Abstract
Introduction
Radical cystectomy (RC) and radical nephroureterectomy (RNU) are commonly performed in urological oncology. Concurrent disease in the upper tract and bladder is rare, so performing both procedures in the same setting is uncommon. Here, we report the perioperative and oncological outcomes of a single-institution series of concurrent RC+RNU.
Methods
We retrospectively reviewed the charts of patients who underwent concurrent RC+RNU for bladder and/or upper tract urothelial carcinoma between 2006 and 2020. Patient demographic and clinical factors, perioperative parameters, and oncological outcomes were obtained.
Results
Twenty-seven patients underwent RC+RNU during the study period; 22 (81%) were male. Median (interquartile range) patient age was 71 (67–75) years. All had a diagnosis of bladder cancer. Concurrent upper tract urothelial carcinoma (UTUC) was the indication for RNU in 12 cases (44%) and non-functional renal unit in the remainder. Two patients (7%) experienced early postoperative mortality. Eight patients (30%) experienced major complications (Clavien-Dindo >3). Complications did not vary significantly between those rendered anephric (5/16, 31%) and those who were not (3/11, 27%) (p=0.82, Chi-squared test). Median (95% confidence interval) and five-year overall survival were 47 (41–52) months and 42%, respectively. Six of 22 male patients (27%) experienced a urethral recurrence and three of 14 patients (21%) with non-functional kidneys had occult UTUC discovered on final pathology.
Conclusions
Combined RC+RNU carries an elevated perioperative risk, primarily in highly comorbid patients. Striking rates of occult UTUC in non-functional kidneys and of urethral recurrence after cystectomy were noted. RC+RNU is an appropriate option in select patients.
Introduction
Urothelial cell carcinoma (UCC) is projected to be responsible for 84 000 new cancer cases in 2021 and to represent the fourth most common cancer in men.1,2 A primary bladder malignancy accounts for 90–95% of all UCC cases, while upper tract urothelial carcinoma (UTUC) accounts largely for the remainder. Radical cystectomy (RC) remains the gold-standard surgical treatment for invasive or pathologically adverse UCC, while radical nephroureterectomy (RNU) remains the gold-standard surgical treatment for pathologically adverse UTUC.2,3
Of the approximately 25% of bladder cancer patients who have disease aggressive enough to warrant RC, a small but appreciable fraction of patients demonstrate concurrent pathology of the upper tract that may warrant simultaneous RNU. The indication for upper tract removal may be due to synchronous UTUC or non-functioning kidney(s) secondary to obstructive uropathy or intrinsic renal disease.2 Indeed, both indications are, to some extent, linked to the presence of UCC of the bladder cancer. Likely due to a shared pathogenesis between UTUC and UCC of the bladder, synchronous UTUC and UCC of the bladder is not uncommon.4,5 As many as 17% of those with UTUC present with synchronous bladder cancer.6
The presence of a non-functioning kidney may similarly demonstrate a relatively high prevalence in patients with aggressive UCC of the bladder. Approximately 27% of patients with muscle-invasive bladder cancer present with hydronephrosis prior to cystectomy, and chronic kidney disease (CKD) patients have been shown to have significantly higher rates of multifocal UCC/UTUC.7–9 The risk of UTUC in end-stage renal disease (ESRD) patients is so high, approaching 50-fold higher than seen in the general population in some nations, that prophylactic bilateral nephroureterectomy of the non-functioning renal units may be considered even in the absence of UTUC when cystectomy is indicated.8,9
Still, there are relatively low proportions of patients who have severe enough pathology of both the upper and lower tracts to warrant simultaneous RC+RNU, which has hampered adequate characterization of patient outcomes. To date, only small case series and individual case reports are available on this topic. 8,10–13 Accordingly, herein, we present the largest case series of patients undergoing simultaneous RC+RNU in North America to date. The aim of this study was to present our single-institution experience of those cases necessitating these two procedures concurrently. Our results will help to guide counselling and management in this rare scenario.
Methods
Patient cohort
Twenty-seven patients who underwent simultaneous RC and unilateral or bilateral RNU between 2006 and 2020 at our tertiary referral center institution were identified. A database of patient characteristics, operative parameters, complications, and oncological outcomes was assembled by chart review. This retrospective review was approved by the institutional review board (protocol number STU 2021–0527) and informed consent was waived.
