Vol 16 No 01 January-February 2019 27 Two-stage Lparoscopic Repair of Two-level Ureteral Strictures: Our Experience of 8 Patients Rui-Zhi Xue1, Zheng-Yan Tang1,2, Ming-Qang Zeng1, Liang-Huang1, Jun-Jie Chen1, Zhi Chen1* Purpose: To evaluate the feasibility and effectiveness of two-stage laparoscopic repair for two-level ureteral stric- tures. Materials and Methods: From October 2010 to January 2017, 8 patients with two-level ureteral strictures, which were located in upper and lower ureter, received two-stage laparoscopic repair in our institution. Laparoscopic ureteroureterostomy was conducted for the upper ureteral strictures in first stage and 8 weeks later laparoscopic ureterovesical reimplantation was performed for lower stricture after the patency of upper lesion was confirmed by antegrade ureteropyelography. The kidney was drained by a nephrostomy tube during the interval period of two operations. Result: All the operations were performed successfully without intraoperative complications except one patient converted to open surgery during second-stage operation. For first-stage surgery, mean operating time was 120.88 ± 16.88 min, mean blood loss was 89.38 ± 13.74 mL, and mean duration of postoperative hospitalization was 3.63 ± 0.74 days. While in second-stage surgery, mean operating time took 125.25 ± 17.00 min, mean blood loss was 65.63 ± 10.16 mL, and mean duration of postoperative hospitalization was 3.62 ± 1.41 days.. On ureteropyelogra- phy 10 weeks after second-stage surgery, the contrast medium flowed from kidney down into bladder unrestrict- edly and the patency of entire ureter was restored in all patients. During the follow-up, one female was observed kidney atrophy with ureteral calculus formed on the lesion side, and was successfully treated by ureteroscopic lithotripsy. No sign of stricture recurrence was found on other patients. Conclusion: Two-stage laparoscopic repair is a feasible and effective treatment for two-level ureteral strictures. But its indication is relatively narrow and confined to ureteral strictures located in two sites with sufficient interval distance and minor stricture length. Keywords: laparoscopy; reconstruction; ureteral stricture; ureteroureterostomy; ureterovesical reimplantation INTRODUCTION During recent years, the widespread diffusion of minimally invasive procedure in ureteral treat- ments has led to an increasing incidence of ureteral strictures.(1) Among them, the two-level ureteral stric- ture, which is defined as two sites of strictures in unilat- eral ureter, is a relatively rare but definitely challenging issue for urology surgeons to deal with. Although nu- merous clinicians have tried various efforts to restore patency, few of them achieved the satisfied outcome, recurrence of strictures is the most common final results for these therapeutic attempts.(1,2) In our report, by describing operational and follow-up data of 8 patients with two-level ureteral strictures, we aim to evaluate the feasibility of our two-stage laparo- scopic repair for this complicated disease, and explore the optimal indication of this procedure. 1Department of Urology, Xiangya Hospital, Central South University, Changsha, Hunan, P.R. China, 410008. 2Hunan Engineering Laboratory for Diagnosis and Treatment Technology of Urogenital Diseases, Changsha, Hunan, P.R. China, 410008. Statement: Dr.Rui-Zhi Xue and Dr.Zheng-Yan Tang contributed equally to this study and should be considered as co-first author *Correspondence: Department of Urology, , Xiangya Hospital, Central South University, Changsha, Hunan, P.R. China, 410008.Tel: +86 15243676149, Fax: +86 0731 89753012, E-mail: docfrankhsueh@126.com. Received August 2017 & Accepted April 2018 MATERIAL AND METHODS Patients From October 2010 to January 2017, 8 patients with two-level ureteral strictures were referred to our in- stitutes and received the two-stage laparoscopic sur- gery. All of the patients signed the informed consent agreements and this study had been approved by ethic committee of the Xiangya Hospital of Central South University. Ranging from 28 to 63 years old, these 8 patients share the same chief complains of flank pain and discomfort. Among them, 5 patients’ etiology were considered as Holmium laser injuries, their historical operational records offered by the local hospital showed that the laser was mainly operated in the upper and low- er parts of ureter, and the patients developed hydrone- phrosis rapidly after surgery. 