JOURNAL OF ENDOUROLOGY Volume 28, Number 6, June 2014 ª Mary Ann Liebert, Inc. Pp. 679–685 DOI: 10.1089/end.2013.0775

Robot-Assisted Technique for Boari Flap Ureteral Reimplantation: Is Robot Assistance Beneficial? Minh Do, MD, PhD,1 Panagiotis Kallidonis, MD, MSc, PhD,1,2 Hasan Qazi, MD, PhD,3 Evangelos Liatsikos, MD, PhD,2 Phuc Ho Thi, MD,1 Anja Dietel, MD,1 and Jens-Uwe Stolzenburg, MD, PhD1

Abstract

Background and Purpose: Ureteral reconstructive surgery necessitates adequate exposure of the ureteral lesion and results in large abdominal incisions. Robot assistance allows the performance of complex ureteral reconstructive surgery through small incisions. The current series includes only cases of Boari flaps performed by robot assistance and attempts to describe in detail the technique, review the literature, as well as to expand the experience in the current literature. Patients and Methods: Eight patients underwent ureteral reimplantation by Boari flap technique. The indications for the performance of the procedure included ureteral stricture from iatrogenic injury in three patients, recurrent ureteral stricture after multiple endoscopic stone management procedures in one patient, ureteral stricture from previous malignant disease in the pelvis or abdomen in three patients, and ureteral stricture due to trauma in one patient. Five cases were located in the left side and three cases in the right side. A variety of parameters were recorded in a prospective database including the time for robot docking and total operative time as well as catheterization and drainage time. The follow-up of the patients included the performance of renal ultrasonography 4 weeks, 3, 6, and 12 months after the procedure. Results: Mean age of the patients was 50.8 (range 39–62) years and mean body mass index was 26.2 (range 23.22–29.29) kg/m2. Operative time ranged 115 and 240 (mean 171.9) minutes. Mean blood loss was 161.3 (50–250) mL. Conversion to open surgery did not take place in the current series. No intraoperative complications were observed. Postoperative complications included one case of prolonged anastomotic leakage. Conclusion: The robot-assisted approach is efficient in the performance of ureteral reimplantation with Boari flap. Low blood loss, short catheterization time, low complication rate, and excellent reconstructive outcome are associated with the approach. Robot assistance seems to be beneficial for ureteral reconstructive surgery. Introduction

U

reteral reconstructive surgery is associated with significant challenge and represents an evolving field of urologic practice. Reconstructive surgery should be considered for a large variety of cases such as ureteropelvic junction obstruction, ureteral trauma, strictures, as well as the management of urothelial tumors located in the ureter.1,2 The length of the ureteral lesion is the most important factor for the determination of the most appropriate procedure for ureteral reconstruction and reimplantation. In fact, implantation by ureterocystotomy is usually indicated for short defects of 4 to 5 cm, while larger defects need either the

1 2 3

psoas hitch and/or Boari flap. Ureteral lesions between 6 and 10 cm could be bridged by psoas hitch, and longer lesions up to 15 cm by the additional performance of a Boari flap.3 The need for adequate exposure of the lesion and the subsequent management of the involved structure results in a large abdominal incision. The latter is associated with significant morbidity.3 The advent of the DaVinci (Intuitive Surgical Inc., Sunnyvale, CA) system provided magnified three-dimensional vision of the operative field, precision in movements, and increased degree of movement in comparison with conventional laparoscopic and open surgical approaches.4 These advantages rendered the performance of complex reconstructive surgery possible through a few

Department of Urology, University of Leipzig, Leipzig, Germany. Department of Urology, University of Patras, Greece. Department of Urology, Gartnavel General Hospital, Glasgow, United Kingdom.

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DO ET AL.