Data collection
Patient data collected included demographic data, age at surgery, clinical comorbidities, body mass index (BMI), tobacco use status, American Society of Anesthesiologists (ASA) classification, history and details of prior bladder or upper urinary tract carcinoma, preoperative cancer grade and stage, and use of neoadjuvant chemotherapy. Operative details documented included RNU laterality, surgical approach for the bladder, surgical approach for the kidney, estimated blood loss, total operative time, transfusion requirement, postoperative course details, complications using Clavien-Dindo classification, and surgical pathology results. The oncological outcomes documented included subsequent therapies, oncological progression, urethral recurrence, last followup, and death with associated cause.
Statistical analysis
Descriptive statistics were performed, with calculation of mean with standard deviation or median with interquartile range (IQR) when appropriate. Perioperative outcomes of interest among patients rendered anephric vs. not and between different surgical approaches were calculated using the Kruskal-Wallis analysis of variance on ranks, Fisher’s exact test, and Chi-squared tests as appropriate. SPSS version 27 (IBM, Armonk, NY, U.S,) was used to generate Kaplan-Meier curves for oncological outcomes of recurrence-free survival, progression-free survival, cancer-specific survival, and overall survival (OS).
Results
Patient characteristics are provided in Table 1. Twenty-seven patients underwent concurrent RC+RNU during the study period. Twenty-two patients (81%) were male. Median (IQR) patient age was 71 (67–75) years. All patients had a diagnosis of bladder cancer. Roughly half of patients (14/27, 52%) had a prior diagnosis of non-muscle-invasive bladder cancer; of these, one underwent RC due to progression to muscle-invasive disease. Concurrent UTUC was the indication for RNU in 12 (44%) cases, with non-functional renal unit as the indication in the remaining 15 (56%) cases. Eleven (41%) patients did not require urinary diversion at the time of RC+RNU as a result of being rendered anephric. Thirteen (48%) cases were performed via an open approach, nine (33%) by a minimally invasive approach, and the remaining five (19%) by a combined approach (laparoscopic kidney, open bladder). Median (IQR) intraoperative transfusion of packed red blood cells was 2 (0–4) units, estimated blood loss (EBL) was 600 (250–1025) mL, and operative time was 405 (379–441) and 346 (247 – 376) minutes for patients undergoing and not undergoing diversion, respectively (Table 2).
Table 1.
Clinical and pathological characteristic of 27 patients who underwent combined radical cystectomy/ radical nephroureterectomy
| Variable | n (%) or median (IQR) |
|---|---|
| Total | 27 |
| Age, years | 71 (66–75) |
| Sex | |
| Male | 22 (81%) |
| Female | 5 (19%) |
| Race | |
| White | 24 (89%) |
| Black | 1 (3.7%) |
| Hispanic | 1 (3.7%) |
| Asian | 1 (3.7%) |
| Smoking status | |
| Never smoker | 8 (30%) |
| Prior smoker | 17 (63%) |
| Current smoker | 2 (7.4%) |
| Lynch syndrome | 2 (7.4%) |
| BMI | |
| Mean (± SD) | 28 (±4.4) |
| ASA score | |
| 1 | 0 (0%) |
| 2 | 4 (15%) |
| 3 | 21 (78%) |
| 4 | 2 (7.4%) |
| Charlson comorbidity index | |
| 0–2 | 4 (15%) |
| 3–5 | 11 (41%) |
| 6–8 | 10 (37%) |
| >9 | 2 (7.4%) |
| Indication for nephrouretectomy | |
| Upper tract urothelial carcinoma | 13 (48%) |
| Non-functional renal unit | 14 (52%) |
| Indication for cystectomy | |
| De novo high-risk NMIBC | 2 (7.4%) |
| De novo MIBC | 11 (41%) |
| Treatment-refractory NMIBC | 13 (48%) |
| Progressive NIMBC | 1 (3.7%) |
| Prior history of NMIBC | 14 (52%) |
| Interval since first diagnosis (months) | 60 (18–67) |
| Bacillus Calmette-Guérin treatment | 13 (93%) |
| Ta/Tis | 11 (79%) |
| T1 | 3 (21%) |
| Low-grade | 4 (29%) |
| High-grade | 10 (71%) |
| Received neoadjuvant chemotherapy | 8 (30%) |
| Clinical tumor stage, bladder | |
| cTa/Tis | 13 (48%) |
| cT1 | 4 (15%) |
| cT2+ | 10 (37%) |
| Clinical tumor stage, upper tract | |
| cTa/Tis | 11 (41%) |
| cT1 | 1 (3.7%) |
| cT2+ | 1 (3.7%) |
| Nodal stage (pelvic and upper tract) | |
| cN0 | 26 (96%) |
| cN+ | 1 (3.7%) |
| Metastatic stage | |
| cM0 | 26 (96%) |
| cM1a | 0 (0%) |
| cM1b | 1 (3.7%) |
ASA: American Society of Anesthesiology; IQR: interquartile range (25th–75th percentiles); MIBC: muscle-invasive bladder cancer; NMIBC: non-muscle-invasive bladder cancer; SD: standard deviation.
