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Minimal invasive surgery of the distal ureter: indications, advantages and technical considerations from a single-center preliminary experience

Abstract

Purpose

The management of vesicoureteric junction (VUJ) diseases is a common and controversial problem in pediatric urology. Minimal invasive approaches were described for vesicoureteric reflux (VUR), obstructive megaureter (POM) and complicated duplex systems treatments. The aim of this paper is to describe our experience with minimal invasive approach focusing on technical considerations and preliminary outcomes.

Materials and methods

Data about patient aged between 0 and 18 years who underwent minimal invasive surgery for VUR, POM or complicated duplex system, were prospectively collected. Complications were classified according to Clavien–Dindo classification. One senior surgeon, trained in laparoscopy, performed surgeries (Lich Gregoir reimplantation, dismembered reimplantation and ureteroureterostomy).

Results

Seventeen patients were included in the study; thirteen had an extravesical reimplantation (nine non-dismembered, four dismembered) and four had an ureteroureterostomy. No complications were described. Median operating time was 98.5 min and median hospital stay was 4.1 days. Median follow-up was 7.5 months. Success rate for VUR was 78%; for dismembered reimplantation, one case showed post-operative VUR. Functional studies showed an improvement in split renal function on the pathologic moieties in patients treated by ureteroureterostomy for complicated ectopic ureters.

Conclusion

This preliminary experience in minimal invasive surgery of the distal ureter shows that this approach is feasible and safe, reduces hospitalization and gives better cosmetic. Results may be impacted by the surgeon’s learning curve and technical modifications. As robotic procedures are described to be more effective and safe, less technical demanding and associated with good results, switching from laparoscopic to robot-assisted surgery could be useful to improve results.

Introduction

Disease processes involving the vesicoureteric junction (VUJ) are a common problem in pediatric urology and their management is still controversial; although open surgery remains the preferred approach for high-grade vesicoureteral reflux (VUR), primary obstructive megaureter (POM) and complicated duplex ureters, minimal invasive approaches were described during the last years, as the laparoscopic and robotic surgery has become popular in pediatric urology. Laparoscopic approach was introduced as early as 1993 [1] and robot-assisted laparoscopic approach followed about ten years later [2]. However, there is a lack of reports and evidence regarding these approaches; so, they are still not recommended both by the European Association of Urology (EAU) and American Urological Association (AUA) guidelines [3, 4]. The aim of this paper is to describe our preliminary experience with minimal invasive approach to VUR, POM and duplex ureters, both by laparoscopic and robotic techniques, focusing on preoperative imaging work-up, technical details and preliminary outcomes.

Patients and methods

This is a prospective observational study conducted in a single tertiary center of pediatric surgery. Data about patients aged between 0 and 18 years, who underwent lower ureter reconstructive surgery by laparoscopic or robotic approach during the period September 2018–September 2019, were collected. Surgical indications were: high-grade VUR, congenital obstructive megaureter both in single and double systems. Surgical procedures included: extravesical reimplantation, according to Lich–Gregoir technique (preserving or not the native VUJ depending on the indications) and ureteroureterostomy. Data include demographics, pre-operative workup, clinical presentation, intra-operative details and surgical time, complications, length of hospital stay, and short-term follow-up. Complications were classified according to Clavien–Dindo classification. A single senior surgeon, experienced in laparoscopic and robotic procedures, performed all operations.

Preoperative workup

All patients had a first-line ultrasound (US) study of the urinary tract; voiding cystourethrography (VCUG) was the main tool to confirm the presence of VUR. Morphological and functional data were obtained by functional magnetic resonance urography (fMRU) that, at our Center, replaced the radiological urography and scintigraphy (Fig. 1). Blood and urine tests were performed.

