Narrative review of nephron-sparing surgical management of upper tract urothelial carcinoma: is there a role for distal ureterectomy, segmental ureterectomy, and partial nephrectomy

Introduction

Radical nephroureterectomy (RNU), bladder cuff excision (BCE) with regional/retroperitoneal and/or pelvic lymph node dissection (LND) is considered as the standard of care for all high-risk non-metastatic upper tract urothelial carcinomas (UTUCs) which is based on the data-driven understanding of multifocality of this disease and the rates of ipsilateral recurrences (1-4). Since this disease is often diagnosed in geriatric age group in whom the renal function is already compromised secondary to advancing age and medical comorbidities, the radical resection negatively impacts the overall renal function. The expected decline in estimated glomerular filtration rate (eGFR) following the loss of a renal unit, which in turn influence the overall survival (OS) by adversely impacting the cardiovascular & cerebrovascular health (5,6), is one of the main arguments favoring nephron-sparing surgery/partial nephrectomy over radical nephrectomy for the management of localized renal masses (7). Surgical alternatives to RNU include segmental ureterectomy (SU)/distal ureterectomy, total ureterectomy (TU), and partial nephrectomy. We present this article in accordance with the Narrative Review reporting checklist to provide a comprehensive review and the status of these evolving alternative techniques, with oncological and functional outcomes (available at https://tau.amegroups.com/article/view/10.21037/tau-23-123/rc).

Methods

This is a non-systematic review of the literature published on outcomes of nephron-sparing alternatives to RNU. We limited our search to include articles published within the last 15 years. Although nephron-sparing management also include endoscopy-guided procedures through antegrade or retrograde approach, we are primarily including nephron-sparing alternatives with surgical resection of UTUC in this review. The electronic search for literature on PubMed (Table 1) was performed using UTUC with “nephron-sparing surgery”, “segmental ureterectomy”, “total ureterectomy”, “partial nephrectomy”, and “ileal ureter” as free text.

Patient selection

As per the recent European Association of Urology (EAU) guidelines, the nephron-sparing alternatives could be offered to patients with localized low-risk tumors (strong recommendation) (3). The main issue with this risk stratification is the significant dependance on the histopathological findings obtained on initial ureteroscopic biopsy. Previous studies have highlighted the challenges with ureteroscopy-guided biopsies which not just includes lack of adequate tissue sampling but is also associated with substantial discordance rates (clinical under-staging/under-grading) between the pathological findings at biopsy and final histopathology after extirpative surgery (8).

Appropriate patient selection is very crucial in achieving acceptable oncological & functional outcomes. Therefore, retrograde pyelogram, ureteroscopic biopsy along with cross-sectional imaging must be considered for diagnostic evaluation before offering these alternative techniques to salvage ipsilateral kidney. Low volume localized urothelial cancer should be the prime consideration besides other factors such as patient’s age, solitary functioning kidney or compromised pre-operative overall renal function, associated comorbidities, patient’s preference, and surgeon/institutional experience with these procedures.

Alternatives to RNU

SU/TU

These alternative options are based on the location of the primary tumor in the ureter. More distally located tumors can be managed with distal ureterectomy with BCE and ureteroneocystostomy with or without psoas hitch. If the defect is too large to bridge, ureteral re-implantations on Boari flap reconstruction could be utilized (9,10). For more proximally located tumors, segmental ureteral resection with end-to-end uretero-ureterostomy after adequate proximal & distal ureteral mobilization, to allow for tension free anastomosis, can be performed (9,10). TU with ileal segment replacement have also been reported in more widespread/multifocal ureteral involvement (11). These procedures can be performed with open, laparoscopic or robotic-assisted approaches based on surgeon’s discretion/experience.

With the obvious advantages of minimally invasive approach robotic-assisted management of UTUC is gradually emerging for these technically demanding surgical procedures (12,13). We have previously published our initial experience with robotic-assisted nephron-sparing management of ureteral tumors (14,15) and recently highlighted (in our most updated series), various reconstructive options including an anecdotal case report of utilizing a wedge of ileum to patch a significant defect following SU (16). Other single and multi-institutional studies have also reported the safety, feasibility and effectiveness of robotic-assisted nephron-sparing management of ureteral tumors (17-21) (Table 2).

