Robot-Assisted Radical Cystectomy with Total Intracorporeal Urinary Diversion: Comparative Analysis with Extracorporeal Urinary Diversion

Abstract

Purpose:

To compare the perioperative outcomes, postoperative complications, and early oncologic outcomes of intracorporeal urinary diversion (ICUD) with those of extracorporeal urinary diversion (ECUD) following robot-assisted radical cystectomy (RARC) performed by a single surgeon at a tertiary referral hospital.

Materials and Methods:

We reviewed a prospectively maintained, institutional review board–approved database of 70 patients treated with RARC and pelvic lymph node (LN) dissection for bladder cancer performed from 2007 through 2014. Data were collected for 64 patients who underwent either ICUD or ECUD.

Results:

Thirty-eight patients underwent ECUD, and the remaining 26 underwent ICUD. Urinary diversion was performed extracorporeally in the first 37 cases and performed intracorporeally thereafter. There were no significant differences in patient characteristics between the ECUD and ICUD groups. Mean total operative time was 468 minutes for ECUD and 581 minutes for ICUD (P < .05). Mean estimated blood loss was 265 and 148 mL, respectively (P < .05). Minor and total complication rates for patients with the ECUD were higher than in patients with the ICUD (minor: 47.4% vs. 15.4%; total: 57.9% vs. 30.8%; P < .05). All patients showed negative surgical margin, while 21% in the ECUD group and 26.9% in the ICUD group had pathologic stage T3 or T4 (P > .05). The mean LN yield was 23.2 and 31.8, respectively (P < .05).

Conclusions:

From our experience, the results show that ICUD after RARC can be successful, with the benefits of decreased blood loss and lower transfusion and complication rates than ECUD. A larger series and long-term follow-up data will be necessary to support our results.

Introduction

Radical cystectomy is the standard treatment for muscle-invasive bladder cancer as well as recurrent high-risk tumors; however, it is a technically complex and challenging procedure associated with significant perioperative morbidity and postoperative complications. Within urology, minimally invasive surgery has been encouraged as a replacement for many open procedures to decrease the morbidity of each operation. The wide acceptance of robot-assisted radical prostatectomy in the past decade has naturally resulted in a growing interest in applying these skills to bladder cancer.¹ Accordingly, robot-assisted radical cystectomy (RARC) has recently emerged as a minimally invasive alternative to open radical cystectomy (ORC), with the goal of reducing procedure-related morbidity. RARC has already superseded the use of pure laparoscopic radical cystectomy and is increasingly becoming an available option at major tertiary care centers.²

Cumulative analyses have demonstrated that lymph node (LN) yields and positive surgical margin (PSM) rates serve as oncologic surrogate markers, and oncologic outcomes of ≤5 years have been shown to be similar between RARC and ORC, although long-term survival outcomes for RARC are limited.³ RARC may provide several advantages over ORC in terms of estimated blood loss (EBL), transfusion rates, and postoperative complication rates.⁴ Nonetheless, the complication rate remained high in a series report on RARC, and Bochner et al.⁵ reported similar complication rates between RARC and ORC in prospective randomized trial results. However, most RARC case reports used extracorporeal urinary diversion (ECUD), a simpler and faster procedure than intracorporeal urinary diversion (ICUD). ICUD is currently performed in very few centers, and use in the United States remains low, accounting for roughly 3% of RARCs.⁶ As surgical experience increases and ergonomics improves, which has become the latest trend, primarily due to potential benefits that include decreased fluid loss from evaporation, reduced body cooling, reduced EBL, less pain, a smaller incision, and a faster return to bowel function.⁷ However, at the present, only a limited number of studies have reported the benefits of ICUD when compared with ECUD.

Therefore, we attempted to analyze the perioperative outcomes, postoperative complications, and oncologic outcomes of ICUD and ECUD following RARC performed by a single surgeon at a tertiary referral hospital.

