Robot-Assisted Radical Cystectomy and Pelvic Lymph Node Dissection: A Multi-Institutional Study from Korea

Abstract

Purpose:

To report short-term retrospective perioperative and pathologic outcomes of the first robot-assisted radical cystectomy (RARC) series in Korea.

Patients and Methods:

Between April 2007 and August 2009, 104 nonconsecutive patients, including 22 women, underwent RARC across seven institutions. We evaluated the outcomes in these cases, including operative variables, hospital recovery, pathologic outcomes, and complication rate.

Results:

The mean age of all patients was 63.6 years (range 39–82 years), and the mean body mass index was 23.6 kg/m² (range 16.0–31.8 kg/m²). Among the 104 patients, 60 had an ileal conduit and 44 had an orthotopic neobladder. The mean total operative time was 554 minutes, and the mean blood loss was 526 mL. The time to flatus and bowel movement was about 3 days, and the time until hospital discharge was about 18 days. The mean number of lymph nodes removed were 18, and 10 patients had node metastatic disease on final pathologic evaluation. Postoperative complications occurred in 28 (26.9%) patients.

Conclusions:

Our initial experience with RARC appears to be favorable with acceptable operative, pathologic, and short-term clinical outcomes. The current series suggests that RARC is becoming more prevalent, not only in Western countries, but also in Asian countries, just as robot-assisted radical prostatectomy has also gained widespread acceptance. Data from long-term, large, prospective, multicenter, ideally randomized comparative studies with open radical cystectomy are needed to confirm the outcome of the novel operation reported here.

Introduction

R adical cystectomy remains one of the most effective oncologic treatments for patients with muscle-invasive bladder cancer and for high-grade, recurrent superficial tumors. Significant morbidity, however, is associated with this procedure in 20% to 50% of patients, and urologists are exploring minimally invasive options to reduce this morbidity.^1,2

Laparoscopic radical cystectomy (LRC) has been reported for more than 500 patients, and these reports suggest that the laparoscopic approach may result in less blood loss, decreased postoperative pain, and quicker recovery, compared with open surgery.³ Many urologists, however, have either not attempted this technique or have abandoned it after intense postgraduate training because of the basic challenges of pure laparoscopic surgery, such as the reduction in the range of motion, two-dimensional vision, and impaired eye-hand coordination.⁴

Recently, with the introduction of robot-assisted radical cystectomy (RARC) in 2003, an attempt was made to facilitate the transition from open surgery to minimally invasive surgery.⁵

The feasibility of radical cystectomy with a robotic approach was shown by Menon and associates⁵ in 2003, when the authors reported on 17 patients who underwent radical cystectomy and extracorporeal reconstruction of urinary diversion. With steady growth in 2008, RARC is now superseding the use of pure LRC at centers where a robot is available and is increasingly becoming an option at major tertiary referral centers.⁶

At present, more than 350 cases of RARC have been performed worldwide, but mostly in the United States.⁶ This expansion is relatively faster than that for pure LRC and is expected to accelerate. There have been no reports in the literature from Asian countries, however, although many robot systems have already been launched in Asia. To date, Korea has launched more than 20 da Vinci robot systems since April 2007, and Korea may actually have the highest robot-launching density and prevalence in Asia.

In Korea, Park and colleagues⁷ reported the first case of RARC that involved an ileal conduit in 2008. Kang and coworkers⁸ performed the first case of RARC that involved an orthotopic neobladder in 2008 and published extended lymph node dissection (LND) results in 2009.

We examined the clinical data for more than 104 patients, including 22 women, from seven institutions that are all members of the Korean Endourological Society. In this article, we report our oncologic and short-term clinical outcomes for the 104 cases of RARC addressing bladder cancer. To the best of our knowledge, this is the first RARC series from an Asian country and involves the largest volume of data worldwide.

Patients and Methods

We retrospectively analyzed data from 104 patients, including 22 women, who underwent RARC from one of seven Korean institutions, all of which performed RARC in more than five cases of clinically localized bladder cancer between April 2007 and August 2009 (Table 1). All patients had proven invasive or recurrent high-grade urothelial carcinoma by transurethral resection of the bladder tumor and were classified by the American Joint Committee on Cancer-Union Internationale Contre le Cancer staging system.

Table 1.

