5%, and 43.1%, respectively (p = 0.377). There were no significant differences in pathologic tumor staging or the presence of concomitant CIS, LVI, PSM, and LN involvement among the groups (p = 0.187, 0.290, 0.217, 0.633, and 0.839, respectively). Adjuvant chemotherapy was administered to 52 (36%) patients with ORC, 3 (13.6%) patients with LRC, and 20 (34.5%) patients with RARC (p = 0.136). PSM rates were 4.0% (6/150) and 3.4% (2/58) in ORC and RARC, respectively. In patient with PSM, adjuvant chemotherapy was used in 66.7% (4/6) of patients and 50.0% (1/2) of patients in ORC and RARC, respectively.

Table 2.

Perioperative and Pathologic Outcomes for the Open Radical Cystectomy, Laparoscopic Radical Cystectomy, and Robot-Assisted Radical Cystectomy

	ORC, n = 150	LRC, n = 22	RARC, n = 58	p
Urinary diversion type,^a n (%)				<0.001
Ileal conduit	113 (75.8)	21 (100)	24 (41.4)
Neobladder	31 (20.8)	0 (0)	34 (58.6)
Ureterocutaneostomy	5 (3.4)	0 (0)	0 (0)
Lymph node yield	15.0 (10.0–20.0)	19.5 (14.8–27.3)	18.0 (14.0–25.3)	0.002
Estimated blood loss, mL	840.0 (557.5–1500.0)	400.0 (300.0–700.0)	500.0 (368.8–700.0)	<0.001
Transfusion at operative field, n (%)	89 (59.3)	3 (13.6)	6 (10.3)	<0.001
Operative time, minutes	466.0 (404.3–547.3)	524.0 (490.8–593.8)	501.5 (440.8–604.0)	0.002
Ileal conduit	464.0 (405.5–547.5)	527.0 (490.5–596.5)	437.5 (372.0–525.5)	0.001
Neobladder	482.0 (437.0–545.0)	—	564.0 (490.8–666.8)	0.001
Hospital stay, days	22.0 (17.0–32.0)	12.0 (10.0–15.0)	28.0 (18.0–34.3)	<0.001
Ileal conduit	21.0 (17.0–28.5)	12.0 (10.0–15.0)	18.5 (17.0–22.8)	<0.001
Neobladder	26.0 (22.0–48.0)	—	32.5 (27.5–37.0)	0.286
Pathologic stage, n (%)				0.377
≤T2	70 (46.7)	12 (54.5)	33 (56.9)
≥T3	80 (53.3)	10 (45.5)	25 (43.1)
Pathologic grade, n (%)				0.187
I	0 (0)	0 (0)	2 (3.4)
II	17 (11.3)	2 (9.1)	7 (12.1)
III	133 (88.7)	20 (90.9)	49 (84.5)
Concomitant CIS, n (%)	36 (24.0)	2 (9.1)	13 (22.4)	0.290
Concomitant LVI, n (%)	58 (38.7)	10 (45.5)	25 (43.1)	0.217
Positive surgical margin, n (%)	6 (4.0)	0 (0)	2 (3.4)	0.633
Lymph node positive, n (%)	39 (26.0)	7 (31.8)	15 (25.9)	0.839
Adjuvant chemotherapy, n (%)	52 (34.7)	3 (13.6)	20 (34.5)	0.136

All values are given as median (interquartile range) unless otherwise indicated.

Missing data for one patient in each of the ORC group and LRC group.

CIS = carcinoma in situ; LVI = lymphovascular invasion.