Materials and Methods

Study design

We reviewed a prospectively maintained institutional review board-approved database of 70 patients treated with RARC and pelvic lymph node dissection (PLND) for bladder cancer, all performed by a single surgeon (S.H. Kang) at the Korea University Medical Center from 2007 through 2014. Among them, there was a consecutive series of 26 patients who underwent RARC and total ICUD from 2011.

Ultimately, 64 patients who received either an orthotopic neobladder or an ileal conduit were retrospectively analyzed in this study. One patient who underwent conversion to open radical cystectomy due to a severe adhesion was excluded from this analysis, as were 5 patients who underwent ureterocutaneous diversion. Among these 5 patients, 2 had a single kidney, and the remaining 3 underwent concomitant nephroureterectomy, as there was either an accompanying ureteral tumor or positive ureteral frozen pathology found during the operation.

Comparisons were made according to patient demographics (age, sex, body mass index [BMI], Charlson comorbidity index [CCI] score, history of neoadjuvant chemotherapy, and pelvic radiotherapy or surgery), perioperative data (mean operative time, mean console time, EBL, length of stay, time to oral intake, and diversion type), standardized complications within 90 days of surgery (reported using the Clavien–Dindo classification), and early oncologic outcomes using surrogate markers (pathologic stage, number of LNs removed, surgical margin, and LN density). The console time was defined as the period during which the surgeon sat at the console and performed the entire procedure, including cystectomy, LN dissection, bowel work, and anastomosis.

Surgical technique

Our surgical technique for RARC with PLND included basic positioning and port placement and was previously described.⁸ For ECUD, after extirpation of the bladder and bilateral PLND, the robot undocked and the specimen was removed through an ∼6-cm periumbilical incision. Urinary diversion with an ileal conduit or orthotopic neobladder (Studer type) was then performed extracorporeally. After ECUD, the robot was redocked into the pelvis, and urethroneovesical anastomosis was performed using robot assistance in cases involving an orthotopic neobladder. For ICUD, all procedures, including bowel work for urinary diversion and anastomosis, were intracorporeally completed regardless of whether an ileal conduit or orthotopic neobladder was selected. The details of the technique for ICUD have been described previously in the report on our initial experience.⁹

PLND was initially conducted within the standard territory, including the common and external iliac vessels and obturator fossa. As the cases accumulated, the range often extended to the inferior mesenteric artery, aortic bifurcation, or sacral plexus. Nodal packets were separately harvested from each packet, and each resected nodal packet was individually extracted with the aid of a small organ bag through the trocar site to minimize metastasis.¹⁰

Statistical analyses

Demographic, clinical, and pathologic variables were summarized using descriptive statistics. The values for continuous variables are given as mean (standard deviation). The statistical analyses were performed using Fisher's exact test and the chi-square test for categorical variables, which are specified as frequency (percentage). All statistical analyses were processed with SPSS version 18.0, and a P value below .05 was considered significant.

Results

Patient demographics

The characteristics of patients are shown in Table 1. There was no significant difference between the ECUD and ICUD groups in mean age (63.1 years vs. 65.4 years), sex distribution (male 92.1% vs. 92.3%), BMI (24.9 vs. 24.8), CCI (5.9 vs. 5.9), or history of abdominal surgery (21.1% vs. 11.5%). Neoadjuvant chemotherapy was administered in 7 patients in the ECUD group and 6 in the ICUD group (18.4% vs. 23.1%). One patient in the ECUD group underwent a salvage cystectomy after the failure of pelvic radiotherapy due to muscle-invasive bladder cancer. The difference was not statistically significant (all P values > .05).

Table 1.

Patient Characteristics

	All	ECUD	ICUD	P value
Number of patients (%)	64	38 (59)	26 (41)
Age (year), mean ± SD	64	63.1 ± 9.9	65.4 ± 10.3	.361^a
Sex				1.000^b
Male (%)	59 (92.2)	35 (92.1)	24 (92.3)
Female (%)	5 (7.8)	3 (7.9)	2 (7.7)
Body mass index, mean ± SD	24.9	24.9 ± 2.9	24.8 ± 2.8	.891^a
CCI, mean ± SD	6.0	5.9 ± 1.6	5.9 ± 1.2	.659^a
Preoperative conditions (%)
Neoadjuvant chemotherapy	13 (20.3)	7 (18.4)	6 (23.1)	.755^c
Prior pelvic radiotherapy	1 (1.6)	1 (2.6)	0 (0)	1.000^b
Prior abdominal and/or pelvic surgery	11 (17.2)	8 (21.1)	3 (11.5)	.502^b

Independent t-test.