Table 2.
Perioperative outcomes and tumor pathology
| Variable | n (%) or median (IQR) |
|---|---|
| Laterality of nephroureterectomy | |
| Left | 7 (26%) |
| Right | 15 (55%) |
| Bilateral | 5 (19%) |
| Patients functionally anephric postoperatively | 11 (41%) |
| Newly HD-dependent | 4 (15%) |
| EBL (cc) | 600 (250–1025) |
| Operative time (min) | |
| Diversion performed | 405 (379–441) |
| No diversion performed | 346 (247–376) |
| LOS (days) | 6 (4.5–9) |
| Transfusion (total for hospital stay) (units pRBC) | 2 (0–4) |
| Pathological tumor stage, bladder | |
| pTa/Tis | 7 (26%) |
| pT1 | 3 (11%) |
| pT2 | 4 (15%) |
| pT3 | 3 (11%) |
| pT4 | 6 (22%) |
| Pathological tumor stage, upper tract | |
| pTa/Tis | 7 (26%) |
| pT1 | 3 (11%) |
| pT2 | 2 (7.4%) |
| pT3 | 4 (15%) |
| pT4 | 0 (0%) |
| Pathological nodal stage (pelvic and upper tract) | |
| pN0 | 20 (74%) |
| pN+ | 7 (26%) |
| Positive surgical margin (any) | 3 (11%) |
| 90-day mortality | 2 (7.4%) |
| 90-day re-admission | 7 (26%) |
| 90-day postoperative complication | |
| Clavien-Dindo 1–2 | 12 (44%) |
| Clavien-Dindo 3–4 | 8 (30%) |
HD: hemodialysis; EBL: estimated blood loss; IQR: interquartile range (25th–75th percentiles); LOS: length of stay; pRBC: packed red blood cells.
There was a significant difference in transfusions after RC+RNU by surgical approach, with median (IQR) packed red blood cell transfusions of 3 (2–5) units for open kidney/open bladder, 0 (0–0) units for minimally invasive kidney/open bladder, and 1 (0–2) units for minimally invasive kidney/minimally invasive bladder approaches. Otherwise, no significant differences were found in perioperative outcomes by surgical approach (Table 3). Eleven (41%) patients were rendered anephric by the procedure. Median postoperative length of stay was 6 (4.5–9) days. Two (7%) patients experienced early postoperative mortality, one due to a myocardial infarction and the other due to rapidly progressive sepsis from a deep surgical site infection. Notably, these deaths were in the two patients with the highest preoperative Charlson-Deyo comorbidity scores (9 and 10, respectively). Eight (30%) patients experienced a Clavien-Dindo grade 3 or 4 complication. The rate of major complications (Clavien-Dindo grade ≥3) did not vary significantly between those rendered anephric by the procedure (5/16, 31%) and those who were not (3/11, 27%) (p=0.82, Chi-square test).
Table 3.
Perioperative outcomes by surgical approach
| Variable, n (%) or median (IQR) | Open/open | MIS/open | MIS/MIS | p |
|---|---|---|---|---|
| Number of patients | 13 (48%) | 5 (19%) | 9 (33%) | – |
| Transfusion (total for hospital stay) (units pRBC) | 3 (2–5) | 0 (0–0) | 1 (0–2) | 0.004 |
| Clavien-Dindo ≥3 | 4 (31%) | 0 | 3 (33%) | 0.71 |
| 90-day re-admission | 4 (31%) | 0 | 3 (33%) | 0.71 |
| LOS (days) | 8 (6–9) | 7 (7–7) | 4 (4–6) | 0.021 |
IQR: interquartile range (25th–75th percentiles); LOS: length of stay; MIS: minimally invasive surgery; pRBC: packed red blood cells.