FIG. 1. Patient position. Notice the angle used for the procedure.

small abdominal incisions, and several investigators have proposed their experience with reconstructive procedures of the ureter.2,3,5–10 Nevertheless, the technique of Boari flaps has been scarcely presented among the above case series and counts a small number of cases.3,4,10,11 The current series includes only cases of Boari flaps performed with robot assistance and attempts to describe in detail the technique, review the literature, as well as to expand the experience in the current literature. Patients and Methods

Eight patients underwent ureteral reimplantation by Boari flap technique. The indications for the performance of the procedure included ureteral stricture from iatrogenic injury in three patients, recurrent ureteral stricture after multiple endoscopic stone management procedures in one patient, ureteral stricture from previous malignant disease in the pelvis or abdomen (no sign of disease at the time of procedure) in three patients, and ureteral stricture from trauma in one patient. Five cases were located in the left side and three cases in the right side. Cases of iatrogenic injury were associated with pelvic surgery, which resulted in accidentally ligating or injurying the ureter. Usually these cases are associated with strictures that tend to become longer after the first endoscopic treatment sessions. Cases of malignant disease were associated with lymphoma, cervical and testicular cancer. Two surgeons experienced in laparoscopy and robotics performed the procedures. The technique performed replicated the steps of the open ¨ belho¨r and was based on procedure of Boari flap according to U the principles previously described by other investigators.3,12

anterior rectus sheath, the optical trocar (Hassan type) is introduced, and pneumoperitoneum is established. An 8-mm robotic trocar is inserted on the left side of the abdomen four fingertips lateral to the midline and 2-cm cephalad of the hypothetical line between the umbilicus and the pubic arch. A laparoscopic instrument could be inserted to facilitate the dissection of any intra-abdominal adhesions and to push the bowel while the remaining the trocars are inserted. A 12-mm conventional laparoscopic trocar is placed two fingers medially and 2-cm cephalad to the right anterior superior iliac spine. The latter port allows the insertion of grasper, clip applicators, endobag, and sutures. Another 8-mm trocar is placed five fingers to the right from the umbilicus and 2-cm cephalad of the hypothetical line between the anterior superior iliac spine and the umbilicus. A fifth trocar (8 mm) is inserted three fingerbreadths medial and 2-cm cephalad to the left anterior superior iliac spine.

Surgical technique Patient positioning and trocar placement. The patient is placed in a dorsal supine position with legs abducted to allow the placement of the robotic system between them. The patient is set in a steep Trendelenburg position of approximately 15 degrees during the robot docking (Fig. 1). All procedures were performed with the use of four robotic arms and five trocars. A 15-mm supraumbilical midline incision is made, and the abdominal cavity is entered. Stay sutures are placed on the

FIG. 2. The trocar placement for right-sided Boari flap ureteral reimplantation. The same positioning could be used for long strictures up to the level of the pelvic brim on the left side. Otherwise, left-side cases could be managed with the placement of the trocars in mirror image to the one presented in the figure.

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FIG. 3. (a) The ureter is prepared caudally toward the bladder. The dissection is extended as close to the bladder as possible. (b) A Hem-o-lok clip is used to seal the distal part of the strictured ureteral segment that is about to be resected. The Double-J stent in the image was inserted before the procedure.

The above trocar positioning takes place for cases of rightsided Boari flaps and cases located on the left side when the strictured site is up to the level of the pelvic brim (Fig. 2). In the case of a left-sided procedure, the two robotic trocars are inserted in the right abdominal wall while the third robotic and assistant trocars are inserted on the other side. Robot docking takes place, and the instruments used are the following: a fenestrated bipolar forceps, a large needle driver, a Hot Shear (monopolar curved scissors) and a ProGrasp forceps. Technique of Boari flap formation. The technique performed is practically a replication of the open Boari flap ¨ belho¨r.12 The cecum or sigmoid technique according to R. U colon is initially mobilized depending on the side on which the procedure takes place. The ureter is identified at the bifurcation of the iliac vessels. Careful preparation of the ureter is performed with caudal direction guided to the site of the stricture (Fig. 3a). The ureter is retracted by the fourth robotic arm during the dissection. A clip is placed proximally to the cephalad side of the strictured ureteral segment while the caudal side is transected as distal as possible at the point that the ureter is inserted into the bladder (Fig. 3b). Then, the bladder is mobilized as distal as possible ipsilaterally to the structured ureter. It is very important not to transect the vascular supply of the bladder. Saline was used to fill the bladder, and the surgeon could decide the performance of a Boari flap ureteral implantation. The posterior bladder wall was fixed on the psoas muscle with the use of 3-0 polyglactin suture (psoas hitch). The Boari flap is formed by an incision with a 2:1 proportion in length and width. The ureter is spatulated and implanted through a submucosal tunnel in the apex of the Boari flap (Figs. 4a, b). The implantation of the ureter replicates the technique described by Politano and Leadbetter13 in the open surgical