Fig. 1
figure1

MRI showing ectopic upper moiety ureter at the vaginal level; patient presented UTI and incontinence (a). MRI showing severe dilatation of the upper moiety in ectopic ureter at the bladder neck (b). Retrograde ureterorenography showing the uretero-ureterostomy with no leak or dilatation after UU (c)

Patient preparation

Patient is placed in a supine Trendelenburg position and sterile urethral catheter is inserted. The monitor is positioned at the feet end; whereas, the surgeon stands behind the patient’s head. A 12-mm camera port is placed in the umbilicus and pneumoperitoneum is achieved up to 12 mmHg. A 5-mm working port and 3-mm trocarless grasper are inserted under laparoscopic vision on both flanks depending on the affected site. During the robotic procedures, two 8-mm ports are placed on both flanks and a 5-mm accessory port is placed laterally on the opposite side of the affected ureter.

Surgical techniques

Laparoscopic Lich–Gregoir extravesical ureteral reimplantation (LG-EUR)

A stay suture is placed at the bladder dome to suspend it and improve the visualization. The ureter is isolated distally to the iliac intersection, preserving the vas and the neurovascular bundle, and mobilized using a vessel loop or a tape. Bladder is filled with saline solution and the detrusor muscle is split, until the mucosa is exposed, creating a 3–4-cm-long tunnel depending on the ureteral diameter. The detrusor is wrapped around the ureter with interrupted 4–0 or 5–0 absorbable sutures in a tension-free top-down fashion. At the end of the procedure, the bladder is filled to check ureteral angulations or leaks. In case of VUR in incomplete double systems, ureters are isolated jointly, tacking care to preserve the common vascularization, and then wrapped with a larger detrusor flap.

Laparoscopic dismembered extravesical ureteral reimplantation (D-EUR)

Exposure and bladder suspension are the same described for LG-EUR. The distal part of the ureter is mobilized using a tape or a vessel loop. The vas and neurovascular bundle are carefully preserved. Ureter is divided close to its bladder insertion and the distal stump is ligated; in case of dilated ureters, a tapering according to Kalicinski–Starr technique is performed. Bladder is filled and the detrusor tunnel is created: a new meatus is created at the lower end of the tunnel. A stent is inserted at this stage and an uretero-vesical anastomosis is performed with interrupted 4–0 or 5–0 absorbable sutures. The detrusor is now wrapped around the ureter as described for the LG-EUR. Bladder filling is done to check waterproofness and ureteral kinking (Fig. 2).

Fig. 2
figure2

Dismembered extravesical ureteral reimplantation. Ureteral dissection extended to the bladder insertion, showing a narrow terminal end of the ureter (a). The ureter is divided just above the stenotic tract (b) and intracorporeal plication according to Starr technique is performed (c). A stent is placed laparoscopically and the ureteroneocystostomy is performed (d). Anti-reflux Lich–Gregoir wrapping is then performed

Laparoscopic uretero-ureterostomy (UU)

A JJ stent in positioned by cystoscopy in the lower moiety. Once ureters are identified, peritoneum is opened and dissection, using a vessel-loop or a tape, is carried down to reach the ectopic VUJ of the upper moiety, avoiding injuries to the vas and neurovascular bundles. Ectopic ureter is divided and the distal stump ligated. Lower moiety ureter (recipient) is incised in its distal part matching the donor ureter size, and an end-to-side anastomosis is performed, using interrupted 5–0 sutures (Fig. 3).

Fig. 3
figure3

Uretero-ureterostomy for duplex renal system with upper moiety ureter ectopic at vagina. Upper ureter was divided distally and end-to-side anastomosis was done on the recipient lower ureter (a). Stent was placed by cystoscopy before starting laparoscopy. View of the completed anastomosis (b)

Data recording and statistical analysis

All collected information was recorded in a digital database according to the Italian Personal Data Protection Act and data were analyzed by two physicians. Descriptive statistics were reported as absolute frequencies and percentages for qualitative data. Median and range were used for ages, time and size measurements, given the wide variability in our series. A 95% confidence interval (CI) was provided when appropriate. Comparison of continuous data was performed using the 2-tailed unpaired t test. In case of scant data or non-normal distribution, non-parametric tests (Mann–Whitney) were used. A p value lower than 0.05 was considered statistically significant.

