Is the Laparoscopic Technique Feasible for ...

Original Article

Is the Laparoscopic Technique Feasible for Performing Ileal Ureter? A Survival Porcine Study Sheng-Long Hsu, Allen W. Chiu1,2,4,5, Victor C. Lin1, Chun-Chieh Wang1, Ying-Huei Lee1, Jyh-Jann Lin2, Ching-Nan Lin3 , Chien-Feng Li3, Chin-Li Lu2 Division of Urology, Department of Surgery, Chiali General Hospital, Tainan; Division of Urology, Department of Surgery, 2Department of Medical Research, 3 Department of Pathology, Chi Mei Medical Center, Tainan; 4 Department of Urology, Taipei Medical University, School of Medicine, Taipei; 5 Taipei City United Hospital, Taipei, Taiwan, R.O.C.

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OBJECTIVE: Ileal-ureteral substitution is a viable surgical procedure to provide a satisfactory solution to the problem of an extensive ureteric defect. We attest to the feasibility of a laparoscopic technique to perform a total ileal-ureteral substitution with and without an antireflux implantation procedure in a porcine model. MATERIALS AND METHODS: With the transperitoneal approach, laparoscopic harvesting of a segment of the ileum and extracorporeal reconstruction of the ileum as a total substitute for the ureter, followed by pyeloileal and ileovesical anastomoses with intracorporeal laparoscopic suturing were performed in 8 pigs (average weight 28 kg). Ileal-ureteral substitution with no antireflux implantation technique was performed as the control model in 2 pigs, and ileal-ureteral substitution with the ileal nipple method or intussusception method was performed in 3 pigs. We completed the above-mentioned procedures without using any automatic anastomosing device intracorporeally or extracorporeally. Perioperative serum creatinine, electrolytes, blood gas, and a follow-up excretory urogram, cystogram, and pathological examination were used to assess the surgical outcome. RESULTS: The total operative time was 6.5 to 11.5 (average, 8.2) hours. A patent ileal ureter from the kidney to the urinary bladder was found in all animals except 2. However, a high rate of postoperative complications occurred; most complications occurred at the pyeloileal anastomotic sites with various degrees of hydronephrosis: 25% (2/8) of cases showed severe narrowing and 50% (4/8) of cases showed mild stenosis. Other complications included partial or total dysfunction of the antireflux procedures in 50% (3/6) and 16.7% (1/6) of cases, respectively. CONCLUSIONS: This study showed that laparoscopic ileal ureter reconstruction is not yet viable in small animals like pigs with an average weight of 28 kg. High failure rates (25%) and stenotic rates (75%) were found. Further refinement of the suturing technique in studies using larger animals is required before the actual clinical application of laparoscopic total ileal ureter substitution can be realized. (JTUA 15:159-66, 2004) Key words: laparoscopy, ileal ureter.

Traditionally, the surgical treatment of patients with extensive damage to the ureter includes a Boari flap with a psoas bladder hitch, downward mobilization of

INTRODUCTION

Received: June 15, 2004

Revised: July 15, 2004

Accepted: Aug. 10, 2004

Address reprint requests and correspondence to: Dr. Sheng-Lung Hsu Division of Urology, Department of Surgery, Chiali General Hospital, No. 606 Singhua, Jiali, Tainan 722, Taiwan, R.O.C. 台灣泌尿醫誌第十五卷第四期（93 年 12 月）

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Is the Laparoscopic Technique Feasible for Performing Ileal Ureter? A Porcine Survival Study

the involved kidney for lengthening of the ureter, a transureteroureterostomy, renal autotransplantation, and an elective nephrectomy. When extensive loss of the ureter occurs secondary to irradiation, surgical complications, or various pathological conditions, segmental or complete ureteral replacement is indicated as a salvage procedure. In the last decade, laparoscopic urology has experienced unprecedented growth, and indications for laparoscopic urology are ever increasing. Initial clinical applications were for simple extirpative procedures. With increasing experience, urologists with laparoscopic expertise have begun to perform reconstructive procedures. Ileal-ureteral substitution is a viable procedure to replace a long segment of a ureteral defect. This operation was first described by Schoemaker in 1906. To the present, it is still a good solution for extensive ureteric defects. The feasibility of using laparoscopic techniques to perform ileal-ureteral substitution is still being questioned. In the literature, only 1 case of laparoscopic ileal-ureteral substitution has been reported by Gill et al.[1] In this study, we attempted to refine the surgical guidelines for laparoscopic ureter substitution in an animal model before clinical application.