Fisher's exact test.

Chi-square test.

CCI, Charlson comorbidity index; ECUD, extracorporeal urinary diversion; ICUD, intracorporeal urinary diversion; SD, standard deviation.

Perioperative outcomes and complications

Of the 64 patients, 38 had their urinary diversion constructed extracorporeally (23 ileal conduits and 15 orthotopic neobladders, 39.5%), and 26 patients had ICUD (15 ileal conduits and 11 orthotopic neobladders, 42.3%; Table 2). The difference was not statistically significant (P > .05).

Table 2.

Perioperative Outcomes

Characteristic	All	ECUD	ICUD	P value
Total operative time (minute), mean ± SD	513	468 ± 77.7	581 ± 76.3	<.001^a
Ileal conduit	474	436	533	.001^a
Orthotopic neobladder	570	516	649	<.001^a
Console time (min), mean ± SD	390	341 ± 79.0	462 ± 79.3	<.001^a
Estimated blood loss (mL), mean ± SD	217	265 ± 118.2	148 ± 62	<.001^a
Hospital stay (day), mean ± SD	16	16.7 ± 8.4	15 ± 7.6	.393^a
Time to flatus (hour), mean ± SD	72	72.1 ± 25.5	71.9 ± 39.0	.979^a
Time to oral intake (day), mean ± SD	5.0	5.6 ± 6.3	4.2 ± 1.3	.186^a
Type of urinary diversion (%)				.821^b
Ileal conduit	38 (59)	23 (60.5)	15 (57.7)
Orthotopic neobladder	26 (41)	15 (39.5)	11 (42.3)

Independent t-test.

Chi-square test.

The two groups were significantly different in terms of mean operative time, mean console time, and EBL. For ECUD, the mean total operative time was 468 minutes with a mean console time of 341 minutes, and for ICUD, the corresponding times were 581 and 462 minutes. The most notable differences were the mean operative times according to diversion type (ileal conduit: ECUD, 436 minutes vs. ICUD, 533 minutes; neobladder: ECUD, 516 minutes vs. ICUD, 649 minutes; P < .001). Mean EBL was 265 mL for ECUD and 148 mL for ICUD (P < .001).

There were no significant differences between the two groups in terms of length of hospital stay, time to flatus, and time to oral intake (P > .05). The mean length of hospital stay was 16.7 days for ECUD and 15 days for ICUD. The mean time to flatus was 71.9 hours for ECUD and 72.1 hours for ICUD. The mean time to oral intake was 5.6 days for ECUD and 4.2 days for ICUD.

In the ECUD group, 22 patients (57.9%) experienced at least one complication of any grade within 90 days of surgery, and 18 of these patients (47.4%) experienced a minor complication (grade 1–2). In contrast, there were only 8 patients (30.8%) in the ICUD group who experienced at least one complication of any grade, 4 (15.4%) of whom experienced a minor complication. The incidences of minor and total complications for the ECUD group were significantly higher than those for the ICUD group (minor: 47.4% vs. 15.4%; total: 57.9% vs. 30.8%; P < .05). Major complications (grade 3–5) occurred in 23.7% and 15.4% of the patients, respectively (P = 0.418; Table 3).

Table 3.

Complication Summary

	All	ECUD	ICUD	P value
Total complication rate, n (%)	30 (46.9%)	22 (57.9%)	8 (30.8%)	.033^a
Minor complication rate (Clavien grade 1–2), n (%)	22 (34.4%)	18 (47.4%)	4 (15.4%)	.008^a
Major complication rate (Clavien grade 3–5), n (%)	13 (20.3%)	9 (23.7%)	4 (15.4%)	.418^b

Chi-square test.