3 patients were diagnosed as two-level ureteral strictures which were caused by impacted calculus. According to their description, they had multiple times of hematuria followed by experience of urinating stones a few months before, and none of LAPAROSCOPIC AND ROBOTIC UROLOGY them had received ureteral surgeries in the past. There is only one patient who had no operation in the past and denied any symptoms of urolithiasis, we concluded his etiology as idiopathic. Because of the fast development of hydronephrosis, all patients had received percutane- ous nephrostomy and kept a nephrostomy tube for tem- porary drainage in local hospital prior to admission to our institution. Operative technique Facing this challenging disease, instead of repairing the two lesions in one single surgery, we adopted two-stage laparoscopic operation. In first stage we repaired the upper stricture of ureter by transperitoneal laparoscopic end-to-end anastomosis, while lower ureteral strictures were dealt with ureteral reimplantation in second-stage surgery. Before operation, upper ureteral stricture was con- firmed by antegrade ureteropyelography in all patients (Figure 1A). When the first-stage surgery began, under general endotracheal anesthesia, patients were placed in a supine position with lesion side elevated, then the three-port laparoscopic approach was established with a 12-mm port positioned infraumbilically and two 12-mm ports in the lateral border of rectus muscles. The ureter was mobilized in the first step, ureteral part above the stricture site is often dilated, thus the joint site of dilated ureter and non-dilated ureter indicates the position of lesion and stricture site of upper ureter could be located accordingly (Figure 2A). The ureteral stricture lesion was excised and its lumen turned out to be completely occluded, no urine flowed out from proximal end (Fig- ure 2B). After trimming the lesion site until normal lumen was seen, an interrupted anastomosis with 4–0 monocryl was performed accordingly. When the upper ureteral anastomosis was finished, since the lower stric- ture still existed, we kept the nephrostomy tube in place to divert urine and had not placed the double J stent. Patients were discharged with nephrostomy tube and re- admitted 8 weeks later to receive second-stage surgery. Before second surgery, all patients’ upper ureter had been confirmed unobstructed by antegrade ureteropy- elography, the contrast medium passed through origi- nal upper stricture lesion fluently (Figure 1B) but ob- structed in lower stricture area, and no contrast medium Table 1. Preoperative data of patient Case Age Gender Side Etiology Presentation Distance between Distance between Interval (years) US & UPJ(cm) LS & UVJ(cm) distance (cm) 1 44 M L Holmium laser Left flank pain 9 2 15 2 38 F L Impacted calculus Left flank pain 3 1 22 3 56 M R Holmium laser Right flank pain 12 4 8 4 55 F R Holmium laser Right flank pain 7 3 14 5 63 F L Impacted calculus Left flank pain 10 1 12 6 33 F R Holmium laser Right flank pain 7 2 15 7 28 M R Idiopathic causes Right flank pain 9 3 14 8 40 M L Holmium laser Left flank pain & fever 7 1 18 Abbreviations: US, Upper Stricture; UPJ, Ureteropelvic Junction; LS, Lower Stricture; UVJ, Ureterovesical Junction Fig.1 A. Preoperative antegrade ureteropyelography of patient showed the contrast medium was obstructed at stricture site of left upper ureter (arrow). B. Before the second surgery, an antegrade ureteropyelography was arranged, the contrast medium passed the anastomotic site of upper ureter smoothly without any sign of stricture or leakage (arrow). C. Although the patency of upper ureter was restored, the contrast medium was obstructed in lower strictured area, and no contrast medium had reached bladder. D. 10 weeks after second-stage surgery, an antegrade ureteropyelography via nephrostomy tube (arrow) was arranged, it showed patency of the entire length of ureter and contrast medium flowed from renal pelvis down into bladder unrestrictedly. Repair of two-level ureteral strictures-Xue et al. Laparoscopic and Robotic Urology 28 Vol 16 No 01 January-February 2019 29 had reached bladder (Figure 1C). In such situation, the second surgery of laparoscopic ureteral reimplan- tation was performed accordingly. The patient was put in supine position with pads under their hips, then three-port laparoscopic approach was established with one 12-mm trocar in the umbilicus, one 12-mm trocar above the symphysis pubis and one 12-mm trocar in the McBurney point or its symmetry point. After the isolation of the stricture lesion of lower ureter (Figure 2C), a cystotomy