approach. The ureter is retracted through the submucosal tunnel (Fig. 5a), and the ureteral adventitia is sutured to the mucosa of the flap using 5-0 polyglactin suture (Fig. 5b). At this point, a Double-J stent is inserted in the ureter over a guidewire (Fig. 6a, b) through an 18-gauge needle after the abdominal wall is punctured by a needle appropriate for percutaneous procedures. The flap is then tabularized (Fig 7a). For this purpose, 3-0 polyglactin sutures are used in two layers. The bladder opening is then closed in two layers using 3-0 polyglactin sutures. The bladder is then filled with 200 mL saline to exclude any extravasation. A drainage tube is inserted through the contralateral to the side of the treated ureter 8-mm ports. Recorded parameters and postoperative management. All cases were recorded in a prospective database. A

variety of parameters were recorded including the time for robot docking and total operative time as well as catheterization and drainage time. The drainage was removed on the second postoperative day. If the drainage was associated with high output, the fluid was examined for the presence of creatinine, and the removal or not of the drainage tube was decided. A cystographic examination of the bladder took place on the sixth postoperative day, and the healing of the bladder incision as well of the ureteral anastomosis was assessed. When no leakage was observed, the catheter was removed. The Double-J stent was removed after at least 4 weeks. The follow-up of the patients included the performance of renal ultrasonography 4 weeks after the removal of the ureteral stent or earlier if symptomatology was present. Renal ultrasonography was repeated at 3, 6, and 12 months after the procedure. Cases suspicious for inefficient drainage were further evaluated with computed tomography urography or

FIG. 4. (a) The ureter has been transected, and the stenotic segment has been excised. At this point, the ureter can be spatulized. (b) A submucosal tunnel is created in the Boari flap.

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FIG. 5. (a) The spatulated ureter is passed through the previously created submucosal tunnel. A suture at the tip of the spatulized ureter is helpful for this maneuver. (b) The ureteral adventitia is sutured with the Boari flap mucosa with 5-0 polyglactin sutures.

FIG. 6. (a) A Double-J stent is inserted over a guidewire and will remain in place for 4 to 6 weeks. The first step is the insertion of the guidewire, which takes place using a needle for percutaneous puncture. (b) The Double-J stent is pushed over the guidewire into the ureter.

FIG. 7. (a) The Double-J stent is inserted and placed also in the opened bladder. Suturing of the Boari flap to close the opening is about to follow. (b) Cystography on the sixth postoperative day in a Boari flap case performed with robot assistance. No extravasation is evident.

MAG3 scintigraphy at the discretion of the treating physician. Patients with malignancy were followed according to the indicated schedule for their disease and were evaluated with the above protocol if it was deemed necessary. Perioperative, short- and long-term complications were also recorded and classified according to the Clavien-Dindo classification of surgical complications.14 Results

Patient characteristics and perioperative results are presented in Table 1. The current series included five male and three female patients with a mean age of 50.8 (range 39–62) years and mean body mass index of 26.2 (range 23.22–29.29) kg/m2. Operative time ranged between 115 and 240 (mean 171.9) minutes. Mean blood loss was 161.3 (50–250) mL.

