Simultaneous Robot-Assisted Nephroureterectomy and Cystectomy in Patients with Uremia and Multifocal Urothelial Carcinoma

Abstract

Background and Purpose:

In Taiwan, patients with uremia have a high risk of the development of multifocal urothelial carcinoma. We report on eight patients with uremia and urothelial carcinoma who underwent simultaneous robot-assisted laparoscopic nephroureterectomy and radical cystectomy (RANUC).

Patients and Methods:

Between April 2006 and August 2010, eight patients with uremia (five women, three men; mean age 66.9 y) who were receiving dialysis underwent RANUC. Patients were classified into two groups: Group I, cases 1 to 4 occurring between April 2006 and June 2009; and group II, cases 5 to 8 occurring between July 2009 and August 2010.

Results:

The mean operative time was significantly shorter in group II (252.5±35.0 min vs 360±25.8 min; P=0.029). The estimated blood loss was also significantly less in group II (332.5±53.8 mL vs 660±137.4 mL; P=0.029). The blood transfusion rate was 75% in group I and 0% in group II. The postoperative stay was reduced from 8.5 days for group I to 7 days for group II. No perioperative morbidity and mortality were noted in either group. None of the patients had died at the short- and intermediate-term mean follow-up of 28.1 months (range 2–54 mos).

Conclusions:

Simultaneous RANUC are feasible and can be performed safely. Long-term oncologic data are awaited; however, at intermediate-term oncologic follow-up, results are satisfactory. RANUC for uremic patients with multifocal urothelial carcinoma necessitating complete urinary tract exenteration is a viable option and patients experience a rapid convalescence.

Introduction

A n increased incidence of malignancy during chronic renal failure was reported as early as 1975.¹ In the 1990s, there were reports of a higher risk group of patients in Taiwan—those with uremia—in whom urothelial carcinoma (UC) developed.^2,3 The incidence of UC among hemodialysis patients ranged from 0.89% to 1.8%.^3

–6 The incidence of UC in Taiwanese patients undergoing dialysis was higher than in the general population.^3

–6 The standardized incidence ratio of UC was 48.2-fold compared with the general population, and the standardized incidence ratio of UC seemed higher in women (65.1-fold) and in the 50- to 54-year-old age group (173.6-fold).⁵ UC in patients with uremia exhibited bilaterality and multifocal (involved bilateral upper urinary tract [UUT] and/or urinary bladder [UB]) tendencies.^4

–9

Multiple operations (bilateral UUT and/or UB) because of frequent recurrence and/or consideration of anesthesia risk in patients with synchronous tumors are not uncommon.^6

–9 Uremic patients have increased anesthesia risks because of compromised immune systems, poor cardiovascular systems, susceptibility of fluid overload, and diathesis of coagulopathy. The perioperative morbidity of open or laparoscopic bilateral nephroureterectomy and/or radical cystectomy has been reported between 12% and 37.5%; the mortality rate ranged from 5.5% to 25%.^6

–11

The da Vinci^® Surgical System (Intuitive Surgical, Inc., Sunnyvale, CA) helps overcome the drawback of pure laparoscopy by providing a high-resolution three-dimensional image and EndoWrist^® instruments that allow the surgeon to operate with better depth perception and with the same dexterity and wrist movement. The da Vinci robot-assisted radical prostatectomy (RARP) was a turning point to utilize this tool for performing pelvic surgeries.¹² Similarly, robot-assisted nephroureterectomy has been reported as a safe, feasible, and minimally invasive option for management of UC in the UUT using the daVinci tool.^13,14

A first large case series of robot-assisted radical cystectomy (RARC) was first reported in 2003.¹⁵ Later, it generated world-wide interest and the International Robotic Cystectomy Consortium database prospectively identified 496 patients who underwent RARC by 21 surgeons at 14 institutions from 2003 to 2009 and concluded that RARC is a challenging procedure but can be reproduced at multiple centers.¹⁶ A randomized controlled trial of robot-assisted vs open radical cystectomy for bladder cancer has also demonstrated that the robotic approach is equivalent to the open counterpart.¹⁷

We present an initial experience of simultaneous robot-assisted laparoscopic nephroureterectomy and radical cystectomy (RANUC) in eight patients with uremia and UC who needed complete pelvic exenteration.

