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Robotic and Laparoscopic Radical Cystectomy for Bladder Cancer: Long-term Oncologic Outcomes
European Urology, 1, 65, pages 193 - 200
Extended oncologic outcomes after minimally invasive cystectomy have not been previously reported.
To report outcomes of robot-assisted radical cystectomy (RARC) and laparoscopic radical cystectomy (LRC) for bladder cancer (BCa) at up to 12-yr follow-up.
Design, setting, and participants
All 121 patients undergoing RARC or LRC for BCa between December 1999 and September 2008 at a tertiary referral center were retrospectively evaluated from a prospectively maintained database.
RARC or LRC.
Outcome measurements and statistical analysis
Primary end points were overall survival (OS), cancer-specific survival (CSS), and recurrence-free survival (RFS) calculated using Kaplan-Meier curves. Secondary end points were survival analysis by number of lymph nodes (LNs) and type of procedure. Surgical outcomes, including complications, were analyzed.
Results and limitations
Most tumors were muscle invasive (≥pT2; n = 81; 67%) urothelial carcinomas (n = 102; 84%). Extended LN dissection was performed in 98 patients (81%), with a median of 14 nodes removed (interquartile range [IQR]: 8–18). Twenty-four patients (20%) had node-positive disease (N1: 10 [8%]; N2: 14 [12%]). Eight patients (6.6%) had positive soft tissue margins. Median follow-up was 5.5 yr (mean: 5.9; IQR: 4.2–8.2; range: 0.13–12.1). At last follow-up, 58 patients (48%) had no evidence of disease, 3 (2%) were alive with recurrence, 59 (49%) had died, and status was unknown in 1. Twenty-eight patients (23%) died from cancer-specific causes, 20 (17%) from unrelated causes, and 11 (9%) from unknown causes. The 10-yr actuarial OS, CSS, and RFS rates were 35%, 63%, and 54%, respectively. At last follow-up, OS for pT0, pTis/a, pT1, pT2, and pT3 versus pT4 was 67%, 73%, 53%, 50%, and 16% versus 0%, respectively (p = 0.02). At last follow-up, CSS for pT0, pTis/a, pT1, pT2, and pT3 versus pT4 was 100%, 91%, 74%, 77%, and 56% versus 0%, respectively (p = 0.03).
The longest oncologic outcomes following RARC and LRC for BCa reported demonstrates results similar to those reported for open RC. Continued analysis and direct randomized comparison between techniques is necessary.
Keywords: Bladder neoplasm, Minimally invasive, Laparoscopy, Robotic assisted, Urinary diversion.
Muscle-invasive urothelial bladder cancer (BCa) has long been treated with open radical cystectomy (ORC) because it is a disease that relies heavily on aggressive surgical treatment to optimize patient survival  and . Although ORC with extended pelvic lymph node dissection (PLND) is the current gold standard for organ-confined muscle-invasive or recurrent high-grade superficial BCa, minimally invasive techniques have increased in application with the goal of minimizing patient morbidity. In nonrandomized comparisons, robot-assisted radical cystectomy (RARC) and laparoscopic radical cystectomy (LRC) have been associated with longer operative time, yet decreased blood loss, lower transfusion rate, quicker bowel function, decreased hospital stay, and more rapid recovery  . Because of encouraging perioperative and intermediate-term (5-yr) oncologic data for minimally invasive cystectomy, RARC and LRC are increasing in popularity, albeit in highly specialized tertiary medical centers  . The paucity of long-term oncologic outcomes of RARC and LRC remains a valid concern, especially given the vital importance of negative surgical margins (NSM) and the thoroughness of lymph node dissection (LND) in radical cystectomy (RC) surgery. As such, reported herein are long-term oncologic outcomes of RARC and LRC with follow-up of up to 12 yr (median: 5.5).
2. Patients and methods
From December 1999 to September 2008, six surgeons performed RARC/LRC with curative intent for BCa in 121 patients. Inclusion criteria comprised patients with recurrent or high-grade superficial or muscle-invasive urothelial cell carcinoma (UCC) or another subtype without evidence of extravesical spread or metastatic disease on preoperative imaging. High-grade recurrent superficial BCa was defined as pT1G3 UCC or any BCa that had recurred despite three or more transurethral resections (TURs) or treatment with intravesical bacillus Calmette-Guérin. Twelve patients (10%) received neoadjuvant chemotherapy. Adjuvant chemotherapy was administered to 11 patients (9%) based on surgical pathology and follow-up imaging.