Conversion to open surgery did not take place in the current series. No intraoperative complications were observed. The catheter was removed according to schedule in all patients (Fig. 7b), except for one patient. In the latter case, a prolonged anastomotic leakage was diagnosed during the cystography examination on the sixth postoperative day. The urinary leakage gradually decreased, while the drainage tube was already removed on the fourth postoperative day. The patient had prolonged catheterization (grade I complication). The 12-month follow-up of the patients did not show any significant complication associated with the procedure. Discussion

Reconstructive surgery of the upper urinary tract represents a challenging field necessitating delicate suturing and

ROBOT-ASSISTED BOARI FLAP URETERAL REIMPLANTATION

Table 1. Patient Characteristics and Perioperative Parameters

Age (years) BMI (kg/m2) Total operative time (min) Access and robot docking time (min) Estimated blood loss (mL) Drainage time (days) Catheterization time (days)

Mean value

Range

SD

50.8 26.2 171.9 15.3

39–62 23.22–29.29 115–240 6–20

9.93 2.05 41.14 4.34

161.3 2.4 6.8

50–250 2–4 6–12

61.98 0.7 2.12

SD = standard deviation; BMI = body mass index.

an operative field extending from the bladder to the proximal ureter. The large incision, which is usually necessary, is balanced by the functional outcome for the patient. The emergence of the laparoscopic approach allowed the performance of reconstructive ureteral surgery without the performance of large incisions and minimized the incisionrelated morbidity. In fact, the laparoscopic approach was associated with lower blood loss, less pain, improved visualization and cosmesis in comparison with the open approach.15–17 The robot-assisted approach combines the advantages of the laparoscopic approach with improved dexterity from the increased degree of freedom of robotic instruments, improved field magnification, and threedimensional visualization. These characteristics result in a shorter learning curve for the experienced open surgeon in comparison with the laparoscopic approach.18,19 Reconstructive robot-assisted surgery of the upper urinary track is currently evolving, and cases of ureteral reimplantation, psoas hitch, and Boari flap have been published.2 Nevertheless, the experience with robot-assisted Boari flap ureteral reimplantations is usually limited to a few cases presented along with a larger series of the aforementioned reconstructive procedures3,8,11 (Table 2). Musch and associates3 have reported their results from a series of 16

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cases of distal reconstructive ureteral surgery. Their study included five cases of Boari flap ureteral reimplantation that represent the highest number of cases so far. The operative time for the above five cases ranged between 230 and 320 minutes. One case of prolonged anastomotic leakage and one case of bladder wall insufficiency with urinary leakage and peritonitis were encountered. The current study presents a series of 8 cases of complex ureteral reimplantation by replicating the Boari flap technique of open surgery in the robot-assisted approach. To our knowledge, the number of cases is one of the largest in the literature (Table 2). The operative time of the current study compares favorably with the presented operative time in the literature while the blood loss is also minimal. The complication rate was low and included a case of anastomotic leakage that was detected by cystography on the sixth postoperative day. The latter time point is considered to be early in comparison with the literature, which usually refers to the removal of the catheter on the 7th to 10th postoperative day after the performance of cystography.1,2,4 The current experience showed that the catheter could be removed 1 day earlier in the cases of Boari flaps probably because of the robot assistance allowing high precision during suturing and the combined performance of cystographic evaluation. Currently, there is no study comparing open, laparoscopic, and robotic approaches for the performance of Boari flaps ureteral reimplanatation. Nevertheless, there is one study with data on open, laparoscopic, and robotic approaches for ureteral implantation with a psoas hitch.7 The latter study showed that the robotic approach was associated with lower blood loss and hospital stay in comparison with the conventional laparoscopic and open approach. The above results should be interpreted with care because of the retrospective nature of the above comparison. Another study compared a prospective series of 10 reconstructive procedures of ureteral reimplanation with 10 matched retrospective cases of open ureteral reimplantation.11 The investigators demonstrated significantly less blood loss and hospitalization time for the robot-assisted procedure in comparison with the open approach while the techniques were equally successful in the management of ureteral pathology.

