Urological complications in 980 consecutive patients with renal transplantation

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1 Blackwell Publishing AsiaMelbourne, AustraliaIJUInternational Journal of Urology Blackwell Publishing Asia Pty Ltd Original ArticleUrological complications of renal transplant HR Davari et al. International Journal of Urology (2006) 13, doi: /j x Original Article Urological complications in 980 consecutive patients with renal transplantation HAMID R DAVARI, 1 HOOMAN YARMOHAMMADI, 1 SEYED A MALEKHOSSEINI, 1 HESHMATOLLAH SALAHI, 1 ALI BAHADOR 1 AND MEHDI SALEHIPOUR 2 1 Division of Surgery and 2 Division of Urology, Organ Transplant Research Center, Nemazee Hospital, Shiraz University of Medical Sciences, Shiraz, Iran Aim: To present the urological complications of renal transplantations performed in the last 14 years at one center and to briefly explain a modified method of Lich Gregoir ureteroneocystostomy. Methods: The data of 980 patients receiving kidney transplants at the authors' institution from April 1991 to February 2004 were reviewed in a retrospective prospective study. In particular, surgical techniques and urological complications were noted. Results: A total of 980 patients had received kidney transplantation. Extravesical ureteroneocystostomy (Lich Gregoir method) was used in the first 480 patients (group A). In the subsequent 500 patients, the authors' modified method of extravesical ureteroneocystostomy, using single layer anastomosis and small feeding tubes as stent, was used (group B). Overall urological complication rate was 2.8% (28 patients), including leakage (13 patients, 1.3%), stenosis (seven, 0.7%), obstruction (one, 0.1%), distal ureter necrosis (four, 0.4%), pelvocalyceal fistula (two, 0.2%) and implantation of ureter into the peritoneum (one, 0.1%). Urological complications were significantly more common in group A compared to group B (16, 3.3% and 9, 1.8%, respectively; P < 0.05). Conclusions: Preserving the adventitia, fat and blood supply of the ureter by delicate dissection of the ureter during donor nephrectomy, short ureters, and fixation of the adventitia, fat and blood supply of the ureter to the bladder wall, to prevent kinking or twisting, are important factors in decreasing urological complications. Additionally, the authors' method of ureteroneocystostomy is also effective in decreasing the incidence of ureteric complications. Key words kidney transplant, Lich Gregoir, ureteroneocystostomy, urological complications. Introduction Ureteric complications make up more than 90% of urological problems after transplantation, and can lead to significant morbidity and mortality. 1 3 The most frequent urological complications after renal transplantation are leakage, stenosis, and reflux with a frequency of 1 30% in different series. 1 3 The most important factor associated with this rate is the method of ureteroneocystostomy performed during transplantation. 3 The risk of complications has significantly decreased during the last few decades, from 20% in the 1970s to 5% in the 1990s, most probably due to use of a short ureter surrounded by its fat and to extravesical Lich Gregoir ureteroneocystostomy becoming the preferred technique. 4 Several techniques for vesico-ureteral anastomosis have been described and information on the success rate of these methods is important in preventing post-transplant complications and securing a functioning transplant. 5 7 Correspondence: Hooman Yarmohammadi MD, Department of Surgery, Faghihi Hospital, Zand Avenue, PO Box , Shiraz, Iran. yarmohml@sums.ac.ir Received 18 May 2005; accepted 15 March In the Shiraz University transplant center, extravesical ureteroneocystostomy (Lich Gregoir) technique was used from 1991 to ,6 After 1998 we used a modified version of the Lich Gregoir method. The aim of this study was to compare the urological complications in our renal transplant patients who had undergone ureteroneocystostomy via different techniques. Methods The data of 980 patients receiving kidney transplants at our institution from April 1991 to February 2004 were reviewed in a retrospective prospective study. Any urological complications, including leakage, stenosis, obstruction, and symptomatic reflux, were determined with attention to different techniques of vesico-ureteral anastomosis. In all patients, the harvesting and transplantation procedures were performed according to the usual technique. Cyclosporine, azathioprine, and low dose steroid were used as immunosuppression in all transplantation recipients but in recent years some patients had received tacrolimus and mycophenolate. There were 114 grafts (11.6%) from cadaver donors and 866 (88.4%) from living donors.