The Seven Institutions Participating in This Study from the Korean Endourological Society

	Cases (N)
Institution 1	27
Institution 2	19
Institution 3	18
Institution 4	16
Institution 5	12
Institution 6	6
Institution 7	6
Total	104

All patients underwent RARC using the four-arm da Vinci S surgical system (Intuitive Surgical, Inc, Sunnyvale, CA). The camera port was placed in the midline cephalad to the umbilicus. The two 8-mm robot ports were placed 8 to 9 cm from the midline. The two assistant ports on the right were placed lateral and caudal to the right robot port.

All patients underwent a standard or extended lymphadenectomy in this study. The boundaries of a standard pelvic lymph node dissection (PLND) for bladder cancer include the lymph node of Cloquet distally, the obturator nerve posteriorly, the bladder medially, the genitofemoral nerve laterally, and the bifurcation of the iliac vessels proximally. An extended lymphadenectomy template extended to the inferior mesenteric artery as the proximal border or the bifurcation of the aorta and included the presciatic and presacral lymphatic tissue.

After the PLND was complete, the RARC was performed, and all urinary diversions were created extracorporeally. The ileal conduit was made by the Bricker method in every institution, and Studer-type or modified Hautmann orthotopic neobladder were formated via a 6- to 8-cm lower midline or suprapubic incision. Of 44 neovesicourethral anastomoses, 27 were performed robotically, necessitating redocking the system. Although the basic operation technique and port configuration were standardized, the complete standardization of surgical techniques was impossible because of the multi-institutional and retrospective design of the study.

Surgical outcome was evaluated in this series, including operative variables (total operation time and estimated blood loss [EBL]), aspects of hospital recovery (time to flatus and time to hospital discharge), pathologic outcomes (pathologic stage, margin status, occurrence of bladder entry, and number of lymph nodes [LNs] removed), and intraoperative and postoperative complication rates. In our study, complications were classified according to the modified Clavien system.⁹

Results

Baseline characteristics and perioperative data

Of the 104 patients, there were 82 men and 22 women. The mean age of all patients was 63.6 years (39–82 y), and the mean body mass index (BMI) was 23.6 kg/m² (16.0–31.8). The mean American Society of Anesthesiologists score of patients was 1.57 (1–3). None of the patients showed preoperative LN metastasis on an abdominopelvic CT scan. The clinical stages of the patients were: 34 (32.7%) with superficial cancer (T₁ and carcinoma in situ), 47 (45.2%) with muscle invasive cancer (T₂), and 23 (22.1%) in advanced stages more than T₂. Among the 104 patients, 60 had an ileal conduit, 44 had an orthotopic neobladder (Table 2).

Table 2.

Patient Characteristics

	Mean/number	Range
Number	104
Age	63.6 ± 10.3	39 – 82
Sex (M/F)	82/22
BMI	23.6 ± 3.3	16.0 – 31.8
Clinical stage
T₁ and CIS	34 (32.7%)
T₂	47 (45.2%)
≥T₃	23 (22.1%)
ASA score (1–6)	1.57 ± 0.55	1 ∼ 3
Type of PLND
Standard PLND	71 (68.3%)
Extended PLND	33 (31.7%)
Type of diversion
Ileal conduit	60 (57.7%)
Orthotopic neobladder	44 (42.3%)
- Studer	31
- Modified Hautmann	13

BMI = body mass index; CIS = carcinoma in situ; PLND = pelvic lymph node dissection; ASA = American Society of Anesthesiologists.

Table 3 presents the perioperative outcomes. The mean total operative time was 554 minutes, and the mean EBL was 526 mL. Twenty-seven (26%) patients received a blood transfusion, and their mean EBL was 710 mL. Time to flatus and bowel movement was about 3 days, and the time to hospital discharge was about 18 days (Table 3).

Table 3.

Perioperative Outcomes

Total operative time (minutes)
Mean	554	248–900
Ileal conduit	469	248–600
ONB	669	540–900
EBL (mL)
Mean	526	50–2550
Ileal conduit	525	150–2550
ONB	541	410–1000
Hospital stay (days)
Mean	18.4	8–65
Ileal conduit	15.1	8–34
ONB	24.3	13–38
Time to flatus (days)
Mean	3.4	2–8
Ileal conduit	3.5	2–8
ONB	3.2	2–5

ONB = orthotopic neobladder; EBL = estimated blood loss.