Table 2. Summary of the Current Literature on Robot-Assisted Ureteral Reimplanation with Boari Flap

Report Schimpf and Wagner 2009 [8] Kozinn et al. 201211

Diagnosis Benign strictures, lymphoma, diverticulum, urothelial carcinoma Benign strictures

Benign strictures, Musch megaureter, et al. 20133 urothelial carcinoma

Number of renal units

Boari flap renal units

Other procedures

Operative time for Boari flap cases

11

2

9 reimplantations (3 cases with psoas hitch)

10

2

18 (2 bilateral cases)

2

8 reimplantations (4 cases with psoas hitch) 230–320 min 14 reimplantations (4 cases with psoas hitch), 1 end-to-end anastomosis, 1 ureterolysis and omentum wrap

Complications in Boari flap cases

150 min, External iliac 188 min vein injury (robotic time) (robotic repair) · 1 case Ileus · 1 case Not reported Not reported Prolonged anastomotic leakage · 1, bladder wall insufficiency · 1, urinary tract infection · 2

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Only one and two cases of Boari flap were included in the open and robotic groups, respectively. An interesting technical aspect of ureteral reimplantation techniques is the use or not of an antirefluxing technique (submucosal tunnel) for the implantation of the ureter in the bladder. The laparoscopic and robotic literature includes series of ureteral implantation using an antirefluxing technique or series with direct ureteral implantation without the performance of any antireflux technique.4,8–10,17,20,21 To our knowledge, the literature is lacking comparative studies between the above implantation techniques, and the final selection of the technique for the robotic approach is based on surgeon preference.1 The more challenging nature of the laparoscopic ureteral reimplantation may dictate the direct anastomosis of the ureter to the bladder.1,5 Nevertheless, robot assistance provides the necessary degree of movement that allows the replication of the open surgical approach as described by Politano and Leadbedder.13 Considering the above in conjunction with the experience of the current series, the robotic approach for Boari flap reimplantation is probably an efficient method that is associated with advantages in terms of blood loss, catheterization, and postoperative course in comparison with the open approach. The laparoscopic approach may be related to a higher technical difficulty in comparison with robotics. Nevertheless, only appropriate comparative studies would eventually prove the benefits of the robotic approach. The limitation of the current experience is the lack of cases performed for malignant disease. Several investigators have proposed the performance of ureterectomy for malignant urothelial tumors of the upper urinary track in carefully selected patients.2,3,8 As a result, the presented results should be interpreted on the basis of a reconstructive procedure rather than an oncologic procedure. Nevertheless, the described technique could be used for the excision of malignant tumors with technical modifications such as the excision of the intramural ureter and the careful clipping of the tumor-bearing ureter. Another limitation is the low number of cases, which should be attributed to the rare indication for the performance of a Boari flap for ureteral reimplantation. Moreover, this series of complex reconstructive procedures was performed by surgeons highly experienced in laparoscopy and robotics. Thus, the reproducibility of the same results in terms of the outcome of reconstruction and complications may necessitate significantly higher operative time and probably a similarly high experience. The follow-up period of the current series is limited to 12 months; the follow-up data for a longer period (ie, 24 mos) are available for very few cases, and these data do not show any complications. Prospective studies including larger patient populations and longer follow-up would probably be more appropriate for the extraction of solid results on the robot-assisted technique for Boari flap ureteral reimplantation. Conclusion

The robot-assisted approach is efficient in the performance of ureteral reimplantation with Boari flap. Low blood

DO ET AL.

loss, short catheterization time, low complication rate, and excellent reconstructive outcome are associated with the approach. The presented technique is reproducible and efficient. Nevertheless, a higher number of cases and longer follow-up periods would provide additional documentation and may establish the procedure in the urologic practice. Robot assistance seems to be beneficial for ureteral reconstructive surgery. Disclosure Statement