2 1272 HR Davari et al. The 980 patients were divided into two groups according to the method of ureteroneocystostomy procedure utilized. Group A consisted of those with the extravesical ureteroneocystostomy (Lich Gregoir) technique, used from 1991 to 1998 (first 480 patients). 6 Stent was only used in selected cases, such as diabetes or when the ureter blood supply was insufficient after harvesting. Group B consisted of the last 500 patients, from 1999 to 2003, in whom our modification of extravesical ureteroneocystostomy with stenting and without antireflux procedure was used (modified Lich Gregoir). Modified Lich Gregoir surgical technique During harvesting we emphasized meticulous dissection of adventitia and blood supply of the ureter and preserving gonadal vein continuity with preservation and sequential anastomosis of accessory renal artery to external iliac artery. The procedure is as follows: After declamping, perfusion of allograft and ureter are checked. A small feeding tube size 5 or 6 is gently placed in the ureter. The ureter is spatulated in the antimesentric side. Vesico-ureteral anastomosis is done in a single layer approximating full thickness of the ureter to the bladder muscle using synthetic absorbable suture 5/0 without any antireflux procedure (Fig. 1). The length of ureter is adjusted when the posterior line of anastomosis is completed. Only mucosa of the ureter is severed and excess adventitia and blood supply of the ureter are left intact. Usually a length of cm of ureter is adequate. The stent is fixed to posterior mucosa of bladder with a chromic 4/0. Excess length of stent is severed with the remaining 5 6 cm of its length and is placed in the bladder. When anastomosis is completed the adventitia and blood supply of the ureter at the site of gonadal vein ligature is fixed by an absorbable U-stitch to the anterior Fig. 1 A small feeding tube size 5 has been gently placed in the ureter. Ureter is spatulated in the antimesentric side. Vesico-ureteric anastomosis in a single layer approximating full thickness of ureter to bladder muscle using synthetic absorbable suture 5/0 without any antireflux procedure is performed. edge of the bladder incision. This fixation is done to prevent kinking or twisting of the ureter and also functions as a tissue to support the anastomosis. The indwelling internal folly catheter is removed within 2 3 days when urine output has decreased to less than 4 5 L. Homovac, which is placed retroperitoneally, is removed when drainage is less than 20 ml per day. It can usually be removed in non-complicated cases in the first week. Ureteral stent is removed after 3 weeks. In patients with urinary tract infection when medical treatment for 48 h fails or the patient has fungal infection it is removed earlier. Patients were evaluated for kidney function by ultrasonography on days 1 and 7, and at 1, 3, 6 and 12 months. Routine urine culture was done every other day for 2 weeks and at 1, 3, 6 and 12 months. In patients with urinary leakage, the drain and internal folly was left in place and if they had been removed were reinserted. A catheter was also guided by ultrasound and placed in the fluid collection. After a short period, usually less than 1 month, of conservative treatment exploration was performed. Re-implantation or relief of the obstruction was the preferred procedure; however, in selected cases, uretero-ureteral or pyelo-ureteral anastomosis was performed. Results There were 114 grafts (11.6%) from cadaver donors and 866 (88.4%) from living donors. The mean age of the patients was 31.2 ± 11.8 years (range, years). There were 677 (69%) male patients and 303 (31%) female patients. All the patients had 1 year or more post-transplant follow-up. There were urological complications in 28 (2.8%) of the recipients. Thirteen (1.3%) of these patients had urinary leakage, seven (0.7%) had urinary stenosis and one (0.1%) had urinary obstruction due to urethral stricture. Four (0.4%) patients developed distal ureter necrosis, two (0.2%) patients had pelvocalyceal fistula, and in one (0.1%) patient implantation of ureter to peritoneum was observed. Revision of anastomosis was done in 15 (1.5%) patients, uretero-ureteral anastomosis in one (0.1%), pylo-ureteral anastomosis in two (0.2%), and new site of ureteroneocystomy in seven (0.7%). Spermatic cord and adhesions were released in two (0.2%) patients. One patient responded to external drainage 9 months after detection of his urinoma. In another patient, ureterovesical stenosis was treated with a double-j stent after removal of a stone in the pelvis of the allograft kidney. One patient with anastomosis of the ureter to the peritoneum was treated with ureteroneocystomy, after evacuation of 9 L of ascitic fluid. The type of operations and treatments for urological complications are shown in Table 1. Urological complications in the two groups are shown in Table 2. Urological complications occurred in 16 (3.3%) patients of group A, and 9 (1.8%) in group B (Table 2). Urological complications were significantly more common in group A compared to group B (P < 0.05).