Partial nephrectomy

For urothelial tumors located within the kidneys, options that have been tried previously include an ex-vivo open partial resection of the renal pelvis with complete ipsilateral ureterectomy with auto-transplantation and pyelovesicostomy, open partial resection of renal pelvis with free peritoneal flap reconstruction, combined open resection with calicoscopic laser coagulation, and open partial/hemi nephrectomy (22-24). Only a few case reports/series could be found in the published literature and these procedures were done for the imperative indication of solitary kidney or pre-existing or anticipated significantly compromised post-operative renal function to prevent end-stage renal disease.

Oncological outcomes

Earliest reported results on SU dates to early 1970s which suggested similar incidence of local recurrence between RNU and distal ureterectomy with re-implantation (25). The first evidence based on a large SEER database, advocating comparable cancer control between SU and RNU was reported in 2009 (26). Their study included 569 vs. 1,222 vs. 253 patients of SU vs. RNU with BCE vs. RNU without BCE and found 86.6% vs. 82.2% vs. 80.5% 5-year cancer-specific mortality free rates. Another population-based analysis of 2,299 patients, published around the same time, reported durable cancer control with SU or RNU in patients with organ-confined (pT1–T2) UTUC (27). Over the years, these findings were reiterated by both multi-institutional and single-center studies with longer follow-up. A multi-institutional study reported from France found 5-year cancer-specific survival (CSS) probability of 87.9% vs. 86.3% for SU vs. RNU for organ-confined UTUC. They also reported recurrence-free survival (RFS) of 37% vs. 47.9% for SU vs. RNU (P=0.48) (9). These reported outcomes objectively highlight comparable cancer control with nephron-sparing surgical alternatives and these procedures could be considered to salvage the ipsilateral kidney. Table 3 summarizes the oncological outcomes of various contemporary studies (multi & single center) on nephron-sparing surgical procedures (SU/distal ureterectomy) vs. RNU.

TU with ileal ureter substitution for patients with multifocal/long segment involvement of ureter

A study comprising 141 patients which included 10, 35, and 96 patients, who underwent TU with ileal ureter substitution, SU and RNU respectively, reported no significant difference in RFS, CSS, and OS, when RNU was compared to SU or TU (11). Despite the small cohort of patients in this study, oncological outcomes are encouraging, and TU can be considered for multifocal/long segment ureteral UTUC.

Distal ureterectomy

Distal ureterectomy with BCE

In a single-center analysis from Austria, comparing 49 and 42 patients treated with DU and RNU, respectively, found no significant difference in 5-year CSS (77% vs. 78% for DU vs. RNU) and RFS (91% vs. 96% for DU vs. RNU). Also, on univariable and multivariable analysis, they found no influence of the type of surgery on CSS and RFS, for the management of distal ureteral UTUC (31). In another multi-institutional study from Japan, no significant difference in 5-year CSS (P=0.70) and RFS (P=0.22) between distal ureterectomy and RNU was noted (10). Our group has previously highlighted the consequences of inadequate excision of the distal ureter (without complete ureterovesical junction & BCE) at the time of RNU, leads to inferior oncological outcomes (33). Although the oncological outcomes comparing distal ureterectomy and RNU seem promising, irrespective of the procedure considered for the management of distal ureteral UTUC, complete circumferential BCE is of utmost importance.

Distal ureterectomy without BCE

A multicentric study compared the oncological outcomes of 84 patients with distal ureteral UTUC, 65 and 19 patients underwent distal Ureterectomy with BCE and re-implantation and SU with termino-terminal ureteric anastomosis, respectively (34). At median follow-up of 22.7 months, no significant difference in 5-year OS, CSS, and RFS was noted between the two nephron-sparing options for distal ureteral UTUC. Interestingly, they also concluded that BCE is not imperative for the management of distal ureteral UTUC. Though, as highlighted in the “Distal ureterectomy with BCE” section, inadequate excision of the distal ureter & bladder cuff, yields inferior oncological outcomes and one may not want to compromise on this step (33). These varied findings require further investigation and thus, consideration for SU over distal ureterectomy with BCE for distal ureteral UTUC, must be at surgeon’s discretion & based on patient-related factors with a shared decision-making process with the patient and family.

Partial nephrectomy

Only a few case reports/series have reported the feasibility of partial nephrectomy for UTUC. A series published in 2014 comprising of eight patients, reported recurrences in 71.4% of patients with four patients who eventually died on follow-up (23). Another series from Germany reported RFS of 24 months with ex-vivo partial nephrectomy, auto-transplantation & pyelovesicostomy through open approach with/without combined calicoscopic approach (24). Feasibility of laparoscopic approach for nephrectomy with ex-vivo excision of high-grade UTUC in calyceal diverticulum and auto-transplantation have also been reported previously in two patients (35). Due to the small sample size of these studies with limited follow-up, no significant conclusions can be drawn.