No competing financial interests exist. References

1. Phillips EA, Wang DS. Current status of robot-assisted laparoscopic ureteral reimplantation and reconstruction. Curr Urol Rep 2012;13:190–194. 2. Stanasel I, Atala A, Hemal A. Robotic assisted ureteral reimplantation: Current status. Curr Urol Rep 2013;14:32–36. 3. Musch M, Hohenhorst L, Pailliart A, et al. Robot-assisted reconstructive surgery of the distal ureter: Single institution experience in 16 patients. BJU Int 2013;111:773–783. 4. Schimpf MO, Wagner JR. Robot-assisted laparoscopic boari flap ureteral reimplantation. J Endourol 2008;22: 2691–2694. 5. Gundeti MS, Kojima Y, Haga N, Kiriluk K. Roboticassisted laparoscopic reconstructive surgery in the lower urinary tract. Curr Urol Rep 2013;14:333–341. 6. McClain PD, Mufarrij PW, Hemal AK. Robot-assisted reconstructive surgery for ureteral malignancy: Analysis of efficacy and oncologic outcomes. J Endourol 2012;26: 1614–1617. 7. Patil NN, Mottrie A, Sundaram B, Patel VR. Roboticassisted laparoscopic ureteral reimplantation with psoas hitch: A multi-institutional, multinational evaluation. Urology 2008;72:47–50. 8. Schimpf MO, Wagner JR. Robot-assisted laparoscopic distal ureteral surgery. JSLS 2009;13:44–49. 9. Uberoi J, Harnisch B, Sethi AS, et al. Robot-assisted laparoscopic distal ureterectomy and ureteral reimplantation with psoas hitch. J Endourol 2007;21:368–373. 10. Yang C, Jones L, Rivera ME, et al. Robotic-assisted ureteral reimplantation with Boari flap and psoas hitch: A single-institution experience. J Laparoendosc Adv Surg Tech A 2011;21:829–833. 11. Kozinn SI, Canes D, Sorcini A, Moinzadeh A. Robotic versus open distal ureteral reconstruction and reimplantation for benign stricture disease. J Endourol 2012;26:147– 151. 12. Becht E, Floth A, Hohenfellner R. Blasenlappenbildung ¨ belho¨r. Aktuel Urol 1988;19:26–32. nach r. U 13. Politano VA, Leadbetter WF. An operative technique for the correction of reflux. J Urol 1958;79:932–941. 14. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: A new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004;240:205–213. 15. Modi P, Goel R, Dodiya S. Laparoscopic ureteroneocystostomy for distal ureteral injuries. Urology 2005;66:751– 753. 16. Nezhat CH, Malik S, Nezhat F, Nezhat C. Laparoscopic ureteroneocystostomy and vesicopsoas hitch for infiltrative endometriosis. JSLS 2004;8:3–7.

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17. Rassweiler JJ, Gozen AS, Erdogru T, et al. Ureteral reimplantation for management of ureteral strictures: A retrospective comparison of laparoscopic and open techniques. Eur Urol 2007;51:512–522. 18. Chang L, Satava RM, Pellegrini CA, Sinanan MN. Robotic surgery: Identifying the learning curve through objective measurement of skill. Surg Endosc 2003;17:1744–1748. 19. Yohannes P, Rotariu P, Pinto P, et al. Comparison of robotic versus laparoscopic skills: Is there a difference in the learning curve? Urology 2002;60:39–45. 20. Gozen AS, Cresswell J, Canda AE, et al. Laparoscopic ureteral reimplantation: Prospective evaluation of mediumterm results and current developments. World J Urol 2010; 28:221–226.

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Address correspondence to: Evangelos Liatsikos, MD, PhD Department of Urology University of Patras Medical School Rion 26 504, Patras Greece E-mail: [email protected]

Robot-assisted technique for boari flap ureteral reimplantation: is robot assistance beneficial?

Ureteral reconstructive surgery necessitates adequate exposure of the ureteral lesion and results in large abdominal incisions. Robot assistance allow...
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