MATERIALS AND METHODS From March to October 2003, the feasibility and reproducibility of the laparoscopic technique for performing ileal ureter were investigated in a porcine study. Seventeen pigs underwent unilateral (left) laparoscopic ileal-ureteral substitution. Eight pigs (6 males and 2 females) with an average weight of 28 (range, 22~32) kg received the above procedure and completed the follow-up studies. Two ileovesical anastomoses were performed with no antireflux procedure (group 1), 3 were performed using the nipple method, and 3 were performed with an intussuscepted valve (group 2). Preoperative preparations. After 3 days of fasting, anesthesia was induced by intravenous administration of 30 mg/kg Pentothal after an intramuscular injection of 10 mg/kg ketamine sedation; Proper anesthetic depth was maintained by isoflurane inhalation. Before surgery, arterial gas was analyzed, and a venous blood sample was obtained to measure serum creatinine and electrolytes. Cefazolin (500 mg) was administered intravenously for infection prophylaxis. Surgical techniques. The procedure was composed of 2 parts: (1) ileal ureter preparation and bowel reconstruction through a minilaparotomy for isolation of a selected ileal segment and reestablishment of ileal con-

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Fig. 1 Bowel diversion (black arrow) and ileal continuity reestablishment (white arrow) through an extended umbilical trocar wound. tinuity; and (2) urinary diversion (isoperistaltic) with intracorporeal suturing to accomplish the pyeloileal and ileovesical anastomoses. The laparoscopic approach was used via a transperitoneal route with 3 to 4 ports. After pneumoperitoneum was created, 3 ports were made; including a 10-mm port above the umbilicus and another two 10-mm ports in the left upper and lower quadrants, respectively. At first, the small intestine was traced distally to the ileocecal junction, and a segment of 15 cm of the ileum distal to the ileocecal junction was identified. The distal margin of the ileal segment was marked with a superficial electrocautery burn. The umbilical port site incision was extended to 2 cm. The preselected segment of the ileum was exteriorized through the 2-cm extension wound of the supraumbilical port site. A 20~25-cm ileal segment proximal to the electrocautery mark was divided and harvested by a conventional open technique with preservation of its vascular supply. Bowel-to-bowel continuity was restored extracorporeally by the traditional hand-sewn method with 3-O Vicryl suturing (Fig. 1). The bowel and the isolated ileal segment were then maneuverized into the abdomen and the enlarged wound was closed in an airtight manner by purse-string suturing. The free ileal segment was used as a substitute for the ureter in an isoperistaltic fashion. The antireflux nipple was constructed by incising the antimesenteric border distally for about 5~6 cm and tapering and folding it back like a split cuff to make an everted opening (Fig. 2). The intussuscepted valve was constructed by stripping 3 supply vessels of the distal portion of the isolated ileal segment, and this was maintained with 2 rows of silk sutures.

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SL Hsu, AW Chiu, VC Lin, et al.

Fig. 2 Distal tapering of the isolated ileal segment and construction a nipple with the split-cuff technique. Pneumoperitoneum was reestablished, and the Toldt line beside the left colon was incised. The left ureter was identified and traced cephalad to renal pelvis. A left total ureterectomy was performed, and the distal end was ligated with endoclips and then transected. The renal pelvis was anastomosed end-to-side with the isolated ileal segment. Pyeloileal anastomosis was begun with 2 stayed ligatures over both ends, and then posterior wall suturing and anterior wall suturing were sequentially performed. A buttonhole of the bladder muscle and its mucous membrane were excised by an electrocautery device. The nipple was shoved into this opening to make it protrude into the bladder cavity. The circular basis of the nipple was then anchored to the bladder wall by interrupted Vicryl stitches. Postoperative care. All animal were monitored

