Indocyanine green fluorescence-guided robotic Boari flap-pelvis anastomosis for the management of long-segment transplant ureteral stricture: a case series of six patients
Case Series

Indocyanine green fluorescence-guided robotic Boari flap-pelvis anastomosis for the management of long-segment transplant ureteral stricture: a case series of six patients

Zhenyu Xu, Haixiang Qin, Renjie Li, Xiaogong Li*, Hongqian Guo*, Guangxiang Liu*

Department of Urology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China

Contributions: (I) Conception and design: Z Xu, H Qin, H Guo, G Liu; (II) Administrative support: X Li, H Guo, G Liu; (III) Provision of study materials or patients: Z Xu, R Li, X Li; (IV) Collection and assembly of data: Z Xu, R Li, G Liu; (V) Data analysis and interpretation: Z Xu, H Qin, X Li; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

*These authors contributed equally to this work.

Correspondence to: Xiaogong Li, MD; Hongqian Guo, MD; Guangxiang Liu, MD. Department of Urology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, 321 Zhongshan Road, Nanjing 210008, China. Email: lxg6691@126.com; dr.ghq@nju.edu.cn; liuguangxiangnju@163.com.

Background: The treatment of transplant ureteral stricture (TUS) has been a great challenge, and there is limited experience with indocyanine green (ICG) fluorescence-guided robotic Boari flap-pelvis anastomosis to identify ureteral stenosis segments (especially long-segment) and their postoperative blood supply. We report case series of ureteral strictures treated with ICG fluorescence-guided robotic Boari flap-pelvis anastomosis in our center.

Case Description: We retrospectively collected clinical data of six patients diagnosed with long-segment even full-length TUS who underwent robotic Boari flap-pelvis anastomosis with the assistance of modified distribution of robotic ports and ICG fluorescence between June 2022 and June 2024, focusing on postoperative renal function, stenosis recurrence, and urinary fistulae. All patients, with long-segment even full-length TUS, underwent robotic Boari flap-pelvis anastomosis, with near infrared (NIR) fluorescence imaging using ICG fluorescence injection through the preplaced nephrostomy tube to find the pelvis and ureteric strictures of the transplant kidney. The median operative time was 181.5 min (range, 167–205 min) and the median blood loss was 65 mL (range, 50–120 mL). There were no high-grade complications (III–IV on Clavien-Dindo classification), and no patients were converted to open surgeries. The double-J stent was removed about two months after surgery, then the nephrostomy tube was removed about a week later. After six months of follow-up, no complications such as stenosis recurrence, urinary fistulae and urinary tract infection occurred. In addition, all patients did not complain for dysuria, frequent micturition, urgent urination, dysuria, or other symptoms in the follow-up.

Conclusions: Robot-assisted Boari flap-pelvis anastomosis guided by ICG fluorescence could be considered as a safe and reliable treatment for long-segment TUS. However, a large number of samples and long-term follow-up are still needed to further prove that it is the preferred option.

Keywords: Transplant ureteral stricture (TUS); indocyanine green (ICG); robotic surgical procedures; Boari flap-pelvis

Submitted Sep 09, 2024. Accepted for publication Dec 04, 2024. Published online Dec 28, 2024.

doi: 10.21037/tau-24-482

Highlight box

Key findings

• Robot-assisted Boari flap-pelvis anastomosis guided by indocyanine green fluorescence could be considered as a safe and reliable treatment.

• We used a modified distribution of robotic ports during surgery.

What is known and what is new?

• It is widely known that ureteral reconstruction is considered as a preferred treatment for complicated transplant ureteral stricture. The iliac fossa region tissue is adhesive, and it is difficult to identify the specific location of the stenosis by preoperative examination.

• By using indocyanine green fluorescence during the operation, we can accurately judge the stenosis segment and its vessels, which will be very helpful to the success of the operation.

What is the implication, and what should change now?

• For the treatment of long segment transplant ureteral stricture, indocyanine green fluorescence-guided robotic Boari flap-pelvis anastomosis is more advantageous than the traditional surgical method.