was made for the reimplantation of the ureter. Prior to complete the ureteroneocystostomy with 4-0 interrupted stitches (Figure 2D), a double J stent was placed. Prevention of vesicoureteric reflux is routinely performed in our institution. Anastomot- ic part of ureter obliquely passed through the bladder muscular layer and was regularly wrapped by vesical membrane to form an artificial tunnel for ureter. The double J stent was kept for 8 weeks, and for safety rea- sons the nephrostomy tube was still kept in place when second-stage surgery was finished. Before removal of the nephrostomy tube, which was regularly arranged 10 weeks after the second-stage operation, antegrade ure- teropyelography via nephrostomy tube was scheduled for all patients, and images showed patency of the entire length of ureter and contrast medium flowed from renal pelvis down into bladder unrestrictedly (Figure 1D). RESULTS For all the 8 patients, the diagnosis of two-level ureteral stricture was confirmed by antegrade ureteropyelog- raphy and retrograde pyelography, which respectively demonstrated upper and lower stricture lesion. Accord- ing to imaging data, the measured distance from the upper ureteral stricture to ureteropelvic junction ranged from 3 cm to 12 cm, and distance between lower ure- teral stricture and ureterovesical junction was no longer than 4 cm. Correspondingly, the approximated interval distance between upper and lower strictures was meas- ured varying from 8 cm to 22 cm. Specific preoperative details of the patients are listed in Table 1. All patients received the surgical treatments on sched- ule and no intraoperative complication was occurred except one patient was converted to open surgery dur- ing his second-stage operation, due to the extreme adhe- sion and difficulty of dissection under laparoscopy. For first-stage surgery, mean operating time was 120.88 ± 16.88 min, mean blood loss was 89.38 ± 13.74 mL, and mean duration of postoperative hospitalization was 3.63 ± 0.74 days. While in second-stage surgery, mean op- erating time took 125.25 ± 17.00 min, mean blood loss Table 2. Operative and follow-up data of patients Case Operation data Follow-up dataa Operating time Operating time Blood loss Blood loss LHS after LHS after Complications Duration of Radiography of FSS (min) of SSS (min) of FSS (mL) of SSS (mL) FSS (days) SSS (days) follow-up (months) recheck 1 115 136 90 75 3 3 None 79 No recurrence of stricture 2 131 112 100 55 4 3 None 33 No recurrence of stricture 3 120 153 90 80 3 7 Converted to open 30 No recurrence surgery during SSS of stricture 4 105 130 80 70 3 3 Kidney atrophy & 25 Kidney atrophy & ureteral calculus ureteral calculus formed formed 5 139 95 100 65 3 3 None 22 No recurrence of stricture 6 90 122 60 70 4 3 None 15 No recurrence of stricture 7 132 125 100 50 5 4 None 11 No recurrence of stricture 8 135 129 95 60 4 3 Moderate stenosis 3 Moderate stenosis of upper of upper anastomotic site anastomotic site Abbreviations: FSS, First-Stage Surgery; SSS, Second-Stage Surgery; LHS, Length of Hospital Stay. aThe data was documented since second-stage surgery, there was no complication or unexpected event occurred during and after the first operation. Fig.2 A.The first stage surgery was performed through transperito- neal approach, after the ureter was mobilized, we located the stric- tured site of upper ureter (arrow). B. When the ureteral stricture lesion was excised, the lumen turned out to be completely occluded and no urine flowing out from proximal end of incision (arrow). C. The second surgery was laparoscopic ureteral reimplantation. The stricture lesion was located at lower end of ureter (arrow). D. The anastomotic site of ureteroneocystostomy was sutured with 4/0 interrupted stitches Repair of two-level ureteral strictures-Xue et al. was 65.63 ± 10.16 mL, and mean duration of postopera- tive hospitalization was 3.62 ± 1.41 days. Foley catheter was removed in the first day after first-stage surgery, while for second-stage surgery the catheter was nor- mally kept for 7 days before removal to prevent early vesicoureteric reflux. In both stages of surgeries, all patients’ abdominal cavity drainage tube was removed when the daily drained volume was less than 10 mL. These 8 patients were under persistent follow-up. One female was observed kidney atrophy and ureteral calcu- lus formed on the lesion side. The ureteral calculus was treated successfully by ureteroscopic lithotripsy the day we found it, by far her serum creatinine and estimat- ed glomerular filtration rate (GFR) are still normal and under regular recheck. No recurrence of strictures or aggravation of hydronephrosis was showed of all other patients. The feedback of telephone follow-up indicated all the patients are asymptomatic by far. Specific pe- rioperative and follow-up data is provided in Table 2. DISCUSSION As a by-product of fast development of endoscopic therapy in urology, ureteral strictures occur much more frequently than the past, and patients with multiple sites of ureteral strictures are not rare to see in nowadays. For decades, urologists have been groping for solutions continuously, but except traditional open ureteral re- construction surgery, which had been proved attached with severe complications and surgical trauma, current minimal invasive treatments for this disease have been fruitless and rarely reported.(2-5) The surgical procedure adopted in our report is the two- stage laparoscopic ureteroplasty, which includes urete- roureterostomy and ureterovesical reimplantation. The main reason of conducting this surgery in two stages instead of in one is to simplify complexity of the op- eration and guarantee good healing of the anastomotic site. By dividing treating procedure into two stages, we focused on only one site of lesions in each surgery, and performing the second-stage treatment only after the success of first surgery was confirmed. Through this step-by-step operation, the curative effect is actually enhanced with minor surgical difficulty. Both of the two stages of laparoscopic surgeries were conducted through transperitoneal approach. Although there are some surgeons preferring to perform upper ureteral anastomosis by retroperitoneal laparoscopy, we think a larger surgical space and greater clarity of vision offered by transperitoneal approach could much facilitate the operation. The laparoscopic ports place- ment in the first surgery was arranged by reference to the relevant surgical instructions(6). To be noticed, the two ports on lateral border of rectus muscles should not be placed too far from midline of body, otherwise much difficult will be met during the process of turning the colon downward to expose retroperitoneal structures. The placement of ports in the second surgery, which aimed to facilitate the dissection of lower ureter and bladder, was regularly adopted in ureteral reimplanta- tion. However, intense carefulness should be paid when inserting the first trocar in umbilicus, because first- stage surgery may have caused intestinal adhesion with visceral abdominal wall, and intestinal puncture injury could occur due to blinded actions. Thus fully pulling up of abdominal skin before puncture and a progressive piercing manoeuvre are necessary to prevent such com- plication. Another advantage of two-stage operation is that it can protect the blood supply of ureter and guarantee good healing of anastomotic site. Ureteral blood supply mainly comes from vascular network that embedded in the periureteral sheath (sheath of waldeyer).(7,8) Per- forming resection and anastomosis of both sites in one- stage surgery will inevitably involve large-scale dissec- tion of periureteral sheath, which will lead to damage of main blood supply of ureters.(9,10) According to the study of 64 patients who recieved ureteral anastomo- sis from Wang,(11) overmuch dissection of periureteral sheath can easily cause ischemia necrosis of anastomo- sis site, while preserving periureteral sheath or covering pedicled omentum on it remarkably reduced this com- plication. In our report, during each stage we only op- erated on one site of ureter, leaving periureteral sheath and blood supply of rest part conserved. By alternately repairing the upper and lower ureteral strictures, maxi- mum protection of ureteral blood supply was achieved. The interval time between two surgeries was set as 8 weeks, which can guarantee scare tissue of anastomotic site stabilized and sufficient neovascularization formed. (12-14) We do not recommend longer interval time due to risks of renal function deterioration and nephrostomy tube falling out. As for the repairing sequence, although all the patients in our report received upper stricture re- pair firstly due to preference of the surgeon, we presume the reversed repairing sequence is also practicable and further relevant control study should continue in future. There are also some limitations of our surgical proce- dures. First of all, the two-stage laparoscopic repair is mainly suitable for two-level ureteral strictures with short lesion length (usually the