overnight. Cefazolin (500 mg) and metronidazole (500 mg) twice daily were given for 1 week postoperatively. Intravenous lactacted Ringer’s solution was maintained at 2000 ml/day throughout 7 days of the postoperative fasting period. Follow-up. One week after the open cystostomy with removal of the double-J catheter, the follow-up study began. Antegrade urinary flow was investigated by intravenous urography in all animals. The capacity of the antireflux nipple or the intussuscepted valve to prevent reflux was checked by cystography which was performed when the bladder was filled with 300~400 ml of opaque material or until the animal spontaneously urinated. Then, the animals were euthanized for necropsy assessment. The kidney, ileal ureter, and anastomosed sites were grossly examined, and microscopic sections were obtained for histopathological evaluation.

RESULTS Eight animals which survived postoperatively were enrolled in our study. The average follow-up period was 9 (range, 3~15) weeks. The average operative time was 8.2 (range, 6.5~11.5) hours. Six (75%) animals achieved urinary drainage from the kidney to the bladder. The major delayed postoperative complication was pyeloileal stenosis which was proven by intravenous urography and necropsy findings. Two (25%) of them had severe stenosis and 4 (50%) had mild stenosis (Table 1). For evaluating the results of the pyeloileal anastomosis, we defined blunting of the renal calyces after contrast injection as mild stenosis and failure of contrast drainage from the kidney to the bladder or obvious fullness and enlargement of renal pelvis and calyces as severe steno-

Table 1. Delayed complications Group 2 Complication

Pyeloileal stenosis, mild Pyeloileal stenosis, severe Failure of contrast from kidney to bladder Total dessusception of the antireflux mechanism Partial dessusception of the antireflux mechanism Metabolic acidosis (pH < 7.20 )

台灣泌尿醫誌第十五卷第四期（93 年 12 月）

Group 1 (2 cases) 1 1

1 1 1

Intussuscepted method (3 cases) 3 0 -

-

1

-

1

-

1

2

3

1

-

1

2

Nipple method (3 cases)

Total (6 cases) 4 2 2

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Fig. 3 The intact ileal nipple (left) and cystography (right) showing a nipple filling defect (arrow). sis. Owing to the limited number of cases in our study, we used the Wilcoxon signed-rank test to compare renal function between preoperative and postoperative data after excluding 3 with no available preoperative data or with severe pyeloileal stenosis. The comparison revealed a p value of 0.043 (< 0.05) (Table 2). The postoperative renal function test was significantly higher than the preoperative data but just marginally so. In the antireflux group, 2 (33.3%) of them were free of reflux, of which 1 had the nipple method (Fig. 3) and

another with the intussuscepted valve (Fig. 4). One (16.7%) of them developed total dessusception in the antireflux mechanism. Three (50%) of them experienced partial dessusception of the antireflux mechanism. Mild vesicoureteral reflux in spite of an intact antireflux mechanism was observed in 2 cases. Two animals (25%) developed metabolic acidosis (pH < 7.2), and no case had an electrolyte imbalance. The histological examination showed good healing, a patent pyeloileal anastomosis, and an intact ileal nipple

Table 2. Follow-up of renal function Subject no. BUN0 (mg/dL)

1*

2*

3

4

5*

6

7

8

-

-

15

11.3

11.1

13.6

11.4

8

p Value

0.043* BUN1

Creatine0 (mg/dL)

17.2

21.0

17.6

17.8

13.1

35

29.3

13

-

-

1.4

1.17

1.58

1.47

1.10

1.6 0.043*

Creatine1

2.28

2.50

2.63

2.2

2.08

2.1

2.02

1.9

Wilcoxon signed-rank test * Excludes subjects 1, 2 , and 5. BUN0, Creatine0: preoperative data. BUN1, Creatine1: postoperative data. Subjects 1 and 2 had no available preoperative data. Subjects 1 and 5 had severe pyeloileal stenosis.

