Robotic Versus Open Radical Cystectomy: Prospective Comparison of Perioperative and Pathologic Outcomes in Japan

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1 Jpn J Clin Oncol 2012;42(7) doi: /jjco/hys062 Advance Access Publication 11 May 2012 Robotic Versus Open Radical Cystectomy: Prospective Comparison of Perioperative and Pathologic Outcomes in Japan Tatsuo Gondo *, Kunihiko Yoshioka, Yoshihiro Nakagami, Hidenori Okubo, Takeshi Hashimoto, Naoya Satake, Choichiro Ozu, Yutaka Horiguchi, Kazunori Namiki and Masaaki Tachibana Department of Urology, Tokyo Medical University, Tokyo, Japan *For reprints and all correspondence: Tatsuo Gondo, Department of Urology, Nishi-shinjuku, Shinjuku-ku, Tokyo , Japan. gonta@tokyo-med.ac.jp Received December 23, 2011; accepted April 4, 2012 Objective: In Japan, no study has compared the perioperative outcomes observed between robot-assisted radical cystectomy (RARC) and open radical cystectomy (ORC). This study aimed at a prospective comparison of the perioperative outcomes between RARC and ORC performed by a single surgeon. Methods: Between 2008 and 2011, 26 bladder cancer patients underwent radical cystectomy by one surgeon, 11 robotically and 15 by open procedure. We prospectively collected perioperative and pathological data for these 26 patients, and retrospectively compared these two different surgical procedures. Results: The RARC cohort had a significant decrease in both estimated blood loss (656.9 vs ml, P ¼ ) and allogeneic transfusion requirement (0 vs. 40%, P ¼ ). The total operative time was almost the same (P ¼ ) but increased duration of bladder removal and lymphadenectomy was observed in the RARC cohort (P ¼ ). Surgeryrelated complication rates within 30 days were not significantly different (P ¼ ). Positive surgical margin was observed in three patients in the ORC cohort and in one patient in the RARC cohort (P ¼ ). The RARC cohort had a larger number of removed lymph nodes than the ORC cohort, and the difference was statistically significant (20.7 vs. 13.8, P ¼ ). Conclusions: We confirmed that RARC is safe and yields acceptable outcomes in comparison with ORC for the treatment of bladder cancer if it is performed by a surgeon who has experience of over 60 cases of robot-assisted radical prostatectomy. It is hoped that RARC will gain acceptance in Japan as a minimally invasive surgery for muscle-invasive bladder cancer. Key words: bladder cancer radical cystectomy robot-assisted radical cystectomy perioperative outcome INTRODUCTION Radical cystectomy (RC) remains the gold standard treatment for patients with muscle-invasive bladder cancer and for those with high-risk recurrent non-muscle-invasive disease (1). Since Stein et al. (2) reported the usefulness of RC in the aspect of its safety and cancer control by large RC series, RC has been recognized as a stabilized procedure if it is performed by a skilled surgeon. However, RC has evolved into a more invasive procedure by the requirement of goodquality lymph node dissection in recent studies (3,4), in addition to conventional need of using the alimentary tract for urinary diversion. Indeed, the complication rates of RC have not necessarily been low (2,5), and RC may still have many concerns to be addressed such as the disadvantage of more # The Author Published by Oxford University Press. All rights reserved. For Permissions, please journals.permissions@oup.com

2 626 Outcomes of robot-assisted radical cystectomy chance of blood transfusion by massive intraoperative bleeding, postoperative pain due to longer skin incision, postoperative ileus caused by excessive handling of intestinal tract and furthermore, prolonged admitted periods due to delay in the recovery of physical condition. The excellent perioperative and long-term results provided by laparoscopic surgery for kidney and prostate cancer have encouraged several urologists to explore the role of laparoscopy in RC. Through different types of urinary diversion, the feasibility and safety of laparoscopic RC (LRC) has been demonstrated by several urologists (6 8). However, LRC is associated with prolonged operative time and the real advantage of LRC over open RC (ORC) is not yet known because the data on comparison of LRC with ORC on a prospective basis are not sufficient only two comparative studies published to date (9,10). Robot-assisted surgery is an innovative procedure, especially in Japan, and its multifunctional ability is used to overcome the disadvantage of laparoscopic surgery. In the field of urology, robot-assisted surgery has spread explosively since robot-assisted radical prostatectomy (RARP) was approved by the Food and Drug Administration (FDA) in With forceps and 3D vision with better perspectives, DaVinci w surgical system (Intuitive Surgical Inc, Sunnyvale, CA, USA) enabled physicians to overcome the technical difficulties of laparoscopic radical prostatectomy (LRP). As a result, it contributed to reduction of the learning curve of LRP, and