Renal function outcomes

The published literature on the impact of SU vs. RNU suggests better preservation of eGFR with SU and this preservation of renal function may favorably impact non-cancer-related mortality. The renal function preservation may also allow the administration of adjuvant chemotherapy, which might not be feasible secondary to significant drop in eGFR following RNU. A recent single-center propensity-matched analysis comparing SU vs. RNU, found significantly improved preservation of eGFR with SU (P<0.001) with comparable CSS, progression-free survival (PFS), and intra-vesical RFS (IV-RFS) (29).

Similarly, a previous analysis of a relatively smaller sample size (SU vs. RNU: 12 vs. 14 patients) with comparable pre-operative eGFR (P=0.19), reported significant decline in eGFR in patients who underwent RNU, at 6 (P<0.01) and 12 months (P=0.02), while eGFR following SU was largely preserved (30).

A prior meta-analysis (SU vs. RNU: 983 vs. 2,980 patients) also reported significantly decreased risk of impairment of renal function following SU in comparison to RNU, with similar oncological outcomes (36). On the contrary, a relatively recent multicentric study comparing RNU vs. SU reported non-significant eGFR decline irrespective of the procedure received (37). For their analysis they included patients with pre-operatively reduced eGFR (<90 mL/min/1.73 m²), with 67 and 26 patients in the RNU and SU groups, respectively. Interestingly, both pre- & post-operative eGFR was significantly higher in patients who received SU and despite significant postoperative increase of creatinine levels in the RNU group (P=0.028), non-significant worsening of eGFR was found in both RNU (P=0.219) and SU patients (P=0.239), postoperatively. The data/literary findings are continuously evolving and in future, probably would provide better understanding of the impact of nephron-sparing surgical procedures on the renal function outcomes.

Role of LND

The utility of LND in patients undergoing RNU continues to evolve. The most important point to consider is the rarity of the disease condition itself which limits high quality, level I evidence. Although staging and prognostic benefit is demonstrated, the evidence in support for survival has not yet been clearly established. A recent National Cancer Database (NCDB)-based analysis including 423 patients with cN positive UTUC, noted no significant improvement in survival with the performance of LND (38). Whereas a systematic review found improved CSS with template based and complete LND in patients with high stage (≥ pT2) tumors of the renal pelvis at the time of RNU. Although, similar benefit was not found in ureteral tumors (39).

The templates for LND at the time of RNU have been reported but, no such templates exist for SU. A relevant point to consider is the underutilization of the LND at the time of surgical management of UTUC. Interestingly, as per the published literature, performance of LND was primarily based on surgeon’s discretion and patient/disease-related factors. In a NCDB-based analysis, rate of the performance of lymphadenectomy with SU and RNU was noted to be 30.1% and 19.9%, respectively (40). Although the performance of LND with SU favored improved survival, it did not reach statistical significance [hazard ratio (HR): 0.87; 95% confidence interval (CI): 0.57–1.32]. Thus, no conclusions can be drawn on the utility and outcomes following LND with nephron-sparing surgical alternatives to RNU.

Extrapolating from above, following templates can be utilized based on primary tumor location at the time of nephron-sparing surgeries (41).

For proximal ureteral tumors:

• Right-side: hilar, paracaval, precaval and retrocaval ± interaortocaval;
• Left-side: hilar, para-aortic and preaortic ± interaortocaval.

For mid ureteral tumors:

• Right-side: paracaval + interaortocaval + right common iliac;
• Left-side: para-aortic + interaortocaval + left common iliac.

For distal ureteral tumors (extended pelvic lymphadenectomy):

• Right-side: right pelvic nodes (obturator, internal & external iliac, and common iliac lymph nodes) ± paracaval;
• Left-side: left pelvic nodes (obturator, internal & external iliac, and common iliac lymph nodes) ± para-aortic.