The median follow-up duration was 27.9 (IQR: 14.7–47.9), 28.8 (IQR: 15.7–41.8), and 32.0 (IQR: 15.5–45.4) months for ORC, LRC, and RARC, respectively (p = 0.955). Disease recurrence occurred in 52, 7, and 13 patients in ORC, LRC, and RARC groups, respectively. Overall, 42 patients in the ORC group, 5 in the LRC group, and 11 in the RARC group had died at the time of analysis, among whom 38, 5, and 9, respectively, died from bladder cancer. There was no significant difference in PFS, CSS, and OS according to type of surgical approach (p = 0.253, 0.431, and 0.527, respectively, Fig. 1). Subgroup analysis revealed that PFS, CSS, and OS were not significantly different for patients with organ-confined cancer (≤pT2) (Fig. 2) or patients with extravesical involvement by cancer (≥pT3) (Fig. 3). Multivariable Cox regression analyses revealed that pathologic tumor stage was independently associated with a significantly increased risk of postoperative tumor recurrence (hazard ratio [HR] = 2.40, p = 0.010), death from bladder cancer (HR = 6.37, p < 0.001), and death from all causes (HR = 5.82, p < 0.001). LVI (HR = 2.62, p = 0.006) was independently associated with postoperative tumor recurrence. PSM was a significant risk factor for tumor recurrence and all-cause death (HR = 4.42, p = 0.002 and HR = 2.85, p = 0.039, respectively). BMI, ASA score ≥3, and intraoperative allogenic blood transfusion were significantly associated with death from bladder cancer (HR = 0.89, p = 0.018; HR = 2.62, p = 0.046; HR = 2.40, p = 0.017, respectively) and all-cause death (HR = 0.88, p = 0.010; HR = 3.95, p = 0.001; HR = 2.77, p = 0.004, respectively). Age was an independent predictive factor for all-cause death (HR = 1.04, p = 0.044) (Table 3).

FIG. 1.

Cumulative survival of 230 patients after radical cystectomy for bladder cancer, stratified by surgical approach type (ORC, LRC, and RARC). (A) Recurrence-free survival; (B) cancer-specific survival; (C) overall survival. LRC = laparoscopic radical cystectomy; ORC = open radical cystectomy; RARC = robot-assisted radical cystectomy.

FIG. 2.

Cumulative survival of 115 patients with organ-confined cancer (≤pT2) after radical cystectomy for bladder cancer, stratified by surgical approach type (ORC, LRC, and RARC). (A) Recurrence-free survival; (B) cancer-specific survival; (C) overall survival.

FIG. 3.

Cumulative survival of 115 patients with extravesical involvement by cancer (≥pT3) after radical cystectomy for bladder cancer, stratified by surgical approach type (ORC, LRC, and RARC). (A) Recurrence-free survival; (B) cancer-specific survival; (C) overall survival.

Table 3.

Multivariable Cox Proportional Hazard Regression Analyses to Predict Postoperative Tumor Recurrence, Death from Bladder Cancer, and Death from All-Cause in 230 Patients with Bladder Cancer Treated with Radical Cystectomy