3 Urological complications of renal transplant 1273 Table 1 Type of operations and treatments for urological complications in 980 patients receiving renal transplant Type of operation No. patients (%) Revision of ureteroneocystostomy 15 (1.5) Pyelo-ureteral anastomosis 2 (0.2) Uretero-ureteral anastomosis 1 (0.1) New site of ureteroneocystostomy 7 (0.7) ± division of spermatic cord External drainage 1 (0.1) Repair of peritoneum and 1 (0.1) ureteroneocystomy Total 28 (2.8) Table 2 Frequency of urinary complications in patients receiving renal transplant Complication Group A (n = 480) Discussion Urological complications following renal transplantation cause significant morbidity and may result in failure of the allograft or even death. Urinary tract reconstruction is usually done by antireflux ureteroneocystostomy and has become the preferred method of urinary tract reconstruction in renal transplant recipients because of the relatively low incidence of postoperative fistula formation and urinary tract obstruction. 8,9 The risk of urological complications has significantly decreased during the last few decades (from 29% in the 1970s to 5% in the 1990) due to use of a short ureter surrounded by its fat and because of the non-stented extravesical Lich Gregoir procedure. 1 4,9 11 Uretero-ureteral anastomosis and ureteropylostomy may be better than ureterovesical anastomosis, but they leave far fewer options if problems occur. 9 Therefore pyeloureterostomy and uretero-ureterostomy are usually reserved for patients with short or ischemic allograft ureter or for patients with very limited bladder capacity. The major factors influencing the success of ureteroneocystostomy include: the vascular integrity of the donor ureter, the anastomotic technique employed, and the avoidance of technical mishaps such as kinks and twisting of the ureter. 11 At many transplantation centers, experience has led surgeons to adopt extravesical ureteroneocystostomy Group B (n = 500) P-value Urinary fistula 8 6 NS Stenosis 3 1 <0.05 Obstruction 1 0 NS Distal ureteral necrosis 2 0 <0.05 Pelvocalyceal fistula 1 1 NS Accidental anastomosis 1 0 NS of ureter Total 16 9 <0.05 Group A, Lich Gregoir technique; Group B, modified Lich Gregoir technique; NS, not significant. procedures such as the modified Lich Gregoir technique in place of the Politano Leadbetter method. 12 Each of these methods has advantages but also drawbacks; the Lich Gregoir technique saves time but is not particularly effective for preventing reflux, while the Politano Leadbetter approach effectively prevents reflux but requires more difficult exposure and longer operative time. The Lich Gregoir and Politano Leadbetter approaches are used either with or without a temporary ureteral stent. A modified method, which incorporates advantages of both the Lich Gregoir and the Politano Leadbetter methods, has been used at our institute with the goals of preventing stricture/stenosis and postoperative complications. At our center, we used the technically easier extravesical Lich Gregoir procedure after the first 20 kidney recipients, who were treated with the Politano Leadbetter method. Lich Gregoir was easy to perform, did not necessitate a large cystostomy, and required a shorter ureter when compared with transvesical approaches. Stent was used in selected cases such as diabetics or those in whom the ureter blood supply was insufficient after harvesting. Urinary leakage rate was 3.3%. After 1998, we used our modified version of the Lich Gregoir method and the results obtained show that the complication rate decreased. We modified the Lich Gregoir technique by using single layer anastomosis of full thickness of detrusor and ureter wall, small feeding tube for stenting in all cases, ureter as short as possible and fixation of adventitia, fat and blood supply of the ureter to the bladder to prevent kinks and twists. We did not use any antireflux procedure. The incidence of urinary complications decreased to 1.8%. Our urological complication rate was lower than other figures previously reported. 