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Fig. 4 Intact intussuscepted ileal valve and good healing of the ileovesical anastomosis. protruding into vesical lumen in those 2 successful cases (Fig. 5). All cases of our study also revealed good healing of the ileovesical anastomoses. No ileovesical obstruction was noted in any animal in this study. All of the ipsilateral kidneys revealed no obvious inflammation regardless of the seriousness of the pyeloileal stenosis postoperatively. Only 1 case in our early study revealed renal pelvis mucosa protruding into the lumen of the pyeloileal anastomosis which caused total occlusion of the pyeloileal anastomosis.

DISCUSSION When ureteral length is severely compromised and cannot be restored with original urinary tract tissues, intestinal ureteral substitution is a favored management

Fig. 5 Intact ileal nipple protruding into the vesical lumen showing good healing of the ileovesical anastomosis. (x12.5)

台灣泌尿醫誌第十五卷第四期（93 年 12 月）

technique. Indications for ureteral substitution include bilateral ureteral cancer, an iatrogenic ureteral fistula after surgery, ureteral stricture after recurrent stone disease, ureteral stricture after radiation, persistent stricture after treatment of retroperitoneal fibrosis, etc. Properties of the ileum which make it suitable for ureteral substitution are its form, its peristaltic activity, its rich blood supply, a long mesentery, and its adaptability for resection of a portion with restoration of continuity [2]. To date, laparoscopic reconstruction for urinary diversion with the bowel has used 1 of the following 3 approaches: (1) extracorporeal suturing outside the port site; (2) bowel diversion through a minilaparotomy and urinary diversion with intracorporeal suturing; and (3) pure intracorporeal suturing [3]. Exteriorization of the bowel through a small skin incision for purposes of bowel exclusion and reanastomosis is an acceptable component of "laparoscopic" colon surgery [1]. In this study, we used an extended trocar wound (2 cm) to exteriorize the isolated ileal segment without difficulty. We further observed that when the color of the isolated bowel changed or when return of the bowel into peritoneal cavity was difficult, the wound had to be further extended to avoid bowel congestion. This approach provides several advantages including that associated with bowel procedures like tapering, intussusception, and the antireflux nipple which can be performed using a handy open surgical technique and that irrigation of the isolated bowel segment can be performed outside the body with no peritoneal contamination [4]. The bowel segment acts as a bumper protecting the kidney from the higher pressures in the bladder. Active peristalsis of the ileum may prevent transmitted pressures reaching as high as the renal pelvis. Reflux appears to have no detrimental effect on renal function in adults with ileal ureters, and therefore, an antireflux procedure might not be necessary [5]. However, some authors still advocate maintaining a normal low-pressure bladder [2]. In young patients with potential longevity, it is important to perform the anastomosis via an antireflux technique to prevent infection and upper tract deterioration. In our antireflux group, although only 2 (33.3%) were successful and 3 (50%) had partial dessusception of the antireflux mechanism, this is compatible with findings from previous reports. Gupta et al. stated that a split-nipple valve or intussuscepted terminal ileum prevents reflux in 60%~70% of cases. Well-vascularized nipple of 3 cm or longer is sufficient to create an antireflux mechanism [6]. Skinner et al. even mentioned nipples of 5 cm or longer. A longer spatulation producing a longer ureteral nipple may be advisable for an adequate antireflux mechanism. Stripping and tapering of the distal isolated ileal segment which leaving a 1-cm strip of 163