	Tumor recurrence			Death from bladder cancer			Death from all-cause
Characteristics	HR	95% CI	p	HR	95% CI	p	HR	95% CI	p
Age, years	1.02	0.99, 1.05	0.223	1.03	0.99, 1.07	0.144	1.04	1.00, 1.07	0.044
Sex
Female	Reference			Reference			Reference
Male	1.01	0.49, 2.06	0.990	1.44	0.61, 3.44	0.407	1.49	0.64, 3.51	0.358
Body mass index, kg/m²	0.99	0.91, 1.07	0.765	0.89	0.80, 0.98	0.018	0.88	0.80, 0.97	0.010
ASA score group
1–2	Reference			Reference			Reference
3–4	1.55	0.52, 4.64	0.432	2.62	1.02, 6.74	0.046	3.95	1.77, 8.81	0.001
Surgical approach
ORC	Reference			Reference			Reference
LRC	1.48	0.60, 3.65	0.369	1.03	0.35, 3.08	0.954	0.92	0.31, 2.70	0.873
RARC	0.97	0.48, 1.97	0.937	1.20	0.50, 2.88	0.686	1.48	0.65, 3.38	0.350
Transfusion
No	Reference			Reference			Reference
Yes	1.70	0.95, 3.05	0.074	2.40	1.17, 4.94	0.017	2.77	1.38, 5.57	0.004
Pathologic stage
≤T2	Reference			Reference			Reference
≥T3	2.40	1.23, 4.69	0.010	6.37	2.66, 15.25	<0.001	5.82	2.55, 13.31	<0.001
Concomitant CIS
No	Reference			Reference			Reference
Yes	0.69	0.37, 1.29	0.245	1.15	0.57, 2.34	0.699	1.03	0.52, 2.03	0.936
Concomitant LVI
No	Reference			Reference			Reference
Yes	2.62	1.31, 5.23	0.006	1.39	0.63, 3.08	0.417	1.42	0.66, 3.05	0.364
Positive surgical margin
No	Reference			Reference			Reference
Yes	4.42	1.76, 11.11	0.002	2.53	0.85, 7.57	0.097	2.85	1.06, 7.67	0.039
Positive lymph node
No	Reference			Reference			Reference
Yes	1.37	0.76, 2.50	0.299	1.75	0.85, 3.60	0.130	1.72	0.86, 3.44	0.127
Adjuvant chemotherapy
No	Reference			Reference			Reference
Yes	1.02	0.55, 1.87	0.963	0.57	0.27, 1.20	0.141	0.63	0.31, 1.28	0.200

CI = confidence interval; HR = hazard ratio.

Discussion

While ORC provides the best cancer control for the treatment of localized muscle-invasive bladder cancer, it is associated with significant perioperative complications, even when performed in large-volume centers.^16,17 Accordingly, there has been growing interest in minimally invasive surgical approaches such as LRC and RARC, which have been rapidly adopted in an attempt to improve morbidity and mortality rates. While a number of studies have demonstrated surgical feasibility with fewer complications and comparable oncologic results,^4
–6 LRC has not been widely adopted due to its long learning curve and prolonged operative time. More recently, the emergence of RARC with the promise of improving the learning curve has enabled more surgeons to perform minimally invasive RC with fewer complications and favorable oncologic outcomes. We previously reported fewer early postoperative complications after RARC relative to ORC at our institution.¹⁴ With the wider availability of robotic technology, many institutions have preferentially adopted RARC over LRC and have reported a shorter learning curve, favorable perioperative outcomes, and lower complications.^7

–11 However, despite these potential advantages, the oncological efficacy of LRC and RARC remains largely unclear.

The perioperative outcomes of this study showed that the operative time was significantly shorter and the intraoperative transfusion rate was significant higher in ORC compared with LRC or RARC. It is not surprising that patients who underwent ORC had a significant higher intraoperative blood loss (median: 840.0 mL; IQR: 557.5–1500.0) compared with patients who underwent LRC (median: 400.0 mL; IQR: 300.0–700.0) or RARC (median: 500.0 mL; IQR: 368.8–700.0). Patients undergoing ORC (median: 22.0 days; IQR: 17.0–32.0) or RARC (median: 28.0 days; IQR: 18.0–34.3) had longer hospital stays than patients undergoing LRC (median: 12.0 days; IQR: 10.0–15.0), while this might be affected by several variables, including patient characteristics, social circumstances, complications, discharge criteria, and health insurance, which might vary nationally. There were no significant differences in pathologic tumor staging, presence of concomitant CIS, LVI, PSM, LN involvement, and receipt of adjuvant chemotherapy according to surgical technique (Table 2).