While only one patient (3.7%) had preoperative clinical node-positive status, seven (26%) patients had node-positive disease on final pathology, two of whom had received neo-adjuvant chemotherapy. Of the 14 patients who had RNU performed for non-functional kidneys, three (21%) were found to have occult UTUC on final pathology (one pTa, two pT3). Three (11%) patients had a positive surgical margin: one with carcinoma in situ at the urethral margin, one with carcinoma in situ at the left distal ureteral margin, and one with pT4b disease and a positive perivesical soft tissue margin. Fourteen patients (52%) were alive at last followup, with median follow up of 36 (11–52) months. Median (95% confidence interval [CI]) and five-year OS were 47 (41–52) months and 42%, respectively (Figure 1). Median (95% CI) and five-year progression-free survival were 30 (16–44) months and 41%, respectively (Figure 2, Table 4).
Figure 1.
Overall survival (OS) of the patient cohort. Kaplan-Meier curves showing OS of patients undergoing combined radical cystectomy (RC) and nephroureterectomy (RNU). Median (95% confidence interval) and five-year OS were 47 (41–52) months and 42%, respectively.
Figure 2.
Progression-free survival of the patient cohort. Kaplan-Meier curves showing progression-free survival of patients undergoing combined radical cystectomy (RC) and nephroureterectomy (RNU). Median (95% confidence interval) and five-year progression-free survival were 30 (16–44) months and 41%, respectively.
Table 4.
Long-term survival and oncological outcomes
| Variable | All patients |
|---|---|
| Median followup, months (IQR) | 36 (11–52) |
| Overall survival | |
| Median, months (95% CI) | 47 (41–53) |
| 2-yr overall survival | 76% |
| 5-yr overall survival | 42% |
| Cancer-specific survival | |
| Median, months (95% CI) | 73 (35–111) |
| 2-yr cancer-specific survival | 76% |
| 5-yr cancer-specific survival | 51% |
| Progression-free survival | |
| Median, months (95% CI) | 30 (16–44) |
| 2-yr progression-free survival | 57% |
| 5-yr progression-free survival | 41% |
| Urethral recurrence | |
| Incidence (%) | 6 (27%) |
CI: confidence interval; IQR: interquartile range.
Notably, six of 22 male patients (27%) experienced a urethral recurrence requiring subsequent urethrectomy, of whom only one had a positive urethral margin at the time of cystectomy. Of these, four had RNU performed for UTUC; a fifth had RNU performed for a non-functional kidney and was unexpectedly found to have UTUC on final pathology.
Discussion
UCC is the fourth most common cancer in men. While UTUC accounts for only 5–10% of all urothelial cancer, it does frequently co-occur with UCC of the bladder. RNU and RC, respectively, constitute the gold-standard therapies for the most severe local forms of each individual malignancy. Reports of simultaneous RC+RNU are limited, however, due to the rarity of clinical scenarios necessitating the procedure.
In this study, we present the largest U.S. case series of patients undergoing RC+RNU. Mortality within 90 days of surgery was 7% and occurred in the two patients with the highest Charlson comorbidity index. Meanwhile, grade III–IV complications were 30% and did not vary between those rendered anephric by the procedure and those who were not. A notable proportion of patients with non-functional kidneys (3/14, 21%) had occult UTUC discovered on final pathology. Most interestingly, we observed a particularly high rate of urethral recurrence (27%) among male patients. Taken together, our results suggest that with careful patient selection, concurrent RC+RNU may be safely performed in most patients. Likely due to underlying disease-related factors, urethral recurrence appears to be high, and providers may emphasize potential need for subsequent urethrectomy in counselling patients, and close surveillance of the urethra. Our findings also emphasize the importance of vigilance for occult UTUC in patients with UCC of the bladder and concurrent hydronephrosis.