stricture length should be no longer than 3 cm), otherwise the anastomosis may fail due to overwhelming anastomotic tension. Second- ly, for strictures that are located too closely to each other (usually < 10cm), the second stage laparoscopic repair may not be achieved. Among our patients, the only one that converted to open surgery in second-stage operation is also the one that has the narrowest interval distance (8cm). Because when the two stricture lesions are too close, the second operation may share the same operational area with the first one. As is well-known, the severe tissue adhesion of surgical region caused by the first surgery will bring extreme inconvenience to second laparoscopic operation. Lastly, due to the rel- atively long period of the whole treating procedures, patients with unfavorable general conditions or re- sidual renal function less than 25%, should be under careful evaluation before being selected for two-stage laparoscopic surgery. One female patient in our study developed kidney atrophy after surgery and renogram showed remained function of the diseased kidney was under 10% by now. We consider this outcome is largely related to the severe hydronephrosis of this patient and long duration of the whole treating process. Although nephrostomy tube can temperately alleviate hydrone- phrosis, longtime indwelling drainage device can also damage renal function.(15) CONCLUSIONS Two-stage laparoscopic repair is a feasible and effec- tive treatment for two-level ureteral strictures. But its indication is relatively narrow and confined to ureteral strictures located in two sites with sufficient interval Repair of two-level ureteral strictures-Xue et al. Laparoscopic and Robotic Urology 30 Vol 16 No 01 January-February 2019 31 Repair of two-level ureteral strictures-Xue et al. distance and minor stricture length. ACKNOWLEDGEMENT We thank for the support from National Natural Sci- ence Foundation of China (No. 81570627) and Natu- ral Science Fund for Youth in Hunan Province (No. 2015JJ3162). CONFLICT OF INTEREST No competing interests exist. REFERENCES 1. Patel RC, Newman RC. Ureteroscopic management of ureteral and ureteroenteral strictures. Urol Clin North Am. 2004;31:107- 13. 2. Komyakov BK, Novikov AI, Ochelenko VA, Guliev BG, Al-Attar TK, Onoshko MV. [Technical features of intestinal ureteroplasty. art 6: simultaneous ureteral and bladder substitution]. Urologiia. 201712-5. 3. Kamat N, Khandelwal P. Laparoscopy- assisted ileal ureter creation for multiple tuberculous strictures: report of two cases. J Endourol. 2006;20:388-93. 4. Shokeir AA, Ghoneim MA. Further experience with the modified ileal ureter. J Urol. 1995;154:45-8. 5. Goldfischer ER, Gerber GS. Endoscopic management of ureteral strictures. J Urol. 1997;157:770-5. 6. RV K. Difficulties in laparoscopic ureteral and bladder reconstruction. In: Al-Kandari AM GI, ed. Difficult Conditions in Laparoscopic Urologic Surgery. Vol 2. New York: Springer; 2011:321. 7. Elkoushy MA AS. Surgical, Radiologic, and Endoscopic Anatomy of the Kidney and Ureter. In: Wein AJ KL, Novick AC, Partin AW, Peters CA, ed. Campbell-Walsh Urology. Vol 2. 11th ed. Philadelphia: Elsevier; 2016:976. 8. Sukumar CD JR, Mahalakshmamma V. An anatomical study on blood supply of ureter. Int J Anat Res. 2015;3:970-5. 9. Javali T, Kasaraneni D, Banale K, Babu PS, Nagaraj HK. Vesicouterine fistula and concomitant ureteric necrosis following uterine artery embolization for fibroid uterus. Int Urogynecol J. 2015;26:1877-8. 10. Sutherland RS, Pfister RR, Koyle MA. Endopyelotomy associated ureteral necrosis: complete ureteral replacement using the Boari flap. J Urol. 1992;148:1490-2. 11. Wang G, Han G, Ren Y, et al. [Clinical effects of pedicled omentum covering and wrapping the ureteral anastomosis to prevent ureteral anastomotic leakage after surgery of abdominal and pelvic tumors]. Zhonghua Zhong Liu Za Zhi. 2014;36:232-5. 12. Andreoni CR, Lin HK, Olweny E, et al. Comprehensive evaluation of ureteral healing after electrosurgical endopyelotomy in a porcine model: original report and review of the literature. J Urol. 2004;171:859-69. 13. Sherratt JA, Dallon JC. Theoretical models of wound healing: past successes and future challenges. C R Biol. 2002;325:557-64. 14. Sahin S, Resorlu B, Atar FA, Eksi M, Sener NC, Tugcu V. Laparoscopic Ureterolithotomy with Concomitant Pyelolithotomy Using Flexible Cystoscope. Urol J. 2016;13:2833-6. 15. Nissenkorn I, Gdor Y. Nephrovesical subcutaneous stent: an alternative to permanent nephrostomy. J Urol. 2000;163:528-30.