changed the MIS to a user-friendly approach. It seems natural that urologists skilled in RARP attempted to apply this favorable approach to RC as the next step. Several recent studies have reported favorable perioperative outcomes, safety and short learning curve associated with RARC (11 16). However, in Japan no study has compared the perioperative outcomes between RARC and ORC. We introduced the DaVinci w surgical system to our institution in 2006 and one surgeon having experience of over 60 cases of RARP started RARC in In this paper the results of our prospective comparison of RARC and ORC with regard to perioperative and pathologic outcomes are presented. PATIENTS AND METHODS PATIENT SELECTION From April 2008 to May 2011, 82 cases of RCs were performed at Tokyo Medical University Hospital. Bladder cancer was histologically confirmed by transurethral resection of bladder tumor in each patient. The indications for RC included muscle-invasive tumors without evidence of distant metastasis (clinical T [ct] 2 4, NX, M0), recurrent multifocal superficial disease refractory to repeat transurethral resection with intravesical therapy or Bacille Calmette-Guerin resistant carcinoma in situ (CIS). The ct stage of a bladder tumor was determined according to the 2002 UICC TNM classification of bladder tumors. Of the 82 RC cases, 26 underwent the procedure by a single surgeon having experience of over 60 cases of RARP at the beginning of this study. Of the 26, 11 underwent the robotic approach and 15 the open technique. None of the 26 patients had received neoadjuvant chemotherapy or radiation therapy prior to cystectomy. The decision on the surgical approach performed for each patient was not randomized. Most data were collected prospectively and fed into our bladder cancer database, supplemented by retrospective information to fill gaps in the medical records. This study was approved by the ethics committee at Tokyo Medical University. SURGICAL TECHNIQUE All the patients underwent RARC with extracorporial urinary diversion. A meticulous standard lymph node dissection was done on all the patients during RC; however, one patient in the RARC cohort and two in the ORC cohort had only limited lymph nodes dissection because of severe adhesion around vessels. ORC was performed through a periumbilical midline incision in the traditional manner (17,18). RARC was performed by surgical procedure that Menon et al. (19) previously reported with a few minor modifications. Briefly, we used a six-port technique (four for robotics and two for assistant). Pneumoperitoneum was achieved using a Veress needle above the umbilicus and a 12-mm trocar was used for the camera. Two 8-mm robotic ports were placed 8 cm inferior and lateral to the camera port in line with the anterior superior iliac spine. A 12-mm assistant port was placed 8 cm superior and lateral to the left-sided robotic port. A 5-mm suction port was placed in between the camera and the left-sided robotic port. The patients were then placed in steep Trendelenburg (308) position. The colon was mobilized medially to allow for identification of the ureters. The ureters were dissected proximally and distally to the level of the bladder and divided using Hem-o-lok w clips (Weck Closure System, Research Triangle Park, NC, USA). A frozen section analysis for the ureteral margins was performed to confirm the presence of cancer. The bladder was subsequently mobilized off the anterior abdominal wall by dividing the medial umbilical ligaments and urachus. The posterior plane was developed distally beneath the posterior layer of Denonvilliers fascia to allow mobilization of the bladder and the base of the prostate from the rectum. Both the vasa deferentia were then transected distally. The lateral plane between the bladder and the pelvic sidewall was then developed using blunt dissection. The lateral dissection was performed with exposure and incision of the endopelvic fascia. Pelvic lymphadenectomy was performed by including all the tissue between the external iliac vessels anteriorly, the pelvic sidewall including the node of Cloquet distally, the upper common iliac artery proximally, the obturator nerve posteriorly and the genitofemoral nerve laterally. The bladder pedicles were exposed and controlled using a shield device and Hem-o-lok clips as necessary. The prostate