Patients and Methods

Eight patients with uremia who were receiving dialysis underwent open or laparoscopic unilateral nephroureterectomy 6 months to 5 years earlier. Metachronous or recurrent multifocal UC in UUT and/or UB developed during the follow-up period, recalcitrant to endourologic management; hence, these patients were candidates for RANUC. The eight patients were classified into two groups: Group I, cases 1 to 4 from April 2006 to June 2009; and group II, cases 5 to 8 from July 2009 to August 2010 to see the impact of experience. The console surgeon performed 150 cases of RARP in June 2009, which was a watershed of the learning curve for reducing complications.¹⁸ Patient demographics and data were recorded.

Surgical procedure

The same surgical team, including the single console surgeon (YO) and a clinical fellow performed all procedures with the same standard da Vinci four-arm system. The surgical procedure was modified from the previously published technique.^{15
–17,19,20} Briefly, our technique is detailed:

The patient is placed in a 60-degree lateral decubitus position.

Trocar placement is illustrated in Figure 1. Three ports for the da Vinci robot arms (10-mm supraumbilical port for the robot camera, and two 8-mm ports for the second and third robot arm) are placed 6 to 8 cm away from the camera port, along a line from the umbilicus to the anterior superior iliac spine (ASIS) and the line from the umbilicus to the tip of the 12th rib.

An additional 12-mm assistant port is placed 6 to 8 cm lateral to the robotic port for suction, retraction, and stapling.

During nephroureterectomy, a 30-degree down laparoscope was used. The line of Toldt was incised, and the colon was mobilized medially.

The perirenal and periureteral space was entered. The renal hilum was dissected. The renal artery and vein were separately clipped with Hem-o-lok (Weck Closure Systems, Research Triangle Park, NC) and divided.

Dissection continued from the ureter downward to the level of the iliac vessel.

Then, the patient position was changed to the lithotomy position with 30-degrees of Trendelenburg, and the surgical field was resterilized and draped.

Three of the previous four ports were retained, and another 8-mm port for the robot arm was placed 8 cm away from the camera port, along the line from the umbilicus to the ASIS.

Repositioning and redocking of the robot were performed.

During radical cystectomy or radical cystoprostatectomy, 0-degree laparoscopy was introduced. The lower ureter at the level of the iliac vessel was identified and dissected to the ureterovesical junction.

Pelvic lymph node dissection was performed in six patients with UC of the UB. Posterior dissection from the cul-de-sac to the posterior peritoneum and above its reflection over the rectum connected with the incisions previously made for the ureteral dissection at the ureterovesical junction occurred.

Dissection was performed caudally, mobilizing the bladder, seminal vesicles, and the base of the prostate (for men) off the rectum.

Subsequently, bilateral dissection with lateral incisions in the peritoneum was used to expose and develop the pedicles. The bilateral pedicles were controlled using the endo-GIA stapler.

After completion of the posterior and lateral dissection, the peritoneum was incised anteriorly, dropping over the bladder. The endopelvic fascia was incised bilaterally.

The dorsal venous complex was ligated with 0 polyglactin on a CT-1 needle or divided with the endo-GIA stapler.

The urethra was transected.

The Foley catheter was clipped with a Hem-o-lok clip to avoid urinary leakage and contamination.

The entire specimen, including the kidney, ureter, urinary bladder, and prostate (for men) was freed and placed in an endocatch II bag. For male patients, the specimen was removed through an extended 4 to 5 cm supra- or infraumbilical incision. In females, the specimen was removed from the vagina.

The pelvis was irrigated, and hemostasis was achieved. A new Foley catheter was placed in the pelvis for drainage. Another Jackson-Pratt or Penrose drain was placed in the abdomen. The operative parameters included total operative time, estimated blood loss, transfusion rate, complications, and length of postoperative stay. Perioperative parameters between both groups were then compared.