Fisher's exact test.

Oncologic outcomes

All patients showed a negative soft tissue surgical margin, and 21% of patients in the ECUD group and 26.9% in the ICUD group had pathologic stage T3 or T4 (Table 4). The mean number of LNs harvested was 23.2 for ECUD and 31.8 for ICUD (P = .012), and the rate of patients who underwent extended PLND was higher in the ICUD group (60.5% vs. 92.3%; P = .005); both of these differences were statistically significant. The LN density (total number of positive LNs/total number removed) was 13.2% in the ECUD group and 19.2% in the ICUD group (P > .05).

Table 4.

Oncologic Outcomes

Characteristic	All	ECUD	ICUD	P value
Pathologic stage (%)				.765^a
T2 or less	49 (76.6)	30 (78.9)	19 (79.1)
T3 or T4	15 (23.4)	8 (21.1)	7 (26.9)
Margin positivity, n	0	0	0
Type of lymph node dissection (%)				.005^a
Standard	17 (26.6)	15 (39.5)	2 (7.7)
Extended	47 (73.4)	23 (60.5)	24 (92.3)
Lymph node yield, mean ± SD	26.7	23.2 ± 13.2	31.8 ± 12.4	.012^b
Standard	14	12.8	22
Extended	31.3	30	32.6
Lymph node density (%)	10 (15.6)	5 (13.2)	5 (19.2)	.728^c

Chi-square test.

Independent t-test.

Fisher's exact test.

Discussion

Although the improved ergonomics enables a surgeon to operate with enhanced vision, precision, dexterity, and control by using robotic technology, the perceived technical difficulties, relatively longer operative times, and steep learning curve have limited the routine use of ICUD to only a small number of high-volume centers. ICUD has continued to gain acceptance among surgeons as their experience increases, and those with a background have a theoretical advantage. However, studies on ICUD are rare. Recently, the International Robotic Cystectomy Consortium (IRCC) published an analysis of 935 patients who underwent ICUD after RARC and were compared with ECUD patients; the results indicated that ICUD produced outcomes that were similar to ECUD and fewer complications.¹¹ However, this multi-institutional database study (18 international centers) was limited due to a degree of disparity in terms of patient selection, surgical technique, and the reporting of complications. In this study, we compared perioperative outcomes, postoperative complications, and early oncologic outcomes of ICUD and ECUD following RARC performed by a single surgeon at a tertiary referral hospital with a prospective maintained database.

In the current study, operative time, EBL, transfusion rates, and postoperative complications within 90 days using the Clavien–Dindo classification were used as important evaluation indicators of the surgical quality of RARC. The longer operative time of RARC is a critical issue regarding this complex procedure, as the longer anesthesia time may adversely impact perioperative morbidity and increase postoperative complications. However, the operative times reported in a contemporary RARC series should be examined with consideration for several factors. First, the mean yield and territory of PLND can influence the outcome. Second, the method of urinary diversion (ileal conduit vs. orthotopic neobladder) and particularly the type of ileal intestinal segment (single folding vs. double folding) used for the orthotopic neobladder should be considered. Urinary reconstruction was the step that was most likely to have variability in operative time and accounted for the longest operative time in a recent study.¹² Third, the rate of ICUD may also have an effect on the outcome. Fourth, there is variability in the learning curves of individual surgeons within an institution, and the impact of training of residents and fellows may offset the operative efficiency of the more experienced surgeons.¹³ The addition of new trainee surgeons and assistants in a teaching hospital makes it difficult to reduce the total operative time.