Demographic data, preoperative BCa data, perioperative data, complications, pathology, adjuvant treatments, and follow-up data were collected in a prospective computerized, secure database with institutional review board approval. Typical postcystectomy follow-up consisted of history as well as physical and serum creatinine at 1 mo along with abdominopelvic computed tomography scans and chest x-ray every 6 mo for 2 yr, then annually thereafter. For this study, follow-up data were obtained either by chart review or telephone contact directly with the patient or with surviving family members or by a check of the Social Security Death Index. Complications were recorded prospectively and graded retrospectively according to an established five-grade Clavien classification  .
The technique of RARC and LRC with urinary diversion (UD) has previously been reported  and . During the initial development of the technique in 2000, standard PLND was used, which consisted of excising lymphatic tissue from the external iliac artery, external iliac vein, obturator nerve, and hypogastric artery up to the common iliac artery. Since August 2002, most surgeries have used an extended template for excising lymphatic tissue, including standard PLND in addition to resection of tissue medial to the genitofemoral nerve and along the common iliac artery up to the aortic bifurcation  . The types of UD, performed mostly extracorporeally, and other intraoperative data are listed in Table 1 .
|Median (range, IQR) or no. (%)||Complications, Clavien grade, no. (%)|
|Type of procedure|
|Pure laparoscopic||17 (14)||9 (53)||2 (22)||2 (22)||4 (44)||1 (11)||0 (0)|
|Laparoscopic assist *||87 (72)||34 (39)||9 (26)||12 (35)||7 (21)||6 (18)||0 (0)|
|Robotic assist *||17 (14)||9 (53)||2 (22)||2 (22)||3 (33)||2 (22)||0 (0)|
|Type of UD|
|Bricker ileoconduit||84 (69)||36 (43)||10 (28)||14 (39)||8 (22)||4 (11)||0 (0)|
|Orthotopic neobladder||29 (24)||11 (38)||2 (18)||2 (18)||4 (36)||3 (27)||0 (0)|
|Indiana pouch||6 (5)||4 (67)||1 (25)||0 (0)||1 (25)||2 (50)||0 (0)|
|Anephric||2 (2)||1 (50)||0 (0)||0 (0)||1 (100)||–||0 (0)|
|Total complications **||–||52 (43)||13 (25)||16 (31)||14 (27)||9 (17)||0 (0)|
|EBL, ml||400 (25–4000, 200–750)||–||–||–||–||–||–|
|OR time, h||7.5 (2–12, 6–9.4)||–||–||–||–||–||–|
* Laparoscopic assist and robotic assist included laparoscopic or robotic cystectomy with a planned extracorporeal UD.
** Complications according Clavien grade  .
IQR = interquartile range; UD = urinary diversion; EBL = estimated blood loss; OR = operating room.
Outcome measures evaluated included pathologic and perioperative outcomes, disease recurrence, overall survival (OS), and cancer-specific survival (CSS). Kaplan-Meier curves were constructed to estimate the survival rate for the whole sample and within subgroups. The log-rank test was used to compare the Kaplan-Meier curves between stage, number of lymph nodes (LNs) removed, type of procedure, and margin status. All statistics were two-tailed, with p < 0.05 considered significant. Analysis was done using JMP Statistical Discovery (SAS Institute, Cary, NC, USA).
3.1. Patient demographics
The study population is described in Table 2 . History of previous upper-tract and nonurologic cancers were present in 11 patients (9%). The number of previous TURs of bladder tumor ranged from one to seven (mean: 1.5).
|Demographic||Median (range, IQR) or no. (%)|
|Age, yr||70 (26–87, 60–77)|
|BMI, kg/m2||26 (17.4–40, 24–30)|
|Previous medical history|
|Cardiac disease||41 (34)|
|Other malignancy||12 (10)|
IQR = interquartile range; BMI = body mass index; ASA = American Society of Anesthesiologists; HTN = hypertension.