Pathologic outcomes

Pathologic stages were T₀ in 6 patients (5.7%), T₁ and CIS (carcinoma in situ) in 29 patients (27.4%), T₂ in 38 patients (35.9%), T₃ or higher in 31 patients (31.1%).

The 104 patients had transitional-cell carcinoma on pathologic examination. Of the two patients with nonurothelial-cell carcinoma, one had primary adenocarcinoma of the bladder and the other had urothelial carcinoma with small-cell carcinoma. The mean number of LNs removed was 18, with a range of 5 to 61, and 10 patients had node metastatic disease on final pathologic examination. Two cases in T₃ and three cases in final pathologic stage T₄ had positive surgical margins.

The mean postoperative follow-up period was 12 months (range 3–24 mos), and four patients died of bladder cancer postoperatively. One patient with LN metastasis died from lung metastasis of bladder cancer, and the other one died from brain metastasis. One patient died of sepsis from vesicovaginal fistula, and the fourth patient died from acute renal failure and sepsis. The overall survival rate was 96.2% (100 of 104 patients), and the disease-specific survival rate was 96.2% (100 of 104 patients) (Table 4).

Table 4.

Pathologic Outcomes

	Mean/number	range
Pathologic stage
T₀	6 (5.8%)
T₁ and CIS	29 (27.9%)
T_2a	22 (21.2%)
T_2b	16 (15.4%)
≥T₃	31 (29.8%)
Pathology
TCC	102
Adenocarcinoma	1
Small-cell carcinoma	1
Positive surgical margin	5 (4.8%)
Retrieved number of LNs	18.4 ± 11.9	5–61
Standard PLND	15.7 ± 10.5	5–50
Extended PLND	24.7 ± 12.5	8–61
Number of patients with LNs (+)	10 (9.6%)
Mean follow-up (months)	12	3–24
Disease-free survival	100/104 (96.2%)

CIS = carcinoma in situ; TCC = transitional-cell carcinoma; PLND = pelvic lymph node dissection; LN = lymph node.

RARC in women

Among the 22 patients, 13 had an ileal conduit, and 9 had an orthotopic neobladder. The mean age was 66.1 years, the median operative time was 567 minutes, and the median EBL was 591 mL. The median length of stay was 20 days. The median number of LNs removed was 16, with four patients revealing node-positive disease. Surgical margins were negative for disease in all patients, and there were no significant differences between male and female patients (Table 5).

Table 5.

Comparison Between Female and Male Patients

	Female	Male	P value
Number	22	82
Age	66.1	62.9	0.221
BMI	23.0	23.7	0.383
Total operative time (min)	567	550	0.644
PLND time (min)	67	79	0.198
UD time (min)	130	140	0.409
EBL (mL)	591	515	0.320
Hospital stay (day)	20	17.7	0.186
Time to flatus (day)	3.5	3.4	0.378
Retrieved number of LNs	16.0	19.1	0.318
Mean follow-up (months)	11.7	12.5	0.517

BMI = body mass index; PLND = pelvic lymph node dissection; UD = urinary diversion; EBL = estimated blood loss.

Intraoperative and postoperative complications

Table 6 presents the intraoperative and postoperative complications. Three patients were converted to open surgery because one had an external iliac vein injury and two had severe adhesion, but there was no rectal injury. Postoperative complications were classified according to an established five-grade modification of the original Clavien system.^10,11 Postoperative complications occurred in 28 (26.9%) patients. Major complications occurred in 8 (7.7%) patients, and minor complications occurred in 20 (19.2%) patients.

Table 6.

Intraoperative and Postoperative Complications

Complication	Number	Management	Modified Clavien grade ^a
Intraoperative
Open conversion	3
Major vascular injury	1
Rectal/adjacent organ injury	0
Total	4 (3.8%)
Postoperative
Mechanical ileus	1	Reexploration	3
Arteriosclerosis obliterans	1	Vascular stenting	3
Ureterointestinal leak	1	PCN	3
Ureterointestinal stricture	1	Revision	3
Ureterointestinal stricture	2	PCN	3
Urethroneovesical anastomosis leakage	2	Catheter indwelling	1
Deep vein thrombosis	1	Antithrombolytic agent	2
Acute renal failure	6	Conservative treatment	1
Paralytic ileus (>5 days)	5	Conservative treatment	1
Others (delirium, APN, etc)	6	Medical treatment	1
Death	2		5
Total	28 (26.9%)
Major grade	6 (7.7%)

Grade 1: Oral medication or bedside intervention.