3 Jpn J Clin Oncol 2012;42(7) 627 pedicles were then controlled with Hem-o-lok clips and divided sharply as described previously (19). The anterior surface of the prostate was exposed, and the dorsal vein complex (DVC) was controlled and divided. When the neobladder was chosen for urinary diversion, the urethra was then divided sharply. For non-nerve-sparing (NS) procedures, the lateral prostatic attachments and prostate pedicles were divided with clips and electrocautery. In NS procedures, release of the neurovascular bundles begins at the tip of the seminal vesicles. When the ileal conduit was chosen for urinary diversion, the robot was undocked and the Trendelenburg position was restored. Then urethrectomy was started using the perineal approach and the bladder and the prostate were simultaneously removed through a lower abdominal incision of 5 7 cm. Finally the bladder, prostate and ureter are removed together, and we started to make ileal conduit extracorporeally. When the neobladder is chosen for urinary diversion, we sutured the proximal part of the resected urethra by 2 0 vicryl before the transection between urethra and prostate. Then the robot is undocked and the Trendelenburg position was restored, and we started making the neobladder. In women, an anterior pelvic exenteration was performed. Briefly, once the ureters were clipped and divided, the uterus was pulled upward by the robotic grasper. The infundibulopelvic ligaments were then clipped and transected. With the adnexa retracted anteriorly, the peritoneum over the apex of the posterior fornix was scored transversely using electrocautery. The cervical cup aids in identifying the posterior fornix. The remaining posterior dissection and vaginal incision were made after DVC preparation. The lateral pedicles were transected after clips were applied, and the bladder was dropped in the usual fashion. The DVC was suture ligated with a 2-0 polyglactin suture on a CT-1 needle. Thereafter, the posterior dissection was focused upon. The transverse incision of the posterior vaginal fornix was completed at the previously scored site. The vaginal incision was then extended distally on either side of the urethra, excising a narrow central strip of vagina en bloc with the bladder specimen. Using a perineal approach, the external meatus and distal urethra were circumferentially cored out by electrocautery. The distal urethra and the underlying strip of the anterior vaginal wall were dissected free using the transvaginal approach. The specimen was delivered en bloc through the vagina. The vagina was reconstructed by combined perineal suturing before urinary diversion was performed. ANALYZED DATA The analyzed perioperative data were patient demographics, preoperative disease characteristics, total operative time, time of bladder removal and lymphadenectomy, estimated blood loss (EBL), allogeneic transfusion requirement, time to regular diet, time of hospital stay, intraoperative complication rates, postoperative complication rates within 30 days and postoperative pathological features [ pathological T ( pt), lymph node metastasis, removed lymph node yield and positive surgical margin (PSM)]. Patient comorbidity was assessed preoperatively using Charlson comorbidity index (20). Surgery-related complications were classified using Clavien classification as reported previously (21). STATISTICAL ANALYSIS Two-sided comparison for several variables between the RARC cohort and the ORC cohort was performed using Fisher s extract test and Mann Whitney s U-test. Statistical analyses were performed using StatView (ver. 5.0; SAS, Cary, NC). P values, 0.05 were considered statistically significant. RESULTS Patient demographics are shown in Table 1. There was no significant difference in age, body mass index and history of previous abdominal surgery between the two groups. There was a trend to choose more organ-confined disease (ct2) in the RARC cohort (90.9 vs. 66.7%), which were suggested in previous report (22), but the difference was not significant (P ¼ ). Perioperative data are shown in Table 2. The median total operative time was 45 min greater in the RARC cohort but was not significantly different between the two groups (P ¼ ). In addition, when we examine the time of bladder removal and lymphadenectomy, the robotic approach had significantly longer operative duration compared with the open approach (P ¼ ). Both the mean EBL and allogeneic transfusion requirement were significantly decreased in the RARC cohort compared with the ORC cohort (P ¼ and , respectively). There was no difference in time to resumption of a regular diet between the two groups (P ¼ ). The intraoperative complication occurred only in one patient in the RARC cohort. This complication was the injury of transverse colon caused when assistant forceps were inserted and successfully repaired robotically. Surgery-related complication rates within 30 days were not significantly different between the two groups (54.5% in RARC vs. 73.3% in ORC, P ¼ ). Minor complications in both the groups were prolonged ileus and wound infection that resolved with conservative management. Pyelonephritis due to urinary diversion was the most common Clavien II complication in both the groups which required pharmacological treatment. One patient in the ORC cohort had Clavien III complication that represented the leakage from ureterointestinal anastomosis, and radiological intervention without general anesthesia was performed. The median follow-up periods were 17.8 month (mean; ). No patient died of cancer in RARC cohort and two patients in ORC cohort died of cancer during this period.