Perioperative outcomes did not differ greatly from those reported in the isolated RC or combined RC+RNU literature. Notably, the two patients experiencing perioperative death possessed the highest Charlson comorbidity index of all patients in the study (9 and 10, respectively). Interestingly, our mortality rate was not dissimilar from the reported range of 4–6% for patients >75 years of age or with severe comorbidities undergoing RC.14–16 Previous studies on combined RC+RNU are heterogeneous, such that reported mortality rates range from 0–25%.8,10–13 The observed 90-day major complication rate (Clavien-Dindo >3) of 30% falls near the high end of the range of 15–27% outlined in RC series.3,15,17,18 Similarly, our 90-day readmission rate of 26% is similar to that reported in the RC literature.19 Nephroureterectomy is a far less morbid procedure, with perioperative mortality rates of <2% and major complications of 7–15%, suggesting that RC disproportionately drove adverse outcomes in this study.20 It is important to note that the cited outcomes data were drawn from a wide variety of time periods and settings, and we are unable to provide a direct comparison with the outcomes of patients undergoing RC without RNU at our institution during the same time period. Thus, while our morbidity outcomes appear generally similar to those reported for patients undergoing RC alone, our comparisons of the morbidity of RC and RC+RNU are necessarily speculative.
Median and five-year OS in this study were 47 months and 42%, respectively, though direct comparisons with prior studies are difficult due to the unique population studied here. That said, median OS following RNU for UTUC in a large study was reported at 24 months.21 Median OS for RC has been reported at as low as 22 months and as high as 70 months, with a five-year OS rate of about 50%.16,18 Previous series of RC+RNU reveal similarly disparate long-term survival outcomes. 8,10–13 Our study population had a comparatively large proportion of patients with non-muscle-invasive clinical staging within the bladder (cTa/Tis/T1), but a large proportion of these had pan-urothelial disease affecting the upper tract as well. Taken together, RC+RNU likely can be approached when indicated without severely endangering long-term survival outcomes.
We further noted that patients rendered anephric by the procedure did not demonstrate higher perioperative morbidity than those who did not, suggesting that in the immediate postoperative period, the increased risk of complications associated with the anephric state may be partially balanced by reducing the risk of morbidity associated with urinary diversion. Interestingly, a previous study of ESRD patients found significantly improved OS in patients who underwent bilateral RNU at the time of RC, though the underlying reason was unclear.11 We noted that a particularly high proportion of patients (21%) undergoing simultaneous RNU for non-functional kidneys possessed occult UTUC. It is possible, especially in ESRD patients, that RNU may have a protective effect due to elimination of present and future risk of progressive UTUC. In light of these findings and the limited benefit of retaining a non-functional kidney, one should consider RC+RNU for patients with bladder cancer and non-functional kidney(s).
Perhaps most interestingly, a high urethral recurrence rate of 27% was observed among male patients in this study, while previous reviews of RC patients summarize the rate of urethral recurrence at 4–6%.22–24 A majority of our urethral recurrence patients had a history of smoking or UTUC and all had non-muscle-invasive disease, all of which are reported risk factors for urethral recurrence.22,23,25,26 A potential explanation for the high urethral recurrence rate is an increased risk of recurrent malignancy due to chronic kidney disease (CKD), which has been shown to increase the risk of recurrence in the bladder following nephroureterectomy.9 CKD was notably present in all patients with urethral recurrence and had an overall high prevalence in our cohort. Likewise, the co-occurrence of UTUC with UCC of the bladder may imply a more severe field effect of the entire urothelium, including the urethra. This is potentially supported by the fact that three of patients with urethral recurrence and prior UTUC had previously undergone contralateral RNU prior to combined RC+RNU. These patients, therefore, all eventually developed metachronous pan-urothelial disease. Notably, only one out of six patients with urethral recurrence had a positive urethral margin at the time of RC, suggesting that margin-positive status is not the primary determinant of urethral recurrence. Ultimately, although the underlying reasons for this finding appear unclear, we would suggest emphasizing the potential for urethral recurrence in these patients and considering performing concurrent urethrectomy at the time of surgery.
Limitations
There are several limitations to our study. Due to this study’s observational, retrospective design, the strength of the conclusions that can be drawn from these results is limited. The study period spanned a long time period, encompassing numerous changes in management practices and available treatment options. Accepting this, the goal of this study was to identify basic information to assist with clinical decisionmaking and counselling. Because of the uncommon coincidence of indications for simultaneous RC+RNU, our sample group was small and may predispose our findings to the effect of chance. This is an inherent problem in research of this topic but could be addressed in the future by pooling of data from multiple institutions. Finally, it is important to note that all surgeries were conducted at a single high-volume academic center, thus limiting the generalizability of our findings to other settings.