Grade 2: Intravenous medications, total parenteral nutrition, enteral nutrition, or blood transfusion.

Grade 3: Interventional radiology, therapeutic endoscopy, intubation, angiography, or operation.

Grade 4: Residual plus lasting disability necessitating major rehabilitation or organ resection.

Grade 5: Death.

Minor: Grade 1–2.

Major: Grade 3–5.

PCN = percutaneous nephrostomy; APN = acute pyelonephritis.

One patient had a postoperative mechanical bowel obstruction that necessitated reexploration via the previous small lower midline incision and surgical reduction. One case of arteriosclerosis obliterans developed and was managed by vascular stent placement. A ureteroileal stricture developed in three patients with an ileal conduit, with two patients needing a Double-J insertion and a percutaneous nephrostomy insertion and the other patient undergoing a revision of the ureteroileal anastomosis site.

In addition to these complications, one patient had pleural effusion, and two patients had paralytic ileus managed by conservative treatment, respectively. Acute renal failure developed in six patients, three with an ileal conduit and three with a neobladder, respectively; it was managed supportive conservative treatment. A urethrovesical anastomosis leak developed in two patients with a neobladder; it was successfully managed by prolonged catheter indwelling. One case of deep vein thrombosis was managed with anticoagulant treatment. Further complications, including delirium, acute pyelonephritis, and epididymitis, were managed with medical treatment.

Discussion

Radical cystectomy is the standard surgical procedure for muscle-invasive bladder cancer, but this formidable operation is associated with significant complications, even in expert hands.¹² There have been major advances in the use of laparoscopy in the field of urology, and LRC has been reported in more than 500 patients.¹³ LRC in the management of bladder cancer, however, has not been performed worldwide, because it is more technically challenging than conventional open cystectomy and requires a protracted learning curve.

The use of robot-assisted surgery in urology has rapidly evolved over the last 5 years, and the robot-assisted laparoscopic approach to radical prostatectomy has gained significant popularity not only in Western countries, but also in Asian countries. Similar to its application in prostate cancer, it is expected that RARC will be one of the novel options for managing bladder cancer. RARC, however, is currently restricted to the domain of a few centers worldwide because of the high level of surgical complexity in performing this procedure and high cost.⁶

To validate RARC as an appropriate surgical and oncologic option for patients with bladder cancer, larger experiences and a larger volume of data are necessary to adequately evaluate its use. The current literature includes a total of 104 patients who have undergone robot-assisted cystectomy procedures, including 22 women.

With regard to perioperative outcomes, our mean operative time was 554 min. The mean operative times of other robot-assisted series are 442 minutes reported by Guru and associates.¹⁴ 366 minutes by Pruthi and Wallen,¹⁵ 390 minutes by Wang and colleagues,¹⁶ and 638 minutes by Rhee and coworkers¹⁷ Although we limited our analysis to institutions in which more than five cases of RARC had been performed, most of the institutions are still in the early stage of the learning curve. Thus, our mean operative time was not disappointing in comparison with that of other reports. In addition, for the most recent 5 of 27 cases performed at institution 1, the operative time was reduced to about 7 hours. This reduction in operative time clearly reflects experience gained using the techniques and steps of the operation. We expect our operative times to continue to decrease, and we will potentially have improved results to report in the near future.

The mean EBL and average hospital stay in our series was 526 mL and 18 days, respectively. Rhee and associates¹⁷ reported 479 mL and 11 days, Wang and coworkers¹⁶ reported 400 mL and 5 days, and Murphy and colleagues³ reported 278 mL and 11.6 days. The mean EBL in our series was acceptable, but the average hospital stay was relatively longer than that in other reports. Specifically, because of the differences in economic health systems and cultural backgrounds, Korean patients often stay in the hospital until patients want to be discharged, while patients in the United States are usually discharged very quickly if the early postoperative course is uneventful.¹⁸

In addition, time to flatus in our series was 3.4 days, and this is longer than that in the previously reported RARC series.^3,19 Although we limited our analysis to institutions in which more than five cases of RARC had been performed, most of the institutions are still in the early stage of the learning curve. The relatively longer operative time and larger EBL may affect the time to flatus.