the mesenterium for antireflux purposes achieves the desired result without vascular compromise. The edges of the isolated ileal segment should diverge at the base of the cuff to prevent circular constriction [7]. Intussusception of the ileal wall can be used, but a proper technique must be chosen to prevent necrosis. Dessusception remains the most-frequent complication of an intussuscepted nipple valve [8]. While the natural tendency of an intussuscepted segment of bowel is not to dessuscept, distension of the intraluminal segment where the nipple or intussusception is placed, if severe enough, will force dessusception. Therefore, the possible morbidity of any antireflux procedure must be carefully weighed against the potential benefits. In the cases of this study, results of the postoperative renal function test were significantly higher than the preoperative data but just marginally so. Stenosis at the pyeloileal junction was responsible for a deteriorated renal function after ileum interposition. Obstruction is the major cause of renal damage following urinary diversion, while reflux in a low-pressure system is not dangerous [9]. Stenosis of the pyeloileal anastomosis might have been due to our immature techniques of intracorporeal suturing, especially due to the smaller size of the normal porcine renal pelvis. One pathological result in our study showed that a piece of urothelium of the renal pelvis had entered the lumen of the pyeloileal anastomosis. This was the only instance in this early animal model. Inaccurate mucosa-to-mucosa anastomosis was seen in that subject. So, greater precision in creating the ureterointestinal anastomosis with sutures being placed under direct vision is important. The histological examinations of the ipsilateral kidneys of all subjects revealed no obvious inflammation regardless of the seriousness of the pyeloileal stenosis. This revealed that inflammation itself was not the cause of the pyeloileal stenosis. However, the most important cause for our unsatisfactory results was likely associated with no proper provision for urinary diversion immediately after the operation to protect the anastomosis. As known from porcine model studies, the anatomic structure of the porcine urethra is elongated and spiral, especially in males and greatly differs from that of the human. It is impossible to catheterize a male pig through the penile urethral opening. Catheterization has to be performed percutaneously in the perineal urethra [10]. We previously attempted antegrade insertion of a catheter or a guide wire through the opening in the dome of urinary bladder but ultimately failed. In the conventional open method of an ileal-ureteral substitution, urethral catheterization or even a percutaneous nephrotomy may be required. Otherwise, urine leakage immediately after the operation may result in peri-anastomosis fibrosis and progressive 164

stenosis later. These observations invite urological surgeons to search for a more-suitable study method in the porcine model. Larger female pigs may be an ideal animal model for future studies. There is no assurance that the lymphoid depletion induced by direct contact of urine with the intestinal mucosa will not affect any segment of the intestinal tract used as a urinary conduit, as was reported by Tapper and Folkman [11]. In addition, we found that the pyeloileal anastomosis might be under some tension when the isolated ileal segment overstrides the colon according to the necropsy examination. In our study, only 1 subject was retroperitonealized. We thus suggest that when possible, it is preferable to retroperitonealize the intestinal segment. However, whether proximal ligation of the vascular pedicle of the colon can be accomplished as successfully with laparoscopy is yet unproven [12]. Mannsson el al. reported ureterointestinal anastomoses with an incidence of approximately 29% of some form of obstruction over the long term [13]. The most-challenging part of the procedure is the free-hand intracorporeal suturing for pyeloileal and ileovesical anastomoses. Although several suturing and tying devices are currently available for laparoscopic use, laparoscopic free-hand suturing with knot tying is a technique that can gradually be learned through experimental training. It is cost-effective as well as very important and essential for reconstructive laparoscopic surgery. We completed the entire procedures without using any GIA device intracorporeally or extracorporeally in order to save the study budget. The average operative time of the entire procedure in our study was excessive. It requires patience and diligence. The development of laparoscopic stapling instruments permits the application of techniques for intestinal anastomoses during exteriorization of the bowel which may shorten operative times. Moreover, as experiences accumulate, we believe decreases in operative times will be achieved. Although there have been numerous reports on the successful use of the open ileal ureter operation, incorporation of the intestine in the closed urinary tract is not universally accepted. The main criticism related to this use of the ileum for ureteral replacement has been the development of intestinal stricture, with its concomitant difficulties in creating an adequate antireflux mechanism [7]. Tanagho stated that isolated bowel segments can successfully be used as conduits for urinary diversion, with limited morbidity. However, these segments do not work as well when incorporated in a closed system because the bowel segment is subjected to totally different hydrodynamics and the variable high intraluminal pressures of the urinary system. The bowel segment assumes JTUA Vol.15 No.4, Dec. 2004


a partial reservoir function which means that a large mucosal area is exposed to urine [14]. This may help explain the occurrence of metabolic acidosis (pH < 7.2) at follow-up in 2 (25%) of the pigs in our study, although no case had an electrolyte imbalance. Therefore, ileal-ureteral substitution is still an alternative option as a salvage procedure for a long-segment ureteral loss, but it should only be used as a last resort. Advances in laparoscopy for surgical repair of the ureter have encouraged urologists to perform laparoscopic ileal ureter. However, Kaouk and Gill still classified it into a clinically evolving category [15]. An ileal ureter may be performed laparoscopically, but it remains an invasive procedure [16]. It is a technically demanding procedure that requires extensive experience in laparoscopic surgery and the use of "state-of-the-art" technology with extreme care to solve a series of difficult surgical problems.