Results

During the study period, 17 patients were treated. Preoperative and clinical details are reported in Table 1. Surgery was LG-EUR in nine cases (53%), D-EUR in four cases (23.5%) and UU in four cases (23.5%). Robotic surgery was used in two cases (1 LG-EUR and 1 UU). Median age at surgery was 3.1 years (range 0.7–12.2); laterality was left in 14 cases (82%) and right in 3. Preoperative ultrasound showed a median pelvic and ureteral diameter of 12.2 mm (range 0–27 mm) and 7.7 mm (range 0–20 mm), respectively. VUR was documented by VCUG in 10 cases with a median grade of 4.2 (range 3–5); low-grade reflux on the contralateral side was present in two cases. Eleven patients had a pre-operative assessment by fMRU that showed a median split renal function (SRF) of 36.8% (range 8–54%). Three patients had an ureterostomy before surgery that was closed at the time of operation. Ureterostomy was performed because of severe dilatation and poor SRF at the time of the diagnosis: one patient had a grade 5 VUR, one had a severely dilated POM and the last a severe dilatation of the upper moiety. Time of surgery was 98.5 min (range 55–170 min) and no surgical complications were described. A stent was placed in eight cases: one case had a LG-EUR and the stent was placed by cystoscopy, prior to surgery, because a concomitant stenosis of the pelvic–ureteric junction; it was removed after 34 days. In three of the four D-EUR, the stent was placed during the operation and left for a median period of 35 days (range 19–55 days). All patients treated by UU had a stent placed; in two cases, the stent was placed pre-operatively by cystoscopy in the lower moiety and in the other two cases, the stent was placed during the operation through the ureterostomy. Stent was left in place for a median time of 18.7 days (range 2–38 days). Only one patient from UU group had a spontaneous elimination of the stent after 2 days. In the UU group 3 patients had a retrograde contrast study at the time of cystoscopy for stent removal and no leaks or anastomotic strictures were reported. Bladder catheter was placed in all cases, except 2 LG-EUR, and it was removed after a median time of 2.7 days (range 1–8 days). No drains were placed. Overall median length of hospital stay was 4.1 days (range 2–11 days). Three complications were reported overall; according to Clavien–Dindo classification, we registered three grade 3b complications: one bowel occlusion because of adhesions at the umbilical scar; one distal ureteral occlusion requiring stent placement, both in LG-EUR; and one recurrent urinary tract infections due to high-grade VUR after D-EUR, requiring endoscopic injection of bulking agent. Median follow-up was 7.5 months (range 1–12 months); details are showed in Table 2. In the LG-EUR Group, VUR resolved in 78% of cases (CI 95% 0.44–0.94); comparing pre-operative and post-operative APD and ureteral dilatation, no significant differences were observed (p 0.5637 and p 0.0351, respectively). In the UU group, there was an improvement on pelvic and ureteral dilatation in one case (25%, CI 95% 0.03–0.71, p 0.4219 and p 0.7304, respectively); SRF on the affected side improved in one case over three who had a fMRI study on follow-up (33.3%, CI 95% 0.05–0.79, p 0.6257) and SRF in the pathologic moiety improved in two (66.6%, CI 95% 0.20–0.94) and remains stable in one (p 0.6335). In the D-EUR group, post-operative VUR appeared in one case presenting with UTI, pelvic dilatation improved in three over four cases (75%, CI 95% 0.28–0.96, p 0.4347) and ureteral dilatation in all (100%, CI 95% 0.45–1.00, p 0.3582). SRF was still not evaluated on follow-up in this group.