3.2. Surgical outcomes
Intraoperative data are detailed in Table 1 . Two surgeons performed 2–4 cases (2–3%) each, with the remaining four surgeons performing 12–65 cases (10–54%). Six patients were converted to open surgery throughout our experience because of patient habitus, multiple prior abdominal surgeries with adhesions, difficulty in ventilation, elective conversion for locally advanced disease, adherent pelvic nodes, or external iliac venotomy requiring open repair.
Complications occurred in 52 patients (43%), largely related to the UD; many of these complications occurred prior to routine performance of extracorporeal UD (laparoscopic assisted procedure type; Table 1 ). Twenty-three patients (19%) had Clavien grade 3–5 complications. A complication requiring surgical intervention (Clavien grade 3) was required in a total of 14 patients (11%), including exploratory laparotomy with lysis of adhesions in 9 patients (7%), repair of urine leak in 1 patient (1%), repair of vaginal fistula in 2 patients (2%) and excision of pouch in 2 patients (2%). These procedures occurred within 30 d of surgery for seven patients (64%), within 90 d for one patient (9%), and >90 d from the original surgery in the remaining two patients (18%). A Clavien grade 4 complication was present in nine patients (7%) and consisted of respiratory failure in four patients (3%), severe hemorrhage in one patient (1%), sepsis in one patient (1%), and cardiac dysfunction in three patients (2%).
3.3. Oncologic outcomes
Final pathology data are shown in Table 3 . UCC was present in 101 cases (83%), squamous cell carcinoma in 7 (6%), and adenocarcinoma in 3 (2%), while the remaining 8 patients (8%) had pT0 status. High-grade tumors (≥2) were present in 113 patients (93%). Median LN count was 14 (interquartile range [IQR]: 8–18), including 5 patients (4.1%) in whom LND was not performed because of comorbidity or dense adhesive tissue around the vessels. Eight patients (6.6%), all of whom had extravesical disease, had a positive soft tissue margin. N1 and N2 disease were confirmed in 10 (8%) and 14 (12%) patients, respectively.
|Stage||Patients, no. (%)||PSM, no. (%)||LN range (median, IQR)||Node staging, no. (%)|
|pT0||12 (10)||0 (0)||0–20 (12, 4–17)||12 (10)||0 (0)||0 (0)|
|pTa||4 (2)||0 (0)||4–17 (12, 5–17)||3 (2)||0 (0)||0 (0)|
|pTis||7 (6)||0 (0)||1–26 (14, 9–16)||7 (6)||0 (0)||0 (0)|
|pT1||17 (15)||0 (0)||3–31 (14, 8–23)||18 (15)||0 (0)||0 (0)|
|pT2||33 (17)||1 (1)||4–26 (14, 9–21)||31 (26)||1 (1)||1 (1)|
|pT3||44 (36)||6 (5)||2–28 (14, 8–18)||26 (21)||9 (7)||10 (8)|
|pT4||4 (3)||1 (1)||2–20 (7, 2–16)||1 (1)||0 (0)||3 (2)|
|Total||121||8 (6.6)||14 (8–18)||98 (81)||10 (8)||14 (12)|
PSM = positive surgical margin; LN = lymph node; IQR = interquartile range.
Median follow-up was 5.52 yr (mean: 5.9; IQR: 4.2–8.2; range: 0.13–12.1). Nine patients (7%) had >10 yr of follow-up. At last follow-up, 58 patients (48%) had no evidence of disease, 3 (2%) were living with recurrence, 59 (49%) were dead, and status was unknown for 1 patient. A flow chart specifying the type of procedure, pathology, and causes of death is shown in Figure 1 . Three patients (5%) died within 2 mo of the procedure and were counted as cancer-specific deaths, whereas 25 (42%) died from cancer-related causes >60 d from the procedure. Importantly, to our knowledge, no patient developed port-site recurrence. The actuarial OS, CSS, and recurrence-free survival rates were 55%, 73%, and 71% at 3 yr; 48%, 71%, and 65% at 5 yr; and 35%, 63%, and 54% at 10 yr, respectively ( Fig. 2 ). Because cause of death was unknown in 11 patients (9%), a secondary analysis was performed in which all of these patients were assumed to have died from cancer-specific causes. By this analysis, the recalculated CSS at 3, 5, and 10 yr was 66%, 62%, and 55%, respectively.