Role of systemic chemotherapy

The role of systemic chemotherapy (neoadjuvant or adjuvant) with RNU is still evolving, although, more recent data does imply benefit with gemcitabine-cisplatin/carboplatin-based adjuvant chemotherapy in high-risk invasive disease (42). It is still largely underutilized even in patients receiving RNU, with up to 85.3% of patients [1,673/1,962] of a large NCDB-based analysis, not receiving any form of systemic chemotherapy (40). In the same analysis, they found 1.3% and 29.6% utilization of neo-adjuvant and adjuvant chemotherapy, respectively, in patients receiving SU but the benefit of its utilization was not found (40). Thus, the role of systemic chemotherapy with nephron-sparing surgical management of UTUC could not be established at this time.

Conclusions

With comparable oncological outcomes and favorable preservation of renal function, nephron-sparing surgical alternatives to RNU can be offered to carefully selected patients. While the evidence is open to selection bias, these options are best suited for patients with low volume, localized UTUC with imperative indication for renal preservation such as solitary kidney, compromised baseline renal function and expected significant decline in post-RNU eGFR. The role of LND could not be clearly established due to the paucity of data but can be performed along with nephron-sparing surgical resection, based on patient/disease-related factors. With established feasibility and effectiveness, robotic-assisted approach can be offered based on surgeon’s discretion/experience as an alternative to open approach in such cases. The role of systemic chemotherapy following nephron-sparing surgical alternatives needs further dedicated studies and may evolve in future especially in setting of high-grade urothelial cancer. The promising results of adjuvant chemotherapy trials (POUT) following RNU could be interpreted and extrapolated to select patients (high-risk invasive disease) for systemic chemotherapy after nephron-sparing management of UTUC. With better renal function preservation, these procedures, can allow the administration of such systemic therapies. Close surveillance following these procedures is also of utmost importance as the risk of recurrence is always a concern.

Acknowledgments

Funding: None.

Footnote

Provenance and Peer Review: This article was commissioned by the editorial office, Translational Andrology and Urology for the series “Upper Tract Urothelial Cancer”. The article has undergone external peer review.

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://tau.amegroups.com/article/view/10.21037/tau-23-123/rc

Peer Review File: Available at https://tau.amegroups.com/article/view/10.21037/tau-23-123/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tau.amegroups.com/article/view/10.21037/tau-23-123/coif). The series “Upper Tract Urothelial Cancer” was commissioned by the editorial office without any funding or sponsorship. A.K.H. served as the unpaid Guest Editor of the series and serves as an unpaid editorial board member of Translational Andrology and Urology from November 2023 to October 2025. The authors have no other 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.

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/.