Table 1 Pre-operative clinical and radiological details reported for each procedure. Of three patients with grade 3 VUR, 2 had previous endoscopic treatments and 1 had a paraureteral diverticulum
Table 2 Short-term follow-up reported for each procedure

Discussion

The minimal invasive approach in pediatric urology gained success in the last decade, although its use is still controversial. Laparoscopic or robotic procedures were described for the treatment of VUR, POM and complicated duplex ureters with different results and recommendations, due to a lack in large series reported in literature. As reported by Bowen in 2016, the overall surgical management of VUR is decreased of 14.3% since 2000–2012, due to conservative and endoscopic approaches; on the other hand, minimal invasive approaches increased from 0.3 to 6.3% in the same period [5]. Based on these studies, we modified our surgical management of distal ureter disease, switching from open procedures to laparoscopic and robotic approaches; LG-EUR was used in VUR, both in single and double ureters, D-EUR with or without ureter tapering was performed for POM and UU was the procedure of choice for complicated duplex systems. Open ureteral reimplantation (OUR) for VUR remains the gold standard with an excellent success rate [3, 4]; even if both the EAU and AUA guidelines do not recommend minimal invasive ureteral reimplantation as a routine procedure, LG-EUR seems to be an excellent alternative with a success rate reported between 77 and 100% and low incidence of complications [2, 6,7,8,9,10,11,12,13]. As reported by Deng [14], patients receiving LG-EUR had a significantly longer operation time, but fewer days of hospital stay and shorter postoperative Foley placement than those receiving OUR. Bustangi, comparing open and laparoscopic reimplantation, concludes with the same findings; they also report a low analgesic needs for minimal invasive treatments [15]. Even if in our series, we do not compare the minimal invasive technique with the open procedures, our results regarding the median length of operation, length of hospital stay and catheter placement duration are the same that the ones reported in literature. In our series, eight patients with VUR in single and one patient with VUR in double system underwent laparoscopic LG-EUR; according to literature, we report a success rate of 78%. Only two patients with high grade VUR (grades IV–V) before surgery presented a persistent VUR (grade III) on post-operative VCUG requiring bulking agent injection. The patient with incomplete double system had a post-operative dilatation of both ureters requiring two stents positioning by cystoscopy; this could be due to a non-sufficient detrusorotomy and a narrow tunnel creation. Rodriguez [16] reported on 16 patients with duplex system who underwent to robotic extravescical reimplantation (RAL) a success rate of 87.5% was described; in two cases, they had a recurrence of reflux. They conclude that RAL common sheath ureteral reimplantation is a safe and effective technique and suggests a wide detrusorotomy with adequate detrusor flap elevation and an appropriate tension during tunnel closure, to avoid occlusive complications. Among complications, post-operative voiding dysfunctions are reported, especially in bilateral cases [17]; in our series, we did not observed post-operative bladder dysfunction. This could be due to the absence of bilateral cases, even if this complication is described in unilateral procedures too.