Longer operative times and lower transfusion rates for LRC or RARC compared with ORC have been demonstrated in most previous surgical series.^5,18,19 Aboumarzouk and colleagues⁵ reported that patients undergoing LRC had significantly longer operative times (mean difference 56.8 minutes) and lower transfusion requirements (26.2% [49/187] in LRC vs. 51.1% [93/182] in ORC) than those undergoing ORC. In their systemic review,^18,19 the Pasadena Consensus Panel reported that mean operative times were longer for RARC than for ORC (mean difference 78.3 minutes) and transfusion rates in RARC and ORC were 19.3% (126/654) and 55.2% (428/775), respectively. Oncologic results after RC can be estimated by several factors, but acceptable LN yields and PSM rates have previously been shown to serve as surrogates for oncologic outcomes. In particular, Herr and colleagues²⁰ proposed that a PSM rate less than 10% with a median of 10 to 14 LNs examined is a reasonable overall standard for RC. PSM rates for ORC, LRC, and RARC in this study were 4.0%, 0%, and 3.4%, respectively (p = 0.633). Median LN yields were significantly lower in ORC than in LRC or RARC (p = 0.002), but all gave adequate yields of >10 LNs. Recent studies of the oncologic outcomes of LRC or RARC also revealed that the PSM rates varied from 0% to 13%, and no difference was found in the rate of PSM between groups (ORC vs. LRC and ORC vs. RARC),^5,18,19 which was consistent with our study.

In this retrospective study, we noted that RFS, CSS, and OS were not affected by surgical technique (Fig. 1). To our knowledge, there are few studies focusing on differences among the three surgical approaches with respect to oncologic outcomes. Recently, Khan and colleagues reported that rates of CSS were 69%, 93%, and 79% with a median follow-up of 3.2 years in ORC, LRC, and RARC groups, respectively.²¹ In contrast to the study by Khan and colleagues, we additionally performed subgroup analysis for patients with ≤pT2 or ≥pT3 and confirmed that there were no significant differences for patients with ≤pT2 and ≥pT3 according to surgical technique with regard to RFS, CSS, and OS (Figs. 2 and 3).

This study shows that pathologic tumor stage predicted tumor recurrence, CSS, and OS. The presences of LVI and PSM were associated with RFS while BMI, intraoperative transfusion, and tumor grade were significantly associated with CSS and OS. Age was also a predictive factor associated with OS. Consistent with our study, several previous studies also demonstrated that these prognostic factors were associated with oncologic outcomes in patients who underwent RC.^22

–25 However, the type of surgical approach for RC was not a significant predictor of RFS, CSS, and OS.

This study has several limitations. Foremost, the retrospective nature of this study should be considered. There might have been a selection bias related to the nature of our institutional referral practice. Moreover, a selection bias might also result from the surgeon effect. In this study, five different surgeons performed RC (one performed only ORC, three performed both ORC and RARC, and one performed both LRC and RARC). The choice of surgical approach was mainly determined by the surgeon's preference in addition to the patient's motivation. Because we did not specifically consider the surgeon effect, it remains unclear whether this factor influenced the outcomes. However, this can also be considered a strength of this study because it represents real clinical practice and our results may therefore be more generalizable than a single surgeon experience. In addition, the uneven distribution of patients among the ORC, LRC, and RARC groups should be considered. We retrospectively reviewed 271 consecutive patients who had undergone RC during the same period. Because the type of surgical approach is determined by several factors, including patient's characteristics and surgeon's preference, the distribution among ORC, LRC, and RARC was different. This uneven distribution could have affected the observed differences.

Nevertheless, despite these limitations, our study results provide important and informative data supporting minimally invasive cystectomy as an alternative to the open approach.

Conclusions

Our findings indicate that short-term oncologic outcomes obtained after minimally invasive cystectomy such as LRC or RARC are comparable to those of conventional ORC for the management of patients with muscle-invasive bladder cancer. The type of surgical approach is not associated with tumor recurrence, death from bladder cancer, or all-cause death after RC regardless of pathologic tumor stage.

Footnotes

Acknowledgment

Some of the material in the article was presented at the 33rd World Congress of Endourology 2015 (October 1–4, 2015).

Author Disclosure Statement

No competing financial interests exist.

Abbreviations Used

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