Introduction

Since Dr. Voronoy performed the first human cadaver-derived kidney transplantation (KT) in 1933, KT has become the preferred replacement therapy for end-stage renal disease (ESRD) with advances in vascular surgery and the rapid development of novel immunosuppressants (1). Although successful implementation of KT can improve patient prognosis and reduce mortality, postoperative complications remain a significant factor impacting long-term patient outcomes (2). Transplant ureteral stricture (TUS), among the urological complications, is the most common manifestation in that the incidence ranges from 2% to 10.5% (3-5).

It is widely known that ureteral reconstruction is considered as a preferred treatment for complicated TUS. However, due to the severe local adhesion of the transplanted kidney and ureter, as well as native bladder, iliac vessels and connective tissues in the iliac fossa, preoperative examinations often cannot precisely identify the accurate stricture segment and its surrounding blood supply, which brings great challenges to find and dissect the pelvis and ureter of the transplant kidney (6,7). Furthermore, none of ureteroneocystostomy, ureteroplasty nor dismembered pyeloplasty is the appropriate solution, due to the fact that severe TUS often appears in long segment even full length. In our study, near infrared (NIR) fluorescence guidance by antegradely injecting indocyanine green (ICG) was taken for intraoperative identification of the transplant pelvis and ureter as well as the stenosis, then robot-assisted Boari flap-pelvis anastomosis was performed, because of the close proximity from the pelvis of the transplant kidney to the native bladder. Up to the present, there are only scattered literatures reporting this strategy in the management of long-segment ureteral stricture of the transplant kidney. Herein, we described the surgical technique details and investigate the feasibility and safety of this surgical procedure. We present this case series in accordance with the AME Case Series reporting checklist (available at https://tau.amegroups.com/article/view/10.21037/tau-24-482/rc).

Case presentation

Patient cohort

The clinical information was retrospectively collected from June 2022 to June 2024 in our hospital (Table 1). All patients were diagnosed with TUS, and percutaneous nephrostomy was performed to temporarily drain urine and protect the function of the transplanted kidney after failed endoscopic treatments. In addition, all patients had no medical history related to bladder diseases, such as chronic cystitis, urinary tuberculosis, and bladder cancer. All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent was obtained from the patients for the publication of this case series and accompanying images. A copy of the written consent is available for review by the editorial office of this journal.

Table 1

Characteristics of 6 patients undergoing robotic Boari flap-pelvis anastomosis

Characteristics Patient 1 Patient 2 Patient 3 Patient 4 Patient 5 Patient 6 Median (range)
Gender F F M F F M –
Age (years) 29 34 64 45 46 57 45.5 (29–64)
BMI (kg/m2) 16.4 17.2 18.3 22.6 21.4 19 18.7 (16.4–22.6)
Onset of symptoms (months) 4 2 5 4 10 7 4.5 (2–10)
Medical history TRAS & UTI Cesarean section – BOT UTI UTI –
Side L R R R R R –
Stricture length FL FL 4 cm FL 3 cm 5 cm –
Preoperative hydronephrosis grade† IV III III IV III IV –
Surgery time (min)‡ 175 205 167 178 192 185 181.5 (167–205)
Blood loss (mL) 50 70 60 120 50 100 65 (50–120)
Postoperative hospital stays (days) 11 7 9 10 7 10 9.5 (7–11)
Remove catheter (days) 12 14 13 12 13 12 12.5 (12–14)
Remove ureteral stent (days) 58 64 62 57 63 62 62 (57–64)
Remove nephrostomy tube (days) 65 71 70 65 69 71 69.5 (65–71)
Follow-up time (months) 12 10 18 12 6 23 12 (6–23)
Clinical success Yes Yes Yes Yes Yes Yes –
Radio graphic success Yes Yes Yes Yes Yes Yes –

†, preoperative hydronephrosis grade, Onen’s Alternative Grading System was used to grade. ‡, surgery time includes the time of establishing pneumoperitoneum, placing the da Vinci ports, and assembling the robotic operating platform. BMI, body mass index; F, female; M, male; TRAS, transplant renal artery stenosis; UTI, urinary tract infection; FL, full-length; BOT, borderline ovarian tumor.