There was no statistically significant difference in OS with respect to patient age or gender. The 10-yr CSS for females was 82% and for males was 68%, which was not statistically significant (p = 0.43). Patients who had more than the median number of LNs resected (14 nodes) had improved 10-yr OS (54% vs 34%; p = 0.01). Increasing pathologic T stage was associated with worse OS and CSS. At 7 yr, OS for pT0, pTis/a, pT1, and pT2 versus pT3 was 67%, 73%, 53%, and 50% versus 16%, respectively (p = 0.02). At 7 yr, CSS for pT0, pTis/a, pT1, and pT2 versus pT3 was 100%, 91%, 74%, and 77% versus 56%, respectively (p = 0.03). The OS and CSS for pT4 disease could not be calculated, because all patients in this subgroup had died prior to 3-yr follow-up. At 10 yr, compared with patients with organ-confined disease, those with extravesical (>pT2) disease had worse OS (48% vs 15%; p = 0.004) and CSS (70% vs 53%; p = 0.007), respectively ( Fig. 3 ). In addition, the absence of nodal disease was associated with prolonged survival, with CSS for N0, N1, and N2 disease being 79%, 50%, and 47% at 3 yr, respectively (p = 0.002; Table 4 ; Fig. 3 ).
|Subgroup||Follow-up, yr, median (IQR)||No. (%)||OS, % **||CSS, % **|
|pT0||4.9 (3.3–6.7)||12 (10)||67||100|
|pTa||5.4 (5.2–5.8)||3 (2)||73||100|
|pTis||5.1 (4.0–5.8)||7 (6)||73||91|
|pT1||5.1 (3.7–7.9)||18 (15)||53||74|
|pT2||5.4 (3.4–8.2)||33 (17)||50||77|
|pT3||5.7 (5.1–8.4)||44 (36)||16||56|
|pT4||9.4 (8.8–11.7)||4 (3)||N/A||N/A|
|Organ confined (≤pT2)||5.3 (3.7–6.6)||73 (60)||48||70|
|Not organ confined (>pT2)||5.7 (5.3–8.8)||48 (39)||15||53|
|pN0||5.3 (3.7–7.04)||97 (80)||49||68|
|pN1||5.9 (5.4–9.4)||10 (8)||N/A||50|
|pN2||5.6 (5.2–8.9)||14 (12)||15||47|
|LN <14||5.7 (5.0–9.1)||67 (55)||34||62|
|LN ≥14||5.3 (3.6–6.1)||54 (45)||54||61|
|NSM||5.5 (3.9–8.2)||113 (9)||42||65|
|PSM||6.2 (5.3–8.3)||8 (7)||N/A||N/A|
|Pure laparoscopic||9.1 (5.3–10.1)||17 (14)||52||68|
|Laparoscopic assist *||5.3 (3.8–6.5)||87 (72)||58||77|
|Robotic assist *||5.6 (5.3–5.7)||17 (14)||39||69|
* Laparoscopic assist and robotic assist included laparoscopic or robotic cystectomy with a planned extracorporeal urinary diversion.
** OS and CSS at last follow-up.
IQR = interquartile range; OS = overall survival; CSS = cancer-specific survival; LN = lymph node; NSM = negative surgical margin; PSM = positive surgical margin.
Currently, ORC with extended PLND is the gold-standard treatment for muscle-invasive or recurrent superficial high-grade BCa. Minimally invasive robotic and laparoscopic approaches have shown technical promise and are being increasingly adopted, as comparisons of perioperative and pathologic features have demonstrated encouraging results  and . Concerns about long-term oncologic efficacy of RARC/LRC remain to be fully addressed, specifically as they relate to the thoroughness of LND, the reliability of routinely achieving NSM, and concerns about the impact of pneumoperitoneum on BCa cells and port-site metastasis.