1 4,13,14 One important reason for the observed lower rate of complications compared to the conventional method may be the meticulous dissection of the adventitia, fat and blood supply of the ureter and utilization of a shorter ureter. In this way we prevented ischemic damage to the ureter and minimized the risk of kinking or twisting. The latter two have been reported to be the main problems in obtaining lower rates of post-transplant complications. The other important reason we suggest is the use of a stent in all patients. It has been shown previously that stenting can decrease complication rates by supporting the anastomosis and preventing twisting and kinking of the ureter. Controversy in using ureteral stent exists. 11,12 Gedroyc et al. compared 78 grafts without and 84 with a Double-J stent and noted seven fistulas and eight cases of stenosis in the group without a stent and no fistulas and only one case of stenosis in the group with a stent. 15 Benoit et al. obtained an 8% rate of urinary complications in the group without a stent as compared with a 1% in patients with stent in two randomized groups of kidney grafts with an ureterovesical anastomosis. 16 Others studying the prophylactic insertion of a Double-J ureteral stent in kidney transplantation reported the same result. 17 Bergmeijer et al. retrospectively studied 36 pediatric renal transplant recipients of whom 18 had stents. 18 They reported three leaks and three obstructions in the non-stented group. 18 The results of French et al. did not reveal a significant benefit

4 1274 HR Davari et al. of routinely placing a stent in pediatric renal transplant recipients. 11 Therefore, it seems that using a stent may be accompanied by a lower rate for fistula, urinary leakage and obstructions Benoit et al. discussed how the ureteral stent is able to decrease the rate of fistula. 16 They proposed that using a double pigtail ureteral stent enabled them to perform the anastomosis more easily, ensuring a sufficient diameter and avoiding ureteral bending. 16 This method helps urine evacuation in cases of edema or clots, and prevents high pressure in the renal pelvis in cases of copious initial diuresis. Stenting can also help secondary healing of small localized necrotic areas, and prevent urinary fistulas in cases of minor anastomotic gaps. 18 Additionally, an indwelling stent excludes leak, obstruction or transient edema as a cause of early postoperative oliguria. 11 We have the same experience with using routine stent in 500 kidney allografts. Some disadvantages of stenting have been observed. These include the potential for an increase in urinary tract infection. 12 We did not observe this, and our findings were similar to those of Benoit et al. 16 The overall rate of urinary tract infection in 840 renal transplants in our center was 3.8%. We remove the stent routinely 3 weeks after transplantation. In cases with a positive urine culture and no response to antibiotic for 48 h or positive culture of Candida, the stent was removed immediately. In children stent removal requires general anesthesia. This adds significant stress to the child and additional cost. The physiological effects of a stent on the transplant ureter are unclear. In vivo studies using color Doppler ultrasound have demonstrated diminished ureteric peristalsis associated with a stent. The degree of hypoperistalsis is related to the length of time the ureter is stented. 19 Passive drainage is the principle mode of urine transport in the stented ureter throughout the diuretic response and particularly within a week of stenting. With longer duration of stenting (2 months) weak peristaltic activity and active ureteric transport become more evident, notably during peak diuresis. 20 Other complications of ureteric stenting include ureteric wall musculature thickening and submucosal edema, and insertional trauma from ureteric perforation may occur when using guide wire. 20 Stent migration is common in the first 2 weeks post-transplant, manifest by irritation on voiding and hematuria. 20 In our experience, long ureteric stent was accompanied by irritation on voiding mostly in woman and children, with a greater incidence of incontinence and incidental removal in women within 1 2 weeks. Minor leakage was corrected in our center by indwelling internal folly. In a few patients in whom the leakage continued Hemovac drain or new catheter placement guided by ultrasonography was the method of treatment. Benoit et al. successfully treated eight urinary leakages after transplantation by placing a nephrostomy tube and a double pigtail ureteral stent via an antegrade approach. 