4 628 Outcomes of robot-assisted radical cystectomy Table 1. Patient characteristics Characteristics RARC (n ¼ 11) ORC (n ¼ 15) P value significant extravesical disease and one patient in the RARC cohort had pt4 disease. Age (years) Mean (median) (70) (73) Range Gender (n) Male 9 13 Female 2 2 Body mass index (kg/m 2 ) Mean Range Previous abdominal surgery Yes 1 3 No Charlson comorbidity index (n) Clinical T stage (n) ct1 6 3 ct2 4 7 ct3 1 3 ct4 0 2 ct1 vs. ct2 6 vs. 5 3 vs ct2 vs. ct3 10 vs vs NS procedure.0.99 Yes 2 2 No 9 13 Diversion type (n) Ileal conduit 7 9 Ileal neobladder 4 6 RARC, robot-assisted radical cystectomy; ORC, open radical cystectomy; ct, clinical T; NS, nerve sparing. Pathological data are shown in Table 3. When patients were grouped into organ-confined ( pt2) and extravesical ( pt3) disease, there were more patients with extravesical disease in the ORC cohort (46.7 vs. 9.1%, P ¼ ). The rates of positive lymph nodes were not different between the groups (P ¼ ). The difference in the mean number of lymph nodes removed in the ORC vs. RARC cohorts was significant (13.8 vs. 20.7, P ¼ ). A higher percentage of patients in the ORC cohort had PSMs but this was not statistically significant (20 vs. 10%, P ¼ ). The three patients with PSM in the ORC cohort were all pt3b with DISCUSSION ORC has been and continues to be the standard of care for bladder cancer. However, it is associated with significant morbidity even when performed by experienced surgeons, in part due to the long incision, prolonged abdominal wall retraction, prolonged exposure of the peritoneal surface with major fluid shifts and poor visibility, particularly in the depth of the pelvis and retrovesical area (23). In an attempt to decrease the morbidity of open surgery, urologists have adopted laparoscopic and robotic minimally invasive approaches to treat urological malignancies (24,25). During , several investigators have shown the feasible perioperative results of laparoscopic and robotic surgeries for bladder cancer patients (26 30). The techniques that have been described appear to duplicate the surgical principles of ORC with regard to the extirpative portion of the procedure and the ability to perform adequate lymphadenectomy (28 31). The surgical and perioperative outcomes of these reports, even early in the procedural experience, appeared to be comparable to those of the open experience (15,30). The potential advantages of the laparoscopic and robotic approaches that have been described include lower intraoperative blood loss, early return of bowel function and more rapid postoperative convalescence (15,26 30). Lowrance et al. (32) described in their report published in 2008 that for 553 patients who underwent ORC, the mean EBL was 750 ml and 38% of patients required transfusion. They also mentioned that the incidence of complication such as postoperative ileus was significantly high in patients who required blood transfusion because of massive bleeding compared with those without transfusion. On the other hand, most of the previous reports that examine the usefulness of RARC suggested its benefits of the minimal intraoperative hemorrhage, which would lower the incidence of postoperative complications. Hayn et al. (11) reported in their collaborated study that the mean EBL was 408 ml and the transfusion rates were 17% in 496 patients who underwent RARC at a total of 14 institutions. Wang et al. (15) reported in their prospective study that compared the outcomes between RARC and ORC that there was no significant difference in postoperative complication rates between the two groups (21 vs. 24%); however, they did not examine complications, using Clavien classification. Ng et al. (13) prospectively recorded the complications by Clavien classification and revealed that the complication rate at 30 days in RARC series was significantly lower compared with those in ORC series (41 vs. 59%, P ¼ 0.04). In this study, EBL and transfusion rate were significantly low in RARC series, as suggested by previous reports. The difference in complication rates between the two groups was not significant (P ¼ ); however, the postoperative ileus and wound

5 Jpn J Clin Oncol 2012;42(7) 629 Table 2. Perioperative outcomes of the 11 robotic cohort and 15 open cohort RARC (n ¼ 11) ORC (n ¼ 15) P value Mean estimated blood loss, ml (median) (548) (1465) Mean operative time, min (median) (418) (364) Time of bladder removal and lymphadenectomy, min (median) (142) (112) Intraoperative allogeneic transfusion, n (%) 0 (0) 6 (40.0) Time to resumption of a regular diet, days (median) 5.6 (5.0) 6.3 (6.0) Time of hospital stay, days (median) 40.2 (39) 37.0 (35.0) Incidence of intraoperative complication, n (%) 1 (9.1) 0 (0) Incidence of complication within 30 days, n (%) 6 (54.5) 11 (73.3) Clavien Grade I 2 6 Clavien Grade II 4 4 Clavien Grade IIIa 0 1 Clavien Grade IIIb 0 0 RARC, robot-assisted radical cystectomy; ORC, open radical cystectomy. infection tended to occur more frequently in ORC cohorts compared with RARC cohorts (20 vs. 9.1% and 33.3 vs. 9.1%, respectively). On the other hand, in this study, the time of bladder removal and lymphadenectomy in the RARC cohorts was significantly longer than that in the ORC