Conclusions
We present one of the largest published series of outcomes following concurrent RC+RNU. Our observed complication rates are comparable to those previously described for RC alone, though we are unable to provide a direct comparison of the morbidity of RC+RNU and RC alone. Further, a substantial proportion of patients can achieve long-term recurrence-free and OS following concurrent RC+RNU, making it an appropriate option in management of carefully selected patients. Patients with non-functional kidneys at the time of cystectomy for bladder cancer may have a higher rate of occult UTUC. A strikingly elevated rate of urethral recurrence was noted among male patients undergoing RC+RNU, suggesting a unique pan-urothelial disease state in these patients and emphasizing the importance of urethral surveillance.
Footnotes
This paper has been peer-reviewed.
Competing interests: Dr. Lotan has received consulting fees from Abbvie, Ambu, AstraZeneca, Cleveland Diagnostics, C2I Genomics, Fergene, Ferring Research, Hitachi, Nanorobotics, Nucleix, Photocure, Seattle Genetics, Stimit, Verity Pharmaceuticals, and Virtuoso Surgical; holds investments in CAPs Medical, C2I Genomics, Nanorobot, and Vessi; and has participated in clinical trials supported by Abbott, BioCanCell, Cepheid, FKD, GenomeDx, Karl Storz, MDxHealth, and Pacific Edge. The remaining authors do not report any competing personal or financial interests related to this work.
References
- 1.Siegel RL, Miller KD, Fuchs HE, et al. Cancer statistics, 2021. CA Cancer J Clin. 2021;71:7–33. doi: 10.3322/caac.21654. [DOI] [PubMed] [Google Scholar]
- 2.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. doi: 10.1016/j.eururo.2020.05.042. [DOI] [PubMed] [Google Scholar]
- 3.Chang SS, Bochner BH, Chou R, et al. Treatment of non-metastatic muscle-invasive bladder cancer: AUA/ASCO/ASTRO/SUO guideline. J Urol. 2017;198:552–9. doi: 10.1016/j.juro.2017.04.086. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Hafner C, Knuechel R, Zanardo L, et al. Evidence for oligoclonality and tumor spread by intraluminal seeding in multifocal urothelial carcinomas of the upper and lower urinary tract. Oncogene. 2001;20:4910–5. doi: 10.1038/sj.onc.1204671. [DOI] [PubMed] [Google Scholar]
- 5.Miyake H, Hara I, Kamidono S, et al. Multifocal transitional cell carcinoma of the bladder and upper urinary tract: Molecular screening of clonal origin by characterizing CD44 alternative splicing patterns. J Urol. 2004;172:1127–9. doi: 10.1097/01.ju.0000129541.23460.48. [DOI] [PubMed] [Google Scholar]
- 6.Cosentino M, Palou J, Gaya JM, et al. Upper urinary tract urothelial cell carcinoma: Location as a predictive factor for concomitant bladder carcinoma. World J Urol. 2013;31:141–5. doi: 10.1007/s00345-012-0877-2. [DOI] [PubMed] [Google Scholar]
- 7.Zhu Z, Zhao J, Li Y, et al. Prognostic value of preoperative hydronephrosis in patients with bladder cancer undergoing radical cystectomy: A meta-analysis. PLoS ONE. 2019;14:e0222223. doi: 10.1371/journal.pone.0222223. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Ou YC, Yang CR, Yang CK, et al. Simultaneous robot-assisted nephroureterectomy and cystectomy in patients with uremia and multifocal urothelial carcinoma. J Endourol. 2011;25:979–84. doi: 10.1089/end.2010.0602. [DOI] [PubMed] [Google Scholar]
- 9.Chung SD, Huang KH, Lai MK, et al. CKD as a risk factor for bladder recurrence after nephroureterectomy for upper urinary tract urothelial carcinoma. Am J Kidney Dis. 2007;50:743–53. doi: 10.1053/j.ajkd.2007.08.007. [DOI] [PubMed] [Google Scholar]
- 10.Buse S, Hach CE, Alexandrov A, et al. Simultaneous en-bloc robot-assisted radical cystectomy and nephroureterectomy: Technique description, outcomes, and literature summary. J Robotic Surg. 2016;10:315–22. doi: 10.1007/s11701-016-0600-1. [DOI] [PubMed] [Google Scholar]