CONCLUSIONS Pyeloileal stenosis was the major delayed complication of laparoscopic ileal ureter in our study. Seeking a suitable method of immediate postoperative bladder urinary diversion in the porcine model is necessary to protect the pyeloileal and ileovesical anastomoses. Further refinement in suturing techniques in a study using larger animals is required. The possible morbidities of any antireflux procedure used must be carefully weighed against any potential benefits. Intracorporeal free-hand suturing is important and essential for reconstructive surgery. Our study revealed that the advanced reconstructive laparoscopic procedure is not always reproducible in less-experienced hands. There are many technical problems to be resolved as shown in this animal study. Clinical application of the procedure is technically demanding and has not matured at the present time with current amateurish laparoscopic techniques.

ACKNOWLEDGEMENTS

genic ureteropelvic junction and upper ureteric obstruction - a long-term follow-up. Indian J Urol 1997;13(2):79-83. 3.Gupta NP, Gill IS, Fergany A, Nabi G. Laparoscopic radical cystectomy with intracorporeal ileal conduit diversion: five cases with 2-year follow-up. BJU Int 2002;90:391-6. 4.Gill IS, Rackley RR, Meraney AM, Marcello PW, Sung GT. Laparoscopic enterocystoplasty. Urology 2000;55(2):178-81. 5.Waldner N, Hertle L, Roth S. Ileal ureteral substitution in reconstructive urological surgery: Is an antireflux procedure necessary? J Urol 1999;162:323-6. 6.Janknegt RA. Construction of ileal nipples as anti-reflux valve technique. Eur Urol 1988;14:46-9. 7.Bejany DE, Lockhart JL, Politano VA. Ileal segment for ureteral substitution or for improvement of ureteral function. J Urol 1991;146:302-5. 8.Gosalbez R Jr, Gousse AE. Reconstruction and undiversion of the short or severely dilated ureter: the antireflux ileal nipple revisited. J Urol 1998;159:530-4. 9.Benson MC, Seaman EK, Olsson CA. RE: The ileal ureter neobladder is associated with a high success and a low complication rate. J Urol 1997;157:2266. 10.Swindle MM, Smith AC, Hepburn BJS. Swine as models in experimental surgery. J Invest Surg 1988;l(l):65-79. 11.Tapper D, Folkman J. Lymphoid depletion in ileal loops: mechanism and clinical implications. J Ped Surg 1976;11(5):871-80. 12.Pandya S, Murray JJ, Coller JA, Rusin LC. Laparoscopic colectomy. Arch Surg 1999;134:471-5. 13.Walsh PC. Campbell's urology. 6th ed. Philadelphia, PA:WB Saunders, 1992:2614-9. 14.Tanagho EA. A case against incorporation of bowel segments into the closed urinary system. J Urol 1975;113:796-802. 15.Kaouk JH, Gill IS. Laparoscopic reconstructive urology. J Urol 2003;170:1070-8. 16.Desgrandchamps F. Endoscopic and surgical repair of the ureter. Curr Opin Urol 2001;11:271-4.

This study was supported by the Fund of Chiali General Hospital and the animal laboratory of Chi-Mei Medical Center.

REFERENCES 1.Gill IS, Savage SJ, Senagore AJ, Sung GT. Laparoscopic ileal ureter. J Urol 2000;163:1199-202. 2.Gupta NP, Chahal R, Wadhwa SN. Ileal substitution as a salvage procedure in the management of iatro台灣泌尿醫誌第十五卷第四期（93 年 12 月）

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