References

1. Rouprêt M, Babjuk M, Burger M, et al. European Association of Urology guidelines on upper urinary tract urothelial carcinoma: 2020 update. Eur Urol 2021;79:62-79. [Crossref] [PubMed]
2. Hall MC, Womack S, Sagalowsky AI, et al. Prognostic factors, recurrence, and survival in transitional cell carcinoma of the upper urinary tract: a 30-year experience in 252 patients. Urology 1998;52:594-601. [Crossref] [PubMed]
3. Zigeuner R, Pummer K. Urothelial carcinoma of the upper urinary tract: surgical approach and prognostic factors. Eur Urol 2008;53:720-31. [Crossref] [PubMed]
4. Grob G, Rogers D, Pandolfo SD, et al. Oncologic outcomes following radical nephroureterectomy for upper tract urothelial carcinoma: a literature review. Transl Androl Urol 2023;12:1351-62. [Crossref] [PubMed]
5. Go AS, Chertow GM, Fan D, et al. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med 2004;351:1296-305. [Crossref] [PubMed]
6. Lau WL, Huisa BN, Fisher M. The Cerebrovascular-Chronic Kidney Disease Connection: Perspectives and Mechanisms. Transl Stroke Res 2017;8:67-76. [Crossref] [PubMed]
7. Wang Z, Wang G, Xia Q, et al. Partial nephrectomy vs. radical nephrectomy for renal tumors: A meta-analysis of renal function and cardiovascular outcomes. Urol Oncol 2016;34:533.e11-9. [Crossref] [PubMed]
8. Mori K, Katayama S, Laukhtina E, et al. Discordance Between Clinical and Pathological Staging and Grading in Upper Tract Urothelial Carcinoma. Clin Genitourin Cancer 2022;20:95.e1-6. [Crossref] [PubMed]
9. Colin P, Ouzzane A, Pignot G, et al. Comparison of oncological outcomes after segmental ureterectomy or radical nephroureterectomy in urothelial carcinomas of the upper urinary tract: results from a large French multicentre study. BJU Int 2012;110:1134-41. [Crossref] [PubMed]
10. Fukushima H, Saito K, Ishioka J, et al. Equivalent survival and improved preservation of renal function after distal ureterectomy compared with nephroureterectomy in patients with urothelial carcinoma of the distal ureter: a propensity score-matched multicenter study. Int J Urol 2014;21:1098-104. [Crossref] [PubMed]
11. Pedrosa JA, Masterson TA, Rice KR, et al. Oncologic outcomes and prognostic impact of urothelial recurrences in patients undergoing segmental and total ureterectomy for upper tract urothelial carcinoma. Can Urol Assoc J 2015;9:E187-92. [Crossref] [PubMed]
12. Saini S, Pathak RA, Hemal AK. Robotic nephroureterectomy in the management of upper tract urothelial cancer: inching toward standard of care? Int Urol Nephrol 2022;54:1777-85. [Crossref] [PubMed]
13. Pathak RA, Hemal AK. Techniques and Outcomes of Robot-assisted Nephro-ureterectomy for Upper Tract Urothelial Carcinoma. Eur Urol Focus 2018;4:657-61. [Crossref] [PubMed]
14. Singh I, Kader K, Hemal AK. Robotic distal ureterectomy with reimplantation in malignancy: technical nuances. Can J Urol 2009;16:4671-6. [PubMed]
15. McClain PD, Mufarrij PW, Hemal AK. Robot-assisted reconstructive surgery for ureteral malignancy: analysis of efficacy and oncologic outcomes. J Endourol 2012;26:1614-7. [Crossref] [PubMed]
16. Saini S, Lukas V, Pathak RA, et al. Robot-Assisted Laparoscopic Ureteral Reconstruction for Malignant Pathology: Single-Center Experience with Analysis of Perioperative, Functional, and Oncologic Outcomes. J Endourol 2023;37:42-9. [Crossref] [PubMed]
17. Palagonia E, Scarcella S, Dell'Atti L, et al. Robot-assisted segmental ureterectomy with psoas hitch ureteral reimplantation: Oncological, functional and perioperative outcomes of case series of a single centre. Arch Ital Urol Androl 2021;93:101-6. [Crossref] [PubMed]
18. Campi R, Cotte J, Sessa F, et al. Robotic radical nephroureterectomy and segmental ureterectomy for upper tract urothelial carcinoma: a multi-institutional experience. World J Urol 2019;37:2303-11. [Crossref] [PubMed]
19. Pugh J, Farkas A, Su LM. Robotic distal ureterectomy with psoas hitch and ureteroneocystostomy: Surgical technique and outcomes. Asian J Urol 2015;2:123-7. [Crossref] [PubMed]
20. Fifer GL, Raynor MC, Selph P, et al. Robotic ureteral reconstruction distal to the ureteropelvic junction: a large single institution clinical series with short-term follow up. J Endourol 2014;28:1424-8. [Crossref] [PubMed]
21. Elsamra SE, Theckumparampil N, Garden B, et al. Open, laparoscopic, and robotic ureteroneocystotomy for benign and malignant ureteral lesions: a comparison of over 100 minimally invasive cases. J Endourol 2014;28:1455-9. [Crossref] [PubMed]