FIG. 1.

Trocar mapping: A total of five ports (1, 2, 3R, 4R, and 5) for right nephroureterectomy and radical cystectomy; right nephroureterectomy using 1, 3R, 4R, and 5; radical cystectomy using 1, 2, 4R, and 5. A total of five ports (1, 2, 3L, 4L, and 5) for left nephroureterectomy and radical cystectomy; left nephroureterectomy using 1, 2, 3L, and 4L; radical cystectomy using 1, 2, 4L, and 5. Port 1 was a supraumbilical camera port, 12 mm; 2, 3L, 3R, and 5 were robotic arm ports, 8-mm; 4R and 4L were assistant ports, 12 mm. ASIS=anterior superior iliac spine.

Statistical analysis

All data are expressed as mean±SD. SPSS 12.0 for Windows (SPSS, Inc, Chicago, IL) was used for statistical calculations. Statistical analysis was performed using the nonparametric Mann-Whitney U test, Fisher exact test, and Yates correction of the contingency test, as appropriate. A P value <0.05 was considered statistically significant.

Results

Table 1 depicts the demographics of the eight patients (five women and three men with a mean age of 66.9 y). The mean duration of hemodialysis was 3.75 years, ranging from 1.5 to 8 years. Previous nephroureterectomy was performed by open surgery in five patients and laparoscopically in three patients.

Table 1.

General Data on Simultaneous Robot-Assisted Laparoscopic Nephroureterectomy and Cystectomy in Patients with Uremia and Multifocal Urothelial Carcinoma

No.	Age	Sex	HD (y)	Hx. of uni. nux. (y)	UUT, UC	Preoperative stage	Grade
1.	65	F	9	5^a	Rt	T₁	High
2.	57	F	3	2^b	Lt	T₁	High
3.	61	F	3	5^a	Lt	T₁	High
4.	71	M	0.5	0.5^b	Rt	T₁	Low
5.	72	F	1	1^a	Rt	T_a	Low
6.	66	M	5	5^a	Rt	CIS	High
7.	78	F	8	2^a	Lt	T₁	Low
8.	65	M	0.5	3.5^b	Lt	T₁	Low
Mean±SD	66.9±6.6		3.75±3.32	3.00±1.87

Open.

Laparoscopy.

HD=duration of hemodialysis; Hx. of uni. nux=number of years since unilateral nephroureterectomy; UUT=upper urinary tract; UC=urothelial cancer; F=female; Rt=right; Lt=left; M=male; CIS=carcinoma in situ; SD=standard deviation.

The first case was challenging, because she had history of appendectomy and hemicolectomy. We performed RANUC with removal of the specimen from the vagina. The entire operative time was 390 minutes, including 50 minutes for lysis of adhesions. The estimated blood loss was 600 mL with necessity for blood transfusion. She was discharged on postoperative day 9 (Figs. 2A, 2B).

FIG. 2.

(A) Trocar wound and drainage in operating room after completion of simultaneous robot-assisted laparoscopic nephroureterectomy and radical cystectomy. A. Previous appendectomy scar; B. previous nephroureterectomy with bladder cuff excision scar; C. right hemicolectomy scar. (B) Abdominal scars 1 month after simultaneous robot-assisted laparoscopic nephroureterectomy and radical cystectomy. Nephroureterectomy four port scar (1, 2, 3L, 4L) and radical cystectomy four port scar (1, 2, 4L, 5).

Table 2 shows the perioperative parameters of the patients who were receiving RANUC. The mean operative time was 306 minutes (range 210–390 min). The mean estimated blood loss was 496 mL (range 280–850 mL). The final pathologic findings of the UUT revealed UC in six cases (stages T_a [2], T₁ [3], and T2a [1]). Two patients had end-stage renal disease (ESRD), and one patient had recurrent attacks of pyelonephritis from nephrolithiasis. The pathologic findings of the UB proved UC in six cases (stages carcinoma in situ [2] and T₁ [4] and grade high [4] and low [2]). All patients had recurrent UC carcinoma of the UB. Two cases revealed no evidence of disease at the time of cystectomy. The mean number of pelvic lymph nodes was seven; none of the patient had disease in the lymph nodes.