A brief summary of the follow-up and survival rates available in the current literature are presented in Table 5 . The initial patients in this series were some of the first done anywhere with minimally invasive techniques, and the authors were still developing the technique of LRC. During this developmental period, our primary focus was on bladder extirpation, with patient selection limited to those with low-volume organ-confined disease. This patient-selection bias can be seen when comparing our rates of organ-confined disease with previous ORC series, with our pT3 and pT4 rates being 36% and 3% versus 36% and 16% for ORC  . Our data set is unable to provide 3-yr survival rates for pT4 disease, as there were relatively few patients with pT4 disease (n = 4; 3%), all of whom died prior to the 3-yr time point. In contrast, Dalbagni et al. reported a 5-yr OS of 27% for pT4 disease, and Stein et al. reported a 10-yr OS of 22%  and . Our survival rates for ≤pT3 disease are consistent with the previously published ORC, LRC, and RARC oncologic outcomes , , , and . These variations in patient populations can be ascribed to patient-selection bias during the learning curve of RARC/LRC, given that this series includes some of the first cases of LRC performed anywhere ( Table 5 ).
|Type of procedure||Reference||No. of patients||Patients per T stage, %||Follow-up, yr (range)||OS||CSS||RFS|
|ORC||Stein et al., 2001 ||1054||pT0–2
|10 * (0.1–28)||66%: 5 yr
43%: 10 yr
|–||68%: 5 yr
60%: 10 yr
|Dotan et al., 2007 ||1589||pT0–2
|10||–||71%: 5 yr||–|
|Dalbagni et al., 2001 ||300||pT0–2
|5||45%: 5 yr||57%: 5 yr||–|
|Madersbacher et al., 2003 ||507||pTa–2
|3.8 (0.1–14.7)||59%: 5 yr
37%: 10 yr
|–||62%: 5 yr
50%: 10 yr
|Nepple et al., 2011 ||29||pT0–2
|1.2 (0.7–1.7) **||63%: 2 yr||63%: 2 yr||58%: 2 yr|
|Konety et al., 2003 ||1923||pTa–2
|5.5 (0–10.9)||62%: ≥2 yr||–||–|
|LRC||DeGer et al., 2004 ||20||pTa–2
|2.75 * (1.1–3.5)||83%: 2–3 yr||83%: 2–3 yr||75%: 2–3 yr|
|Hemal et al., 2007 ||30||pTa–2
|3.2 (1.3–4.5)||87%: 3 yr||–||77%: 3 yr|
|Huang et al., 2010 ||171||pTa–2
|3.1 * (0.25–6.9)||74%: 5 yr||81%: 5 yr||72.6%: 5 yr|
|RARC||Murphy et al., 2008 ||23||pT0–2
|1.4 (0.3–3.3)||96%: 1–2 yr||96%: 1–2 yr||92%: 1–2 yr|
|Nepple et al., 2011 ||36||pT0–2
|1.2 (0.6–1.7) **||68%: 2 yr||75%: 2 yr||67%: 2 yr|
|Kauffman et al., 2011 ||85||pT0–2
|1.5||79%: 2 yr||85%: 2 yr||73%: 2 yr|
|Dasgupta et al., 2008 ||20||pT0–2
|1.9 * (0.6–3.7)||95%: 3.5 yr||–||90%: 3.5 yr|
|Pruthi et al., 2008 ||50||pT0–2
|1.1 (0.2–2)||90%: 1 yr||94%: 1 yr||86%: 1 yr|
|Hayn et al., 2011 ||164||pT0–2
|0.7 * (0–3.9)||50%: 3 yr #||–||–|
|Jonsson et al., 2011 ||45||pT0–2
|2.1 * (0.3–7.5)||–||86%: 3 yr||84%: last follow-up|
|Khan et al., 2013 ||14||pT0–2
|(5–8)||64%: >5 yr||75%: >5 yr||50%: >5 yr|
|5.52 * (0.13–12.1)||55%: 3 yr
48%: 5 yr
35%: 10 yr
|73%: 3 yr
71%: 5 yr
63%: 10 yr
|71%: 3 yr
65%: 5 yr
54%: 10 yr
* Median value reported.
** IQR reported.
# Approximate value.
OS = overall survival; CSS = cancer-specific survival; RFS = recurrence-free survival; ORC = open radical cystectomy; LRC = laparoscopic radical cystectomy; RARC = robot-assisted radical cystectomy; IQR = interquartile range.