Surgical technique

All patients underwent surgical procedures with the da Vinci Xi system (Intuitive Surgery, Sunnyvale, CA, USA). After general anesthesia, the patient was put into a 30° Trendelenburg position similar to which was used for robotic ureteral reimplantation. A modified distribution of robotic ports was utilized (Figure 1).

Figure 1 Patient position and port placement. The diagram (A) and a representative case (B,C) showed the modified port distribution and the patient position, with the da Vinci cart located in the foot side of the patient [refer to the operating manual of da Vinci Xi system (www.davincisurgery.com/safety and www.intuitivesurgical.com/safety)].

Briefly, pneumoperitoneum was established using a Veress needle inserted in the umbilicus. Then an 8 mm endoscope port was placed at about 4 cm beside the umbilicus on the healthy side. Under the direct vision of the laparoscopic camera, the left and right instrument ports were placed 8 cm apart on each side of the endoscope port, along nearly a line parallel to the inguinal ligament of the transplant kidney side. The third instrument port, in some cases, was also needed and placed 8 cm apart from the ventromedial port. One or two assistant ports were placed in the cephalad abdominal 8 cm away from the endoscope port and the neighboring instrument port.

After docking the robot, the transplanted kidney and ureter as well as surrounding tissues were fully dissociated. In the meantime, ICG solution was prepared by dissolving 25 mg of sterile ICG powder in 20 mL of distilled water. Then 10–20 mL of diluted ICG was injected into the nephrostomy tube. Immediately after injection, the nephrostomy tube was clamped to maximize ICG retention in the renal pelvis. The course of the ICG-injected pelvis was clearly discernible from surrounding tissue because of emitted green fluorescence under NIR fluorescence. With the guide of ICG fluorescence imaging, the renal pelvis and the ureter stenosis was determined, then the obstructed ureter was dismembered at uretero-pelvic junction (UPJ). After the bladder was dropped from the abdominal wall, an inverted U-shaped bladder flap was created in the transplant kidney side on the anterior wall of the bladder, with a broad base to ensure adequate blood supply. The bladder flap is pulled into a tubular shape, to whose end the transplant renal pelvis was anastomosed with 4-0 barbed suture, and a double-J ureteral stent was inserted. In the cases of which the anastomosis was proceeded with some tension, intravenous injection of 5 mL diluted ICG was performed to observe real-time fluorescence images for assessing blood supply at the anastomotic stoma. By comparing the differences in fluorescence brightness between the anastomotic stoma and surrounding tissues, the blood supply at the anastomosis can be determined. The bladder flap or the transplanted kidney pelvis with inadequate blood supply should be thoroughly trimmed to reduce the rate of postoperative stomal leak and stenosis recurrence. When the anastomosis was completed, the nephrostomy tube clamp shall be released to help drain urine (Figure 2).

Figure 2 Critical steps of the surgical technique. (A,B) The transplanted ureter was identified under NIR fluorescence by antegrade injection of ICG through the preplaced nephrostomy tube. (C) The UPJ of the transplanted kidney was dissected and cut off, then an 8-Fr ureteral stent was inserted into the renal pelvis as a guide. (D) An inverted U-shaped bladder flap was created. (E) the Boari flap-pelvis anastomosis was performed with 4-0 barbed suture with a 6-Fr double-J tube indwelled. (F) Normal saline was injected into the bladder through the catheter to check for leaks. NIR, near infrared; ICG, indocyanine green; UPJ, uretero-pelvic junction.