Table 2.

Perioperative Parameters of Simultaneous Robot-Assisted Laparoscopic Nephroureterectomy and Cystectomy in Patients with Uremia and Multifocal Urothelial Carcinoma

No.	BMI	ASA	Operative time (min)	EBL (mL)	UUT, UC	Stage	Grade	UB, UC	Postop stay (d)
1.	24.5	III	390	600	Lt	T_a	Low	NED	9
2.	25.6	III	370	530	Rt^a	T_2a	High	T₁, high^a	7
3.	23.5	III	330	850	Rt^a	T₁	High	T₁, high^a	9
4.	18.4	II	350	660	Lt	T₁	Low	NED	9
5.	23.3	III	290	300	Lt	T_a	Low	T₁, low^a	7
6.	25.6	III	270	350	Lt	ESRD	Nil	T₁, high^a	7
7.	24.1	III	210	400	Rt	Stone, PN	Nil	CIS, high^a	7
8.	31.8	II	240	280	Rt	T₁	High	CIS, low^a	7
Mean±SD	24.60±3.69		306.25±64.13	496.25±199.92					7.75±1.04

Recurrent tumor necessitating frequent endoscopy.

BMI=body mass index; ASA=American Society of Anesthesiologists; EBL=estimated blood loss; UUT=upper urinary tract; UC=urothelial cancer; UB=urinary bladder; postop=postoperative; Lt=left; NED=no evidence of disease; Rt=right; ESRD=end-stage renal disease; PN=pyelonephritis; CIS=carcinoma in situ.

Table 3 showed the comparison of the perioperative parameters of both groups who were receiving simultaneous RANUC. The mean operative time was significantly shorter in group II (252.5±35.0 min vs 360±25.8 min; P=0.029). The estimated blood loss was also significantly less in group II (332.5±53.8 mL vs 660±137.4 mL; P=0.029). The blood transfusion rate was 75% in group I and 0% in group II. The postoperative stay was reduced from 8.5 days for group I to 7 days for group II. No perioperative morbidity or mortality was noted in either group. The overall survival rate was 100%, with a mean follow-up of 28.1 months (range 2–54 mos).

Table 3.

Comparison of Perioperative Parameters of Both Groups Receiving Simultaneous Robot-Assisted Laparoscopic Nephroureterectomy and Cystectomy in Patients with Uremia and Multifocal Urothelial Carcinoma

Parameter	Group I (April 2006–June 2009)	Group II (July 2009–June 2010)	P
Case number	4	4
Age	63.5±5.97	70.25±6.02	0.114
M/F	1/3	2/2	1.000
BMI	23.00±3.18	26.20±3.85	0.486
ASA class	2.75	2.75	1.000
Operative time (min)	360±25.8	252.5±35.0	0.029^a
EBL (mL)	660±137.4	332.5±53.8	0.029^a
Transfusion rate (%)	75%	0%	0.143
Complication rate (%)	0%	0%	1.000
Postoperative stay (d)	8.5±1.0	7±0	0.114

P<0.05.

BMI=body mass index; ASA=American Society of Anesthesiologists; EBL=estimated blood loss.

Discussion

The da Vinci robot-assisted procedure for pelvic surgeries galvanized after the success of radical prostatectomies.^12,15,18,21 This led to the development of robot-assisted radical cystectomy with urinary diversion.^{15
–17,19,20} The first to report concomitant nephroureterectomy and cystectomy that was performed laparoscopically for two men with muscle-invasive transitional-cell carcinoma of the UB and preexisting dialysis-dependent ESRD were Berglund and associates²² in 2006. Both patients tolerated the procedure well, and there were no intraoperative complications. ²² The second patient's course after surgery, however, was complicated by a prolonged adynamic ileus and infection of the catheter placed for continuous ambulatory peritoneal dialysis; he was discharged 28 days after surgery and died from unknown causes at 30 days.²² Afterward, simultaneous laparoscopic nephroureterectomy and cystectomy were reported in the literature.^9
–11