The surgical management of POM, according to recent guidelines, is indicated in case of obstructive ureters, defined as: SRF below 40%, or a drop in SRF of 5% on serial scans, and increasing dilatation on serial ultrasound scans [3]. Chertin published that renal function < 30%, grade III and IV hydronephrosis and ureteric diameter > 1.33 cm are statistically significant and independent predictive factors for surgery [18]. Almost 80% of perinatally detected megaureters spontaneously resolved and conservative treatment appears to be the current option. Some authors described the endoscopic dilatation of POM [19]; however, its use is not universally accepted. Kutikov described the first report of laparoscopic repair of POM in 2006 [20]. The principal techniques used for tailoring megaureters are either plication reported by Kalicinski and Starr [21, 22], or tapering reported by Hendren [23]; it is still debated if this should be performed by laparoscopic tapering/tayloring or open approach [24, 25]. In our 4 cases, the ureters were tapered laparoscopically according to Starr technique. We speculate that no difference could be observed between intra- and extracorporeal tailoring/tapering; being a demanding surgery, it depends mostly on the surgeon’s experience and laparoscopic skills. Reimplantation was performed at the level of the native ureteral meatus and the detrusorotomy was performed in a longitudinal shape for orthotopic ureters; in case of ectopic ureter, it was ligated as distally as possible and a new hiatus was created in the posterior lower bladder wall. Some authors suggest performing a psoas hitch to prevent ureteral angulations, provide a tension-free anastomosis and the stabilization of the submucosal tunnel with the implanted ureter. In our experience, we followed the technical modification proposed by Gundeti describing the LUAA technique [13]: we believe that an adequate tunnel length, an apical stay stich and the incorporation of ureteric adventitia during the detrusorraphy are all useful elements to stabilize the ureter, avoiding tense anastomosis or ureteral slip. Differently from Gundeti, we prefer to perform a top-down suturing using interrupted stitches, as suggested by Koh [26]; we agree that fixing the ureter at the apex of the detrusorotomy allows to assess the tension-free reimplantation, reducing the ureteral mobilization. Moreover, the top-down suturing avoids the necessity of ureteral elevation with one of the instruments, simplifying the suturing maneuver. Landa-Juarez described an orthotopic reimplantation without tailoring: it consists in incising the stenotic ureter longitudinally, maintaining its posterior wall attached to the bladder; the anterior wall of the ureter is then anastomosed transversally to the bladder mucosa to liberate the obstruction [27]. In our opinion, this technique, leaving a portion of pathologic ureter attached to the bladder, could lead to incomplete ureteral washout and recurrence of the dilatation; thus, we prefer to perform a full-dismembered reimplantation. Tunnel orientation is argument of debate: Bondarenko assesses that a transverse tunnel orientation in comparison with anterolateral provides a longer length, reducing the post-operative VUR incidence [25]; Neheman in 2019 described the extravesical cross-trigonal ureteral reimplantation with intracorporeal tailoring of the ureter by robotic approach; they conclude that this technique is safe, feasible and reproducible, although their follow-up period was short [28]. In our series, all tunnels were performed with an antero-lateral direction. Length of hospital stay, mean surgical time, time of Foley and stent placement observed in our series are similar to those reported in literature. If a stent is placed, the need for a Foley catheter placement could be discussed; in his series, Lopez did not use a bladder catheter after surgery, describing no voiding dysfunctions or ureteric leak [24]. Because of the risk of post-voiding dysfunction even in unilateral operations, we prefer to leave a catheter during the first 24–48 h after surgery, even if a stent was placed; as it contributes towards the reduction of urinary pressures thereby diminishing the risks of urine leak, and it is not related to longer hospitalizations. Post-operative VUR is one of the most frequent complications; Lopez and Bondarenko reported only one case of post-operative VUR (14.2% and 10%, respectively) [24, 25]. It is difficult to assess the real incidence of post-operative VUR, because a VCUG is not performed routinely in all series. Our approach is to perform VCUG in case of suspected VUR (UTI or worsening of dilatation); of four cases in our series, only one developed post-operative UTI because of grade V reflux, requiring a bulking agent injection.