- 11.Tseng SF, Chuang YC, Yang WC. Long-term outcome of radical cystectomy in ESDR patients with bladder urothelial carcinoma. Int Urol Nephrol. 2011;43:1067–71. doi: 10.1007/s11255-011-9960-7. [DOI] [PubMed] [Google Scholar]
- 12.Barros R, Frota R, Stein RJ, et al. Simultaneous laparoscopic nephroureterectomy and cystectomy: A preliminary report. Int Braz J Urol. 2008;34:413–21. doi: 10.1590/S1677-55382008000400003. [DOI] [PubMed] [Google Scholar]
- 13.Pérez-Utrilla Pérez M, Aguilera Bazán A, Alonso Dorrego JM, et al. Simultaneous cystectomy and nephroureterectomy due to synchronous upper urinary tract tumors and invasive bladder cancer: Open and laparoscopic approaches. Curr Urol. 2012;6:76–81. doi: 10.1159/000343514. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Quek ML, Stein JP, Daneshmand S, et al. A critical analysis of perioperative mortality from radical cystectomy. J Urol. 2006;175:886–90. doi: 10.1016/S0022-5347(05)00421-0. [DOI] [PubMed] [Google Scholar]
- 15.Novara G, Catto JWF, Wilson T, et al. Systematic review and cumulative analysis of perioperative outcomes and complications after robot-assisted radical cystectomy. Eur Urol. 2015;67:376–401. doi: 10.1016/j.eururo.2014.12.007. [DOI] [PubMed] [Google Scholar]
- 16.Bream MJ, Maurice MJ, Altschuler J, et al. Increased use of cystectomy in patients 75 and older: A contemporary analysis of survival and perioperative outcomes from the national cancer database. Urology. 2017;100:72–8. doi: 10.1016/j.urology.2016.08.054. [DOI] [PubMed] [Google Scholar]
- 17.Bochner BH, Dalbagni G, Marzouk KH, et al. Randomized trial comparing open radical cystectomy and robot-assisted laparoscopic radical cystectomy: Oncologic outcomes. Eur Urol. 2018;74:465–71. doi: 10.1016/j.eururo.2018.04.030. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Gschwend JE, Heck MM, Lehmann J, et al. Extended vs. limited lymph node dissection in bladder cancer patients undergoing radical cystectomy: Survival results from a prospective, randomized trial. Eur Urol. 2019;75:604–11. doi: 10.1016/j.eururo.2018.09.047. [DOI] [PubMed] [Google Scholar]
- 19.Stimson CJ, Chang SS, Barocas DA, et al. Early and late perioperative outcomes following radical cystectomy: 90-day readmissions, morbidity and mortality in a contemporary series. J Urol. 2010;184:1296–1300. doi: 10.1016/j.juro.2010.06.007. [DOI] [PubMed] [Google Scholar]
- 20.Raman JD, Jafri SM. Complications following radical nephroureterectomy. Curr Urol Rep. 2016;17:36. doi: 10.1007/s11934-016-0595-1. [DOI] [PubMed] [Google Scholar]
- 21.Margulis V, Shariat SF, Matin SF, et al. Outcomes of radical nephroureterectomy: A series from the upper tract urothelial carcinoma collaboration. Cancer. 2009;115:1224–33. doi: 10.1002/cncr.24135. [DOI] [PubMed] [Google Scholar]
- 22.Gakis G, Black PC, Bochner BH, et al. Systematic review on the fate of the remnant urothelium after radical cystectomy. Eur Urol. 2017;71:545–57. doi: 10.1016/j.eururo.2016.09.035. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Fahmy O, Khairul-Asri MG, Schubert T, et al. Urethral recurrence after radical cystectomy for urothelial carcinoma: A systematic review and meta-analysis. Urol Oncol. 2018;36:54–9. doi: 10.1016/j.urolonc.2017.11.007. [DOI] [PubMed] [Google Scholar]
- 24.Khanna A, Zganjar A, Lyon T, et al. A contemporary analysis of urethral recurrence following radical cystectomy. J Urol. 2021;206:970–7. doi: 10.1097/JU.0000000000001842. [DOI] [PubMed] [Google Scholar]
- 25.Boorjian SA, Kim SP, Weight CJ, et al. Risk factors and outcomes of urethral recurrence following radical cystectomy. Eur Urol. 2011;60:1266–72. doi: 10.1016/j.eururo.2011.08.030. [DOI] [PubMed] [Google Scholar]
- 26.Huguet J, Monllau V, Sabaté S, et al. Diagnosis, risk factors, and outcome of urethral recurrences following radical cystectomy for bladder cancer in 729 male patients. Eur Urol. 2008;53:785–93. doi: 10.1016/j.eururo.2007.06.045. [DOI] [PubMed] [Google Scholar]