Based on the literature, we attempted simultaneous RANUC in patients with uremia who had multifocal UC, and to best of our knowledge, this is the first large series in the literature. A report of eight cases of RANUC for patients with uremia demonstrated a mean operative time of 306 minutes with a mean estimated blood loss of 496 mL. No perioperative complications or mortalities were noted. The mean postoperative stay was 7.75 days. The big advantage in our patients was low body mass index. In addition, there was uremic tissue yield and high pliability, which helps in easy dissection.

Patients with uremia have increased risks of anesthesia-related complications because of compromise in immune system function, poor cardiovascular system, and impaired hemostatic mechanisms. They are prone to such perioperative complications as bleeding, infection, septic shock, prolong ileus, electrolyte imbalance, pulmonary edema, pulmonary atelectasis, cardiovascular disease, and cerebrovascular attack.^6,8

–11 Even in recent years, treatment of such patients is challenging and necessitates cooperation from the anesthesiologist, surgeon, intensive care specialist, and nephrologist.

The perioperative morbidity of open or laparoscopic bilateral nephroureterectomy and/or radical cystectomy is high and ranges from 12% to 37.5%.^6

–11 The mortality rate of open or laparoscopic nephroureterectomy and radical cystectomy was unacceptably high, ranging from 5.5% to 25%.^6,9,10 Kang and colleagues⁶ reported on 70 patients with uremia and UUT UC who received nephroureterectomy and/or radical cystectomy; there were 5 (7.14%) deaths, with a significantly higher perioperative mortality (3/13, 23.1%) in patients who were undergoing cystectomy (P=0.042) than in patients without cystectomy (2/57, 3.5%). The three patients who underwent one-stage unilateral or bilateral nephroureterectomy and radical cystectomy had massive blood loss and died of cardiovascular complications.

Previously, Wu and coworkers⁷ recommended one-step bilateral nephroureterectomy and radical cystectomy for patients with UC receiving dialysis because of the high incidence of synchronous and subsequent tumors. In the present series, previous unilateral nephroureterectomy reduced operative time, anesthesia time, and the risk of perioperative complication for the patient with uremia. In our limited experience of eight patients undergoing RANUC, no perioperative morbidity or mortality was reported.

Repositioning after robot-assisted nephroureterectomy for cystectomy can be performed expediently and takes 15 to 20 minutes for an experienced surgical team. A total of five or six ports can be used to complete RANUC as per need, and the whole specimen can be removed from the vagina in females and a small abdominal incision by extending a trocar site in males.

For the purpose of evaluation as to whether experience matters or not, patients were classified into two groups. The mean operative time was statistically significantly shorter in group II than in group I (252.5±35.0 min vs 360±25.8 min, P=0.029). The estimated blood loss was statistically significantly less in group II than in group I (332.5±53.8 mL vs 660±137.4 mL, P=0.029). The blood transfusion rate was reduced from 75% in group I to 0% in group II. The postoperative stay was reduced from 8.5 days for group I to 7 days for group II.

The drawback of the study is the limited number of patients (N=8), but this is a rare condition. A center with the availability of the daVinci system, however, can use this for single-stage pelvic or UUT and lower urinary tract exenteration.

Conclusion

Simultaneous RANUC is another viable application of robot-assisted surgery. RANUC for patients with uremia who have multifocal UC is feasible, safe, and provides rapid convalescence. RANUC can be offered to patients who need simultaneous nephroureterectomy and cystectomy.

Footnotes

Disclosure Statement

No competing financial interests exist.

Abbreviations Used

References

Matas

, Simmons

, Kjellstrand

et al. Increased incidence of malignancy during chronic renal failure. Lancet, 1975; 1:883–886.

Jiaan

, Yu

, Lee

, huang

. Uraemia with concomitant urothelial cancer. Br J Urol, 1993; 72:458–461.