Postoperative evaluation

The indwelling catheter was removed 1–2 weeks after surgery and the double-J stent was removed about 2 months postoperatively. Then the nephrostomy tube was maintained consecutive clamped to verify that the anastomosis was unobstructed. If the patient showed neither symptoms like renal colic in the transplanted kidney area, nor indications of hydronephrosis or anastomotic stenosis on antegrade pyelography, then the nephrostomy tube was removed a week later. The ultrasonography and computed tomography urography (CTU) scan were performed at 3 and 6 months postoperatively, then ultrasound was performed at 6-month intervals thereafter (Figure 3).

Figure 3 Imaging examinations of a representative case. (A) Preoperative CTU and (B) antegrade pyelography images showed a long segment TUS. (C) Antegrade pyelography images 2 months after surgery confirmed that the Boari flap-pelvis anastomosis was unobstructed. CTU, computed tomography urography; TUS, transplant ureteral stricture.

Discussion

As a common long-term urological complication after KT, TUS is associated with graft loss and mortality (8). Therefore, early diagnosis and effective treatment of TUS are crucial for KT success (9). The treatment of TUS is still controversial (2). At present, it is believed that the main treatment methods are endoscopic interventions and ureteral reconstruction surgeries including open, laparoscopic and robotic strategies (10). Previous studies have shown that endoscopic interventions, such as ureteral stents placement, ureteral balloon dilatation, and endoscopic incision, are effective to some extent in treating patients with early-stage, distal, short-segment (<0.5 cm), and non-ischemic strictures (2,11).

Although the endoscopic treatments offer cost-effectiveness and reduced invasiveness, they are associated with severe infection and compromised success rates or increased recurrence rates in complex cases (12,13). Furthermore, several studies have demonstrated that antegrade or retrograde balloon dilation or endoscopic incision with holmium laser in complicated ureterostenosis, exhibited significantly lower success rates of 45% to 62% compared to reconstruction surgery (10,14). In addition, the success rate of balloon dilation was 51% for the first treatment but decreased to 25% on the second attempt (15). It follows that patient with failures in endoscopic treatments, recurrences after treatment, obstructions longer than 3 cm or full-length stenosis should receive ureteral reconstruction surgery (11,16).

Nowadays robotic assisted laparoscopic ureteral reconstruction is a preferred surgical strategy for treating complex TUS, due to its advantages of minimal invasiveness, three-dimensional visualization, much dexterity and accelerated postoperative recovery (17). Depending on the location, length, and timing of the TUS, surgical options vary greatly. If the ureteral stricture is short than 1 cm, ureteral reimplantation (distal stenosis), pyeloureteroplasty (UPJ obstruction), or ureteroureterostomy (middle ureteral stricture) can be attempted to perform. But for long-segment (especially more than 3 cm) TUS, the proximal and distal ureters cannot reach each other after removing the stricture segment, so the autologous onlay/graft technique is needed. However, for KT patients, oral mucosal graft ureteroplasty, appendiceal onlay flap ureteroplasty and ileal ureteric replacement are not recommended, due to the great difficulty and large wounds in surgery as well as the huge risk of serious infection and slow postoperative recovery (10,18,19). Recently, Kim et al. (15) adopted the native ureter as an autologous substitution to treat long segment TUS by robot-assisted laparoscopic in two patients. Though the surgery was feasible and successful, limitations still exist. First of all, if the patient with ESRD has undergone nephrectomy for particular reasons, then the ipsilateral native ureter has been wrecked or shriveled, thus not available for re-use. Secondly, excision of the native kidney must be performed at the same time to harvest the native ureter, which brings additional risks and injuries to a great extent. Moreover, their pioneering experience with the two cases needs further exploration with more patients.