cohorts. We could not clearly explain the difference in the operative time between the two groups. Some of the surgical procedures including the NS in the RARC procedure may affect the prolonged time of bladder removal and lymphadenectomy, in comparison with the ORC cohorts. However, the difference in the time of bladder removal and lymphadenectomy between the NS group and the non-ns group was almost the same (156.5 min for NS group (n ¼ 2) vs min for the non-ns group (n ¼ 9), P ¼ ) in the RARC cohorts. These results suggest that factors other than the NS procedure may prolong operative time, especially in RARC cohorts. The ability to perform an adequate lymphadenectomy remains an important part in RC. Herr et al. (3) reported in 2002 that a lymph node count of at least nine during RC is essential to evaluate the presence of lymph node metastases and this lymph node count contributed to improve the survival of bladder cancer patients. They also reported in 2004 that the standard number of retrieved lymph nodes was (4). Kauffman et al. (12) reportedintheir85rarc cases that the mean retrieved lymph node count was Furthermore, Hayn et al. (11) reported a mean retrieved lymph node count of 18 and a learning curve for resection of over 20 lymph nodes of 30 cases in a study of 496 RARC cases at 14 institutions. These results suggest that the RARC is favorable in the quality of lymph node dissection compared with the open approach. Our experience indicated that a standard lymphadenectomy can be performed robotically, and our mean lymph node count of 20.6 compares favorably Table 3. Pathologic outcomes of the 11 robotic cohort and 15 open cohort RARC (n ¼ 11) ORC (n ¼ 15) P value Pathologic stage (n) ptis, pta 2 0 pt1 5 1 pt2 3 7 pt3 0 7 pt4 1 0 Organ confined ( pt2) vs. 10 vs. 1 8 vs extravesical ( pt3) Lymph node metastasis (n) Negative Positive 1 2 Mean lymph node yield (range) 20.7 (632) 13.8 (527) Surgical margin (n) Negative Positive 1 3 RARC, robot-assisted radical cystectomy; ORC, open radical cystectomy; pt, pathological T. with our open experience (mean lymph node count of 14.1). We cannot definitively conclude that the LN dissection ability is superior in the RARC procedure compared with the open procedure because the sample size in our study was relatively small. Earlier studies suggested that the LN yield was equal between ORC and RARC cohorts (15,33), and the ability to remove more lymph nodes seems to be the same between these two procedures. One of possible explanations

6 630 Outcomes of robot-assisted radical cystectomy for our result is an error occurring because of a small sample size and/or individual differences in the condition of operative field (degree of adhesion, etc.). Another possible explanation is that meticulous dissection due to 3D vision with better perspectives and decreased blood loss due to pneumoperitoneum might give the surgeon the advantage of acquiring higher LN yield in the RARC cohort. A further study with a larger sample size is necessary to elucidate the difference in LN dissection ability between the two procedures. Herr et al. (4) described that in their 1091 ORC series the accepted PSM rates of this surgery were fewer than 10% of all cases,,15% for bulky (pt3 4) tumors and,20% of salvage cystectomies after prior treatment. Recent studies that reported the oncologic results of RARC revealed that the PSM rates varied from 0 to 13% (13,15,34 36). These rates seem acceptable; however, the limitation of these results is selection bias occurred due to its early aspect of RARC series. Indeed, the incidence of extravesical disease ( pt3) in RARC series (12 15,37) was lower compared with those in contemporary ORC series (2,4,32,38) (22 38% in RALC vs % in ORC). These selection bias in early RARC series has made it difficult to evaluate its real impact on pathological outcomes (22). Furthermore, a study by the International Robotic Cystectomy Consortium showed that the surgical margin (SM) status for RARC with extravesical disease ( pt3) was 16.6% (37), whereas the SM status for the ORC series reported by a recent large multicenter study with 4410 patients was 12.4% (39). Thus, currently, RARC cannot yield equivalent oncological outcomes, especially with regard to the SM status of extravesical disease. This study has several limitations. We could not evaluate long-term oncologic control outcomes, and the sample was relatively small compared with that in the previous reports of RARC in high-volume robotic centers. However, in Japan, the morbidity rate of bladder cancer is not high and it is difficulttoperformover20casesofrcperyearevenina high-volume cancer center. Recently, Hayn et al. (40) reported that previous RARP experience might affect the perioperative outcomes of RARC. This study suggests that RARC can be successfully performed for the first time by a surgeon who has performed over 60 cases of RARP. We believe that our results have laid the foundation for future larger randomized studies in Japan. CONCLUSIONS We confirmed that RARC is safe and yields acceptable outcomes in the treatment of bladder cancer if it is performed by a surgeon who has experience of over 60 cases of RARP. 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