16 We explored major leakage after a few days to a few weeks of conservative treatment with reimplantation of ureter or uretero-ureteral anastomosis and occasionally pylo-ureteral anastomosis. Voiding cystography was done in all patients. Although reflux was observed in some of the patients, symptomatic reflux or increased incidence of urinary tract infection was not detected. We had one ureteral implantation into thickened peritoneum, which was revised. Gibbons et al. reported two such cases and one implantation into an ovarian cyst. 9 In their report, two patients had chronic ambulatory peritoneal dialysis and thickened peritoneum and the third patient had multiple prior pelvic operations. One should be careful if the patient has a small, defunctionalized or scarred bladder, has undergone pelvic operation or has had pelvic inflammatory disease. In conclusion, preserving the adventitia, fat and blood supply of the ureter by delicate dissection of the ureter during donor nephrectomy, short ureters, and fixation of the adventitia, fat and blood supply of the ureter to the bladder wall, to prevent kinking or twisting, are important factors in decreasing urological complications. Additionally, our method of ureteroneocystostomy is also effective in decreasing ureteric complications. Acknowledgment The authors would like to thank Shiraz University of Medical Sciences for financial support of this study. References 1 Mundy AR, Podesta ML, Bewick M et al. The urological complications of 1000 renal transplants. Br. J. Urol. 1981; 53: Jaskowski A, Jones RM, Murie JA et al. Urological complications in 600 consecutive renal transplants. Br. J. Surg. 1987; 74: Loughlin KR, Tilney NL, Richie JP. Urologic complications in 718 renal transplant patients. Surgery 1984; 95: Thrasher JB, Temple DR, Spees EK. Extravesical versus Leadbetter Politano ureteroneocystostomy: a comparison of urological complication in 320 renal transplants. J. Urol. 1990; 144: Politano VA, Leadbetter WF. An operative technique for the correction of vesicoureteral reflux. J. Urol. 1958; 79: Gregoir W. [Surgical management of congenital reflux and primary megaureter.] Urol. Int. 1969; 24: (in French). 7 Lich R, Howerton LW, Davis LA. Recurrent urosepsis in children. J. Urol. 1961; 86: Salvatiera O Jr, Kountz SL, Belzer FO. Prevention of ureteral fistula after renal transplantation. J. Urol. 1974; 112: Gibbons WS, Barry JM, Aefty TR. Complications following unstented parallel incision extravesical ureteroneocystostomy in 1000 kidney transplants. J. Urol. 1992; 148: Shoskes DA, Hanbury D, Cranston D et al. Urological complications in 1000 consecutive renal transplant recipients. J. Urol. 1995; 153: French CG, Acott PD, Crocker JFS et al. Extravesical ureteroneocystostomy with and without internalized ureteric stents in pediatric renal transplantation. Pediatr. Transplant. 2001; 5: Bassiri A, Amiransari M, Yazdani Y et al. Renal transplantation using stents. Transplant. Proc. 1995; 27:

5 Urological complications of renal transplant Emiroglu R, Karakayall H, Sevmis S, Akkoc H, Bilgin N, Haberal M. Urologic complications in 1275 consecutive renal transplantations. Transplant. Proc. 2001; 33: Mahdavi R, Khamar A. Ureteral complication after renal transplantation: review of preventive measures. Transplant. Proc. 1997; 29: Gedroyc WM, Koffman G, Saunders AJ. Ureteric obstruction in stented renal transplantations. Br. J. Urol. 1988; 62: Benoit G, Alexander EL, Bensadoun H et al. Insertion of a double pigtail ureteral stent for the prevention of urological complications in renal transplantation: a prospective randomized study. J. Urol. 1996; 156: Lin LC, Bewick M, Koffman CG. Primary use of a Double J silicone ureteric stent in renal transplantation. Br. J. Urol. 1993; 72: Bergmeijer JH, Nijman R, Kalkman E et al. Stenting of the ureterovesical anastomosis in pediatric renal transplantation. Transpl. Int. 1990; 3: Patel U, Kellett MJ. Ureteric drainage and peristalsis after stenting, studied using color Doppler ultrasound. Br. J. Urol. 1996; 77: Culkin DJ. Complications of ureteral stents. Infect. Urol. 1996; 9:

Indications and effectiveness of the open surgery in vesicoureteral reflux

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