22. Steffens J, Humke U, Alloussi S, et al. Partial nephrectomy and autotransplantation with pyelovesicostomy for renal urothelial carcinoma in solitary kidneys: a clinical update. BJU Int 2007;99:1020-3. [Crossref] [PubMed]
23. Macari D, Faerber GJ, Hafez KS, et al. Open surgical partial nephrectomy for upper tract urothelial carcinoma. Int J Urol 2014;21:409-12. [Crossref] [PubMed]
24. Latz S, Hauser S, Müller SC, et al. Kidney sparing surgery for urothelial carcinoma of the pyelocalyceal system: is there a role for open techniques? Results from a small series. Urol J 2014;11:1442-6. [PubMed]
25. Mazeman E. Tumours of the upper urinary tract calyces, renal pelvis and ureter. Eur Urol 1976;2:120-6. [Crossref] [PubMed]
26. Jeldres C, Lughezzani G, Sun M, et al. Segmental ureterectomy can safely be performed in patients with transitional cell carcinoma of the ureter. J Urol 2010;183:1324-9. [Crossref] [PubMed]
27. Lughezzani G, Jeldres C, Isbarn H, et al. Nephroureterectomy and segmental ureterectomy in the treatment of invasive upper tract urothelial carcinoma: a population-based study of 2299 patients. Eur J Cancer 2009;45:3291-7. [Crossref] [PubMed]
28. Abrate A, Sessa F, Sessa M, et al. Segmental Ureterectomy Versus Radical Nephroureterectomy in Older Patients Treated for Upper Tract Urothelial Carcinoma. Clin Genitourin Cancer 2022;20:381-7. [Crossref] [PubMed]
29. Kim TH, Lee CU, Kang M, et al. Comparison of oncologic and functional outcomes between radical nephroureterectomy and segmental ureterectomy for upper urinary tract urothelial carcinoma. Sci Rep 2021;11:7828. [Crossref] [PubMed]
30. Kato T, Nakayama R, Haba T, et al. Oncological and renal outcomes of segmental ureterectomy vs. radical nephroureterectomy for upper tract urothelial carcinoma. Oncol Lett 2018;16:6861-7. [Crossref] [PubMed]
31. Dalpiaz O, Ehrlich G, Quehenberger F, et al. Distal ureterectomy is a safe surgical option in patients with urothelial carcinoma of the distal ureter. Urol Oncol 2014;32:34.e1-8. [Crossref] [PubMed]
32. Bagrodia A, Kuehhas FE, Gayed BA, et al. Comparative analysis of oncologic outcomes of partial ureterectomy vs radical nephroureterectomy in upper tract urothelial carcinoma. Urology 2013;81:972-7. [Crossref] [PubMed]
33. Pathak RA, Hemal AK. Fate of residual ureteral stump in patients undergoing robot-assisted radical nephroureterectomy for high-risk upper tract urothelial carcinoma. Transl Androl Urol 2020;9:856-62. [Crossref] [PubMed]
34. Abrate A, Sessa F, Sebastianelli A, et al. Segmental resection of distal ureter with termino-terminal ureteric anastomosis vs bladder cuff removal and ureteric re-implantation for upper tract urothelial carcinoma: results of a multicentre study. BJU Int 2019;124:116-23. [Crossref] [PubMed]
35. Meng MV, Freise CE, Stoller ML. Laparoscopic nephrectomy, ex vivo excision and autotransplantation for complex renal tumors. J Urol 2004;172:461-4. [Crossref] [PubMed]
36. Fang D, Seisen T, Yang K, et al. A systematic review and meta-analysis of oncological and renal function outcomes obtained after segmental ureterectomy versus radical nephroureterectomy for upper tract urothelial carcinoma. Eur J Surg Oncol 2016;42:1625-35. [Crossref] [PubMed]
37. Abrate A, Sessa F, Campi R, et al. Segmental ureterectomy vs. radical nephroureterectomy for ureteral carcinoma in patients with a preoperative glomerular filtration rate less than 90 ml/min/1.73 m2: A multicenter study. Urol Oncol 2020;38:601.e11-601.e16. [Crossref] [PubMed]
38. Piontkowski AJ, Corsi N, Morisetty S, et al. Benefit of lymph node dissection in cN+ patients in the treatment of upper tract urothelial carcinoma: Analysis of NCDB registry. Urol Oncol 2022;40:409.e9-409.e17. [Crossref] [PubMed]
39. Dominguez-Escrig JL, Peyronnet B, Seisen T, et al. Potential Benefit of Lymph Node Dissection During Radical Nephroureterectomy for Upper Tract Urothelial Carcinoma: A Systematic Review by the European Association of Urology Guidelines Panel on Non-muscle-invasive Bladder Cancer. Eur Urol Focus 2019;5:224-41. [Crossref] [PubMed]
40. Lec PM, Venkataramana A, Lenis AT, et al. Trends in management of ureteral urothelial carcinoma and effects on survival: a hospital-based registry study. Urol Oncol 2021;39:194.e17-24. [Crossref] [PubMed]
41. Matin SF, Sfakianos JP, Espiritu PN, et al. Patterns of Lymphatic Metastases in Upper Tract Urothelial Carcinoma and Proposed Dissection Templates. J Urol 2015;194:1567-74. [Crossref] [PubMed]
42. Birtle A, Johnson M, Chester J, et al. Adjuvant chemotherapy in upper tract urothelial carcinoma (the POUT trial): a phase 3, open-label, randomised controlled trial. Lancet 2020;395:1268-77. [Crossref] [PubMed]