The cephalad extent of LND for RC is currently debated, but there is evidence that an extended LND provides a survival advantage, presumably because it identifies patients who require adjuvant chemotherapy, provides tumor debulking, and may remove micrometastasis , , and . A median of 14 LNs were removed in our series, which approximates previously reported data for open (average/median of 13–43 nodes), laparoscopic (average/median of 10–16 nodes), and robot-assisted (average/median of 16–19 nodes) RC , , , , , , , , and . It has been shown that pathologic processing of individual node packets can significantly affect total node counts  . In this cohort, LNs were typically submitted en bloc, which could also have artificially lowered nodal counts. In addition, it should be noted that we included in our analysis five patients (4.1%) in whom LND was not performed because of comorbidity or dense adhesive tissue around the vessels, which was not likely to markedly change the LN counts and skew the distribution. Nevertheless, although we did not note a CSS advantage, we did note an OS advantage in patients who had >14 LNs removed. These data are in keeping with previously published reports, reiterating the importance of an extended and diligent LND. More recently, an increased focus on thorough high-extended LND during RARC/LRC yielded a median of 31 nodes  .
Positive soft tissue margin rates during cystectomy range from 1% to 6.3% , , and . Our positive soft tissue margin rate was 6.6%. These positive margins were more likely to occur in patients with extravesical extension. We were unable to discern the exact location of positive margins from an additional retrospective review of the pathology reports. We recognize that our early margin rates are higher than desirable and anticipate improvement with more mature experience. Indeed, positive margin rates during RARC have decreased to 0% of 23 patients, 0% of 50 patients, and 6% of 36 patients in three recent series , , and .
Limitations of this study include the relatively few patients who have completed 12 yr of follow-up. We identified 3 patients alive at 12 yr and 21 patients who were alive with >5-yr follow-up. This reflects the slow and careful initial incorporation of RARC/LRC into our BCa management protocol as well as the high mortality of this patient population. This series includes patients who were operated on at the inception of the surgical learning curve for intracorporeal diversion, which has now been shown to have an improved safety profile  . Also, our cohort is heterogeneous, including patients undergoing RARC and LRC, patients with different bladder tumors undergoing a variety of intra- and extracorporeal diversions. Because of the relatively few patients evaluated, our study was not powered to discern differences in survival stratified by use of neoadjuvant versus adjuvant chemotherapy, intra- versus extracorporeal UD, type of minimally invasive surgery, and differing LN templates. Unfortunately, determination of a typical learning curve for RARC/LRC is outside the scope of the present article but certainly warrants further investigation. However, despite these limitations, we believe that it is important to examine long-term oncologic data to guide further responsible investigation in this developing technique.
To our knowledge, we report the longest follow-up data of RARC/LRC for cancer. Our data suggest that minimally invasive RC provides encouraging oncologic outcomes mirroring those reported for ORC. Ongoing prospective randomized trials comparing ORC and RARC will provide further higher level evidence on this controversial topic.
Author contributions: Georges-Pascal Haber had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.
Study concept and design: Haber, Campbell.
Acquisition of data: Snow-Lisy.
Analysis and interpretation of data: Snow-Lisy, Gill, Campbell, Haber.
Drafting of the manuscript: Snow-Lisy, Haber, Campbell, Gill.
Critical revision of the manuscript for important intellectual content: Kaouk, Fergany, Gill, Campbell, Haber.
Statistical analysis: Hernandez, Snow-Lisy.
Obtaining funding: None.
Administrative, technical, or material support: Snow-Lisy.
Other (specify): None.
Financial disclosures: Georges-Pascal Haber certifies that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the manuscript (eg, employment/affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: None.
Funding/Support and role of the sponsor: None.
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a Glickman Urological and Kidney Institute, Cleveland Clinic Lerner College of Medicine, Cleveland, OH, USA
b USC Institute of Urology, Catherine and Joseph Aresty Department of Urology, Keck School of Medicine of University of Southern California, Los Angeles, CA, USA
c Department of Quantitative Health Sciences, Cleveland Clinic Lerner Research Institute, Cleveland, OH, USA
© 2013 Published by Elsevier B.V.