In our experience, the oncologic principles and pathologic outcomes appear to be maintained with a robot-assisted approach. There were no cases of an inadvertent bladder injury or positive surgical margin in localized bladder cancer. Although a positive margin was observed in three cases, all were pathologic T₃ and T₄ stage in the final pathology reports.

PLND is a crucial part of RARC in the management of bladder cancer, which has both prognostic and potentially therapeutic importance. Although there is still controversy regarding the boundary of lymphadenectomy, it is expected that extended pelvic lymphadenectomy gives potential survival benefits and excellent tumor control. Herr and associates²⁰ suggest that more than 14 lymph nodes should be retrieved in patients who are undergoing open radical cystectomy (ORC) to obtain better oncologic outcomes. Current data, however, on lymph node yield and oncologic outcome in minimally invasive robot-assisted cystectomy series are limited.^3,19,21,22

The learning curve independent of the surgical method used should not be underestimated regarding lymph node yield. In our series, one major vascular injury happened during treatment of an early second patient in one center, so the case was ultimately converted to open cystectomy. In this study, extended LND was performed in 33 cases, and a mean of 24.7 (range 8–61) lymph nodes was retrieved with the robot-assisted approach. A mean LN count of 15.7 was retrieved with standard LND. Similarly, Pruthi and Wallen¹⁹ performed an extended LND and reported a median node yield of 28 nodes (range 12–39), and Guru and colleagues²¹ reported a median node yield of 23 nodes (range 10–39).

Extended robot-assisted LND has been shown to be technically feasible with intraoperative morbidity similar to that of an open series. We recommend, however, that in one's early experience, dissection around major vessels should be undertaken carefully in extended LND to minimize the technical difficulty for the surgeon and to reduce the potential morbidity to the patient.

The postoperative complication rate in this study was 26.9%, with complications occurring in 28 patients, serving to remind us that radical cystectomy by any approach remains a formidable procedure. Although it was discouraging in terms of the three open conversion cases, the complication rate was comparable, with 26% reported by Murphy and associates³ and 30% reported by Pruthi and Wallen.²³

The potential limitations of this study should be considered. The major limitation was the nonrandomized and retrospective multi-institutional nature of the study design. The study comes from seven different institutions with different types of diversions: 60 ileal conduit and 44 orthotopic neobladder. Moreover, the neovesicourethral anastomoses are performed in different techniques; of 44 neovesicourethral anastomoses, 27 were performed robotically and 17 were open procedures. Overall, these differences may affect the operative and postoperative parameters. Although the basic operative technique and port configuration were standardized, the complete standardization of surgical techniques was impossible because of the multi-institutional and retrospective design of the study.

Another potential limitation is that the median follow-up period of this study was short for the evaluation of long-term oncologic outcomes of RARC for bladder cancer. Therefore, we are planning to perform a randomized controlled study with comparison with open cystectomy in the future. Some bias might occur with regard to patient selection for the robotic approach. In our early experience, we tended to choose patients with low-volume, nonbulky tumors. Indeed, the pathologic outcomes of the robotic series showed that nearly 70.2% of patients had pathologically localized tumors. This is compared with the open experience of Stein and coworkers²⁴ in which only 56% of patients had pathologically localized tumors.

Nevertheless, there are several important points to consider in regard to the current series. First, this is the first case series from an Asian country. Second, this is the largest volume data including 22 female patients that still need to be added to the otherwise limited small case series and anecdotal reports that currently exist in the literature. The current series does suggest that RARC is becoming more prevalent outside Western countries and could replace ORC, just as robot-assisted radical prostatectomy is gaining widespread acceptance, with about 60% of prostatectomies performed via robot in the United States.⁶

Conclusion

RARC with PLND was safely performed at multiple institutions during the initial experience. Data on long-term, large, prospective, multicenter, ideally randomized, comparative studies with ORC are still needed to clarify this novel operation. Different from that LRC is just performed about 500 cases so far in the United States and globally, the current series demonstrates that RARC is becoming more prevalent.

Footnotes

Acknowledgments

This research was supported by the Korean Endourological Society.

Disclosure Statement

No competing financial interests exist.

Abbreviations Used

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