Here we reported a series of long-segment TUS cases which were managed successfully with the strategy of Boari flap-pelvis anastomosis. Up to the present, there are very few literatures describing this method performed under robot-assisted laparoscopy. Abdul-Muhsin et al. (20) reported the success of robotic ureteral reconstruction using pyelovesicostomy with Boari flap in two patients who failed endoscopic treatments, and no stenosis recurrences or urine leakages were identified postoperatively. Kim et al. (21) also reported that three patients with long segment TUS underwent robotic Boari flap-pelvis anastomosis successfully, without conversions to open surgery and severe complications during follow-up. Despite limited operating experiences, we still highly recommend this robotic strategy for the following two main reasons (22). On the one hand, it is a very limited distance from the pelvis of transplant kidney to the native bladder, so even the multi or whole segments of the transplanted ureter were stenosed, a 4–6 cm inverted U-shaped bladder flap with superiorly dissection of the bladder still can be created and anastomosed to the transplanted renal pelvis barely with any tension. On the other hand, compared with other autologous onlay/graft methods, Boari flap does not cause additional injuries to the intestinal canal or the oral cavity, so the risk of hemorrhage during operation is significantly reduced, and the postoperative complications including bowel dysfunction and oral pain may be totally avoided. In our study, we carried forward this robot-assisted surgery in more cases, and improved the efficiency and effect with modified port placement and ICG fluorescence navigation. All the patients went through the minimally invasive operation successfully without being converted to open surgery and severe intraoperative complications, and the double-J stents and the nephrostomy tubes were removed successfully after surgery.

In renal transplant patients, it is a formidable challenge to identify the transplanted ureter and renal pelvis because their location is highly variable without innate anatomical landmarks (15), and they are often surrounded by severe adhesions caused by dense desmoplastic reactions from previous transplant operation or endoscopic interventions (21). In this study, we injected diluted ICG antegradely through the preplaced nephrostomy tube to help navigate the complex anatomy. ICG is a water-soluble fluorescent dye that was approved for clinical use by the Food and Drug Administration (FDA) in 1959 (23). It has been widely used in oncological surgeries for the identification and characterization of tumors and metastatic lymph nodes (24). In recent years, with the further investigation of drug properties and development of imaging equipment, ICG has also been applied to urological operations (25). In 2013, Bjurlin et al. firstly reported the intravenous use of ICG in robotic upper urinary tract reconstruction to identify the ureter and locate the stenosis segment, with an overall success rate of 95.2% (7). So far accumulated researches have confirmed the advantages of ICG such as not radioactive, strong capacity of light absorption, low toxicity, and cost-effectiveness (25-27). In addition, compared with intraoperative guidance of ureteroscopy synchronously, ICG injection through the nephrostomy tube is convenient and safe, because it avoids complicated positioning and equipment preparation, as well as edema and exudation of the ureter (28).

The major limitations of our study were the small sample size and lack of comparison with other surgical strategies. Comparative studies with larger patient cohort, longer follow-up period would be needed.

Conclusions

We herein presented a series of TUS cases managed by robot-assisted Boari flap-pelvis anastomosis. Intraoperative administration of ICG through a preplaced nephrostomy tube was employed to visualize the ureteral stenosis and renal pelvis under the NIR fluorescence imaging, thereby facilitating precise anastomosis to enhance surgical success rates. This surgical strategy is a safe, effective, and reliable treatment procedure.

Acknowledgments

Funding: This work was supported by funding for Clinical Trials from the Affiliated Drum Tower Hospital, Medical School of Nanjing University (No. 2023-LCYJ-MS-16), and Nanjing Healthcare Science and Technology Development Special Fund Project (No. YKK22066).

Footnote

Reporting Checklist: The authors have completed the AME Case Series reporting checklist. Available at https://tau.amegroups.com/article/view/10.21037/tau-24-482/rc

Peer Review File: Available at https://tau.amegroups.com/article/view/10.21037/tau-24-482/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tau.amegroups.com/article/view/10.21037/tau-24-482/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent was obtained from the patients for the publication of this case series and accompanying images. A copy of the written consent is available for review by the editorial office of this journal.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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Cite this article as: Xu Z, Qin H, Li R, Li X, Guo H, Liu G. Indocyanine green fluorescence-guided robotic Boari flap-pelvis anastomosis for the management of long-segment transplant ureteral stricture: a case series of six patients. Transl Androl Urol 2024;13(12):2812-2819. doi: 10.21037/tau-24-482

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