Uretero-ureterostomy represents a valid alternative to reimplantation in patients with complicated duplex system. The prevalence of a duplex renal system in autopsy series ranges from 0.8 to 8% [29]. It may present with obstruction, ureterocele, VUR, UTI and renal function loss. Upper pole nephrectomy (UPN) has been the traditional surgical approach for patients with ectopic upper pole ureters and poorly functioning upper pole moieties, secondary to obstruction, VUR or infection. Concerns regarding the use of UU include hypertension from upper pole dysplasia, ureteral strictures, need for additional surgeries, UTI and new-onset of VUR (yo–yo reflux). On the other hand, UPN may cause injuries and loss of function on the lower moiety and ureteral stump-related complications. The significant degree of renal dysplasia in the pathological upper moieties can cause hypertension, proteinuria and malignancies. In different series on UPN specimens, dysplasia was found in 40–70% of cases [30, 31] but, despite these concerns, there is still poor evidence of dysplasia-related complications [32]; Levy reported a similar incidence of hypertension comparing patients with UPN and patients with lower urinary reconstruction (9% and 8%, respectively), after a 15-year follow-up [33]. New onset VUR (yo–yo reflux) can occur due to the Y-shaped configuration of the ureteroureteral anastomosis; however, this is theoretical and not confirmed on reported series. It is believed that performing the anastomosis distally, leaving a shorter distal segment of the recipient ureter before the UVJ, helps to avoid VUR [34]. Valuating the last series on robotic UU the complication rate was 7.8%: no VUR were described, neither additional surgeries on the ureteral stump were required. Robotic UU was compared with open UU showing no differences in mean operative times or complication rates [31]. Infections on the ureteral stump require surgery in 5–14% of UPN and 5–12% of open UU for ectopic ureters [31]. However, laparoscopic and robotic UU series reported no cases of subsequent ureteral stump excision; this could be due to the possibility of a more extensive excision of the ureter down in the pelvis in minimal invasive procedures. Based on the idea of a renal sparing surgery and considering the risks of UTI and lower moieties loss of function following UPN, we believe that a lower reconstructive surgery is to be preferred. Data from our series match with the current literature. Ascendant pyelography performed at the time of stent removal did not show anastomotic strictures; no VUR or UTI was observed. On follow-up, SRF improved in two patients and remains stable in one. Median length of operation, period of Foley catheter and length of hospital stay are similar to those reported in literature [35]. Stent is usually left in the recipient ureter; it could be discussed if the stent is needed to prevent anastomotic strictures or to preserve the most functioning lower moieties from obstruction. In our series, the stent was placed in two cases (50%) in the upper moieties: these two patients had a previous ureterostomy that was closed at the same time of UU and the stent was left to prevent stenosis or leak in the site of the ureterostomy. The other two cases had the stent placed by cystoscopy in the lower moieties.

Renal scintigraphy is considered as the gold standard for the evaluation of SRF, which is mandatory before surgery. However, this exam is not radiation free and it does not provide anatomical and etiological information. Functional magnetic resonance urography is a “one stop shop” technique which provides both anatomical and functional information, being very useful for the surgeon planning the operation; as we reported in a recent study, fMRI showed a high concordance with surgical findings avoiding radiation exposure [36]. A limit of fMRI is that it requires general anesthesia in young children.

Conclusions

Our preliminary experience in minimal invasive surgery of the distal ureter shows that this approach is feasible and safe. As it is well known, it reduces the need for post-operative analgesia and is related with a shorter hospitalization and better cosmetics. Even if we did not compare our series with previously open procedures, our data match with literature ones. Results may be impacted by the surgeon’s learning curve; as reported by Gundeti [37], results improve with surgeon’s experience and by introducing technical modifications. Our study has several limitations: series size and patient’s inhomogeneity do not permit valid statistical considerations; follow-up is short, not standardized and not completed in all cases. Even our results encourage the use of the laparoscopic techniques, more homogeneous studies are needed, with a long-term follow-up to better evaluate the outcomes. As robotic procedures are described to be more effective and safe, less technical demanding and associated with good results, switching from laparoscopic to robot-assisted surgery could be useful to improve outcomes.

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Carlucci, M., Fiorenza, V., Wong, M.C.Y. et al. Minimal invasive surgery of the distal ureter: indications, advantages and technical considerations from a single-center preliminary experience. J Ped Endosc Surg (2020). https://doi.org/10.1007/s42804-020-00047-9

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Keywords

  • Distal ureter
  • Ureterovesical junction
  • Duplex renal system
  • Laparoscopy
  • Reimplantation
  • Ureteroureterostomy