Bochner et al.⁵ reported a mean operative time of 464 minutes and a mean EBL of 500 mL in their RARC cohort. The urinary diversions in their study were performed extracorporeally, and 53% of patients (30 of 56) underwent orthotopic neobladder formation; in addition, the mean LN yield was 31.8, and the rate of patients who underwent extended PLND was 88%. Canda et al.² reported a mean operative time of 594 minutes and a mean EBL of 429 mL for ICUD, of which 92% of patients underwent orthotopic neobladder formation; in this series, the mean LN yield was 24.8, and 93% of patients (25 of 27) underwent extended PLND. However, the analysis only included the console time. In our study, the mean total operative time was 513 minutes with a mean console time of 390 minutes and a mean EBL of 217 mL. The mean number of LNs harvested was 26.7, and the rate of patients who underwent extended PLND was 73.4%. Also, 41% (26 of 64) of the urinary diversions were constructed intracorporeally, and the rate of orthotopic neobladder urinary diversion was 41%. We performed orthotopic neobladder urinary diversion with the double-folding Studer-type pouch, and trainee surgeons, including residents and fellows, participated throughout the whole process of the operation as first assistants. Of the 18 institutions in the IRCC,¹¹ the ICUD rate was 17.8%, the neobladder rate was 28%, and there was no difference in operative time between the ICUD group and the ECUD group. In our study, the mean overall operative time for the ICUD group was more prolonged than the ECUD group (468 minutes vs. 581 minutes; P < .001), and the results were also similar when compared according to each urinary diversion type (ileal conduit: 436 minutes vs. 533 minutes; neobladder: 516 minutes vs. 649 minutes; P < .001). Bowel harvest and intracorporeal suturing for anastomosis accounted for a greater portion of the total operative time than console time for orthotopic neobladder creation. The operative times for ICUD appear to decrease with experience. Nevertheless, a major stumbling block to the wider adoption of ICUD primarily relates to concerns about prolonged operative times, particularly early in the learning curve.¹² Studies demonstrating novel surgical techniques and instruments that shorten operative time are thus necessary.

We found that the mean EBL in the group with ICUD was significantly lower than that in the group with open urinary diversion (265 mL vs. 148 mL; P < .001). Moreover, the rate of perioperative transfusion in the ICUD group was lower than that in the ECUD group (28.9% vs. 3.8%; P = .02). Similarly, the transfusion rate in the IRCC report was significantly lower in the ICUD group, indicating that robotic surgery may reduce blood loss and the need for blood transfusion.

Based on a standardized reporting approach, complication rates for RARC vary between 34% and 80%.^14–17 Yuh et al.¹⁷ reported the 90-day complication rate for ECUD as 80% and the major complication rate as 35%, using a modified Clavien system. Recently, Bochner et al.⁵ reported that their prospective, randomized trial resulted in 62% and 66% 90-day postoperative complication rates in RARC- and ORC-treated patients, respectively, both of which involved extracorporeal reconstruction. Until now, RARC is still associated with significant complications. However, it is important to consider that most series reporting on RARC involved ECUD. Many of the perioperative complications following radical cystectomy may come from the urinary diversion portion of the procedure. Several studies have shown that open abdominal surgery with peritoneal air exposure is associated with postoperative systemic inflammatory response, leading to postoperative ileus (POI), and that laparoscopic surgery results in a significantly lesser systemic inflammatory response after surgery and a much shorter period of POI.^18–21 Although the difference in the degree of surgical trauma has been directly linked to the difference in outcomes between ECUD and ICUD, another potentially important advantage of ICUD is the reduction of exposure of the peritoneal cavity to air and bowel handling, which can result in a faster return of bowel function, a shorter hospital stay, and an earlier return to normal activities.²² The IRCC analysis¹¹ reported that 49% in the ECUD group and 41% in the ICUD group presented with complications within 90 days of surgery, and gastrointestinal complications and postoperative infections constituted the majority of the complications, occurring in 20% and 17% of all patients, respectively. Both of these complications were significantly lower in the ICUD group (10% and 12%, respectively).