Chen

, Lai

, Huang

et al. Urologic cancers in uremic patients. Am J Kidney Dis, 1995; 25:694–700.

, Pan

, Lin

et al. Transitional cell carcinoma in dialysis patients. Eur Urol, 2000; 37:90–94.

Chang

, Yang

. Renal diagnosis of chronic hemodialysis patients with urinary tract transitional cell carcinoma in Taiwan. Cancer, 2007; 109:1487–1492.

Kang

, Chen

, Chiang

. Primary urothelial carcinoma of the upper urinary tract in dialysis patients with 5-year follow-up. Jpn J Clin Oncol, 2010; 40:241–246.

, Shee

, Ho

et al. Different treatment strategies for end stage renal disease in patients with transitional cell carcinoma. J Urol, 2004; 171:126–129.

Tai

, Lai

, Chung

et al. Intermediate-term oncological outcomes of hand-assisted laparoscopic versus open bilateral nephroureterectomy for dialysis and kidney transplant patients with upper urinary tract urothelial carcinoma. J Endourol, 2009; 23:1139–1144.

Lin

, Hung

, Chen

et al. Single-session laparoscopic total urinary tract exenteration without repositioning for multifocal urothelial carcinoma in dialysis-dependent patients. Urology, 2011; 77:98–103.

10.

Barros

, Frota

, Stein

et al. Simultaneous laparoscopic nephroureterectomy and cystectomy: A preliminary report. Int Braz J Urol, 2008; 34:413–421.

11.

, Wang

, Wu

et al. Laparoscopic complete urinary tract exenteration with the specimen withdrawn transvaginally. BJU Int, 2009; 104:82–86.

12.

Menon

, Hemal

. VIP Team. Vattikuti Institute prostatectomy: A technique of robotic radical prostatectomy: Experience in more than 1000 cases. J Endourol, 2004; 18:611–619.

13.

Nanigian

, Smith

, Ellison

. Robot-assisted laparoscopic nephroureterectomy. J Endourol, 2006; 20:463–466.

14.

Patel

, Krane

, Hemal

. A novel technique of robotic nephroureterectomy with bladder cuff excision for the management of upper tract transitional cell carcinoma without repositioning or dedocking the robot. J Endourol Part B, Videourology, June 2010; 24, No. 3.https://dx-doi-org.web.bisu.edu.cn/10.1089/vid.2010.0006. 2011 February 1.

15.

Menon

, Hemal

, Tewari

et al. Nerve-sparing robot-assisted radical cystoprostatectomy and urinary diversion. BJU Int, 2003; 92:232–236.

16.

Hayn

, Hussain

, Mansour

et al. The learning curve of robot-assisted radical cystectomy: Results from the International Robotic Cystectomy Consortium. Eur Urol, 2010; 58:197–202.

17.

Nix

, Smith

, Kurpad

et al. Prospective randomized controlled trial of robotic versus open radical cystectomy for bladder cancer: Perioperative and pathologic results. Eur Urol, 2010; 57:196–201.

18.

, Yang

, Wang

et al. The learning curve for reducing complications of robotic-assisted laparoscopic radical prostatectomy by a single surgeon. BJU Int, 2010 Nov 2 10.1111/j.1464-410X.2010.09847.x. [Epub ahead of print]

19.

Pruthi

, Stefaniak

, Hubbard

, Wallen

. Robot-assisted laparoscopic anterior pelvic exenteration for bladder cancer in the female patient. J Endourol, 2008; 22:2397–2402.

20.

Pruthi

, Wallen

. Robotic-assisted laparoscopic radical cystoprostatectomy. Eur Urol, 2008; 53:310–322.

21.

Coelho

, Chauhan

, Palmer

et al. Robotic-assisted radical prostatectomy: A review of current outcomes. BJU Int, 2009; 104:1428–1435.

22.

Berglund

, Matin

, Desai

et al. Laparoscopic radical cystoprostatectomy with bilateral nephroureterectomy: Initial report. BJU Int, 2006; 97:37–41.