In our study, the incidences of minor and total complications for patients in the ECUD group were higher than those for patients in the ICUD group (minor: 47.4% vs. 15.4%; total: 57.9% vs. 30.8%). There was a significant difference in the chi-square test (P < .05), yet there was no significant difference in major complications (23.7% vs. 15.4%; Table 3). Transfusion, postoperative infections, and wound revision constituted the majority of the complications according to the categorization system used (Table 5). Four patients underwent wound closure, which was performed under general anesthesia, and all of them had received RARC with ECUD. Gastrointestinal complications, including prolonged paralytic ileus up to 10 days after surgery and mechanical ileus, occurred in the ECUD group only, and none occurred in the ICUD group. Mean time to oral intake was shorter for ICUD than for ECUD (4.2 days vs. 5.6 days). Although no statistically significant differences were observed between the two groups, the results appeared to favor the ICUD group, in concordance with the potential benefits of ICUD.

Table 5.

Complication Summary Using System-Based Categories

Category	ECUD	ICUD	P value
Transfusion, n (%)	11 (28.9%)	1 (3.8%)	.021^a
Infectious, n (%)	9 (23.7%)	3 (11.5%)	.331^a
Wound revision, n (%)	4 (10.5%)	0
Genitourinary, n (%)	3 (7.9%)	3 (11.5%)	.680^a
Procedural, n (%)	3 (7.9%)	1 (3.8%)	.640^a
Gastrointestinal, n (%)	2 (5.3%)	0
Respiratory, n (%)	2 (5.3%)	0
Nervous, n (%)	1 (2.6%)	0
Vascular, n (%)	1 (2.6%)	0

Fisher's exact test.

Yuh et al. reported no significant differences in oncologic efficacy following either RARC or ORC, a PSM rate of 5.6% (1%–1.5% for T2 disease and 0%–25% for T3 and higher disease), and an LN density of 22% in a systemic review and cumulative analysis.³ A PSM rate of <10% is suggested for adequate quality in ORC.^23,24 The PSM rate for the 939 cases in the IRCC analysis was 9%.¹¹ In the present study, the PSM rate was 0%, and the LN density was 13.2% in ECUD group and 19.2% in ICUD group, indicating that the patient selection bias toward earlier stage disease (T2 or less, 76.6%) likely played a role in the lower PSM rates and LN positivity. In this study, the number of extended LND cases and the mean number of LNs harvested in the ICUD group were greater than those in the ECUD group (P = .005, P = .012). The method of urinary diversion is in fact irrelevant when considering oncologic outcomes. The reason for the difference is that PLND was initially conducted within the standard territory, and as the completed cases accumulated, the range extended to the level of the inferior mesenteric artery, aortic bifurcation, or sacral plexus.

Although ICUD remains a high-risk and complex procedure with a prolonged learning curve, the outcomes of this study are essentially in common with the results of previous studies demonstrating the potential benefits of ICUD following RARC, which include decreased blood loss, a lower transfusion rate, a shorter hospital stay, and less time to oral intake.^2,25 Our study also demonstrated lower complication rates after ICUD than after ECUD, including decreased wound dehiscence and infection. If the learning curve can be overcome safely with a clearly defined training program and a standardized approach, ICUD will certainly be a reproducible and promising technique.

This study had several limitations. First, the sample size was relatively small; thus, it was difficult to reach a definitive conclusion. Second, this was a comparative study of nonrandomized patients, and selection bias may have existed and influenced the results. Third, urinary diversion was performed extracorporeally only up to the 37th case and thereafter performed intracorporeally in this study. Due to this late start, ICUD was performed after the surgeon had accumulated more experience, and the LN yields and complication rates could have been influenced by this difference. However, it was not a completely consecutive series, as the technique for ICUD required another separate learning curve. Finally, our study had a relatively short follow-up period during which we evaluated the oncologic outcomes using surrogate markers.

Conclusion

From our experience, the results indicate that ICUD after RARC can be accomplished with the benefits of decreased blood loss, a lower transfusion rate, and a decreased complication rate compared to ECUD. Larger series and long-term follow-up data will be necessary to support our results. In addition, a comparison between RARC with ICUD and ORC is necessary to assess the advantage of ICUD in perioperative outcomes.

Footnotes

Acknowledgment

This study has been supported by a research grant from the Korea University College of Medicine (Seoul, Korea).

Disclosure Statement

No competing financial interests exist.

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