ABSTRACT
Introduction:
It is unclear when pelvic lymph node dissection (PLND) should be performed during laparoscopic radical cystectomy. Proponents of PLND performed before cystectomy claim that early PLND skeletonizes the urinary bladder’s vascular pedicles, making cystectomy easy. Others contend that an early cystectomy provides space and flexibility during subsequent PLND. This first-of-its-kind study compared PLND before and after cystectomy for the ease of performing surgery (total operative time, cystectomy time, and PLND time) and the operative outcomes (number of lymph nodes removed, blood loss, and complication rates).
Methods:
This ambispective cohort study included a predetermined sample size of 44 patients. The first 22 patients underwent PLND after cystectomy (Group 1), and the following 22 underwent PLND before cystectomy (Group 2). The primary outcome was total operative time. Secondary outcomes included cystectomy time, PLND time, number of lymph nodes removed, blood loss, and complication rates.
Results:
The baseline characteristics were similar in both groups. The total operative time (344.23 ± 41.58 min vs. 326.95 ± 43.63 min, P = 0.19), cystectomy time (119.36 ± 34.44 min vs. 120.91 ± 35.16 min, P = 0.53), PLND time (126.82 ± 18.75 min vs. 119.36 ± 23.34 min, 0.25), number of dissected lymph nodes (13.27 ± 4.86 vs. 14.5 ± 4.76, P = 0.40), and blood loss (620.45 ± 96.23 ml vs. 642.27 ± 131.8 ml, P = 0.20) were similar in the two groups. The complication rates categorized by Clavien–Dindo grading were identical in the two groups.
Conclusions:
PLND done after cystectomy was comparable to PLND done before cystectomy regarding the ease of surgery and the operative outcomes.
INTRODUCTION
Pelvic lymph node dissection (PLND) during laparoscopic radical cystectomy (LRC) has a prognostic and therapeutic value.[1,2] Most existing literature covers PLND templates, lymph node yield, density, positive pathological rates, and oncological benefits.[2-8] Whether PLND should be performed before or after cystectomy is seldom investigated and not mentioned in the guidelines. PLND is traditionally done before cystectomy. The proponents of this technique argue that PLND skeletonizes the vascular pedicles of the urinary bladder. Identifying and controlling these vascular pedicles during cystectomy becomes easy [Figure 1b].[9] As opposed to this, some advocate early cystectomy as it provides space for better maneuverability during PLND [Figure 1a]. Since the data are lacking on the timing of PLND in LRC, this study was done to evaluate whether PLND after cystectomy is better than PLND before cystectomy. Total operative time, cystectomy time, and PLND time as surrogates were chosen for determining the ease of surgery while comparing the estimated blood loss, lymph node yield, and complication rates in the two groups. This is a first-of-its-kind study in English literature, to the best of our knowledge.
Figure 1.
(a) Large bladder tumor distending the urinary bladder. There is very limited space to perform pelvic lymph node dissection (PLND). Performing cystectomy first in such cases may allow better maneuverability to perform PLND. (b) PLND done before cystectomy exposed the vascular pedicles of the bladder that may make cystectomy easy. The left obturator nerve is clearly seen along its entire course. (c) Figure depicting the standard five ports used for radical cystectomy in the study. Supraumbilical 12 mm port for the camera, 12 mm working port at the level of the umbilicus on the right side (for the right-handed surgeon), 5 mm working port at the level of the umbilicus on the left side, 5 mm assistant ports on the right and the left iliac fossae
MATERIALS AND METHODS
Study design and setting
This ambispective cohort study was done in a tertiary care hospital. The study protocol was approved by the Institute Ethics Committee (IEC) in August 2021. The study was registered in the clinical trial registry India (CTRI/2021/09/036473). Till August 2021 (time of IEC approval), we performed PLND after cystectomy as a departmental protocol. The required data of these patients were collected from prospectively maintained operative notes and departmental records (Group 1). After August 2021, we performed PLND before cystectomy. The data of these patients were collected prospectively (Group 2). The primary objective was to compare the total operative time among the two groups. Secondary objectives included comparing the cystectomy time, PLND time, number of dissected lymph nodes, and the estimated blood loss among the two groups. The ancillary analysis compared the abdominal drain indwelling time, length of hospital stays, and surgical complications among the two groups. The calculated sample size required 22 patients in each group to show a difference of 45 min in the primary outcome between the groups with a power of 80% and an alpha error of 5%. [Supplementary file].
Patient population
All patients who underwent LRC + extracorporeal ileal conduit between January 2019 and June 2022 at the study center were eligible for inclusion. Patients who required total urethrectomy were converted to open surgery and whose data were missing from the database were excluded from the study. Written informed consent was obtained from all the patients. The study procedure adhered to the ethical guidelines of the declaration of Helsinki.
Surgical procedure
The standard five-port technique was used [Figure 1c]. Three surgeons who were well-versed in the surgeries performed the surgeries. In patients who underwent cystectomy first, the ureters were identified at the pelvic brim and dissected till the vesicoureteric junction. Posterior bladder dissection along the Denonvilliers fascia extended distally up to the prostatic apex. Lateral dissection was carried out till the endopelvic fascia. The vascular pedicles were sealed and cut using THUNDERBEAT® (Olympus Medical and Surgical Systems, USA) vessel sealer. The anterior dissection freed the bladder’s apex and the urachus from the anterior abdominal wall. The dorsal venous complex was suture ligated and transected. The endopelvic fascia was incised on both sides, and the dissection continued till the prostatic apex circumferentially. Both the ureters were clipped and transected at this moment near the vesicoureteral junction. The urethra was transected at the prostatic apex taking adequate care to avoid spillage. An extended template was used for PLND. Presacral lymph nodes were not included in our template.
Apart from the sequence, similar steps were followed in patients undergoing PLND first. The vascular pedicles of the bladder were sealed and cut during PLND. Cystectomy was done after the completion of lymphadenectomy. In females, a hysterectomy with anterior vaginal wall excision was also a part of the procedure. A midline infraumbilical incision was used for specimen extraction and ileal conduit formation (extracorporeal).
Outcome measures and data collection
The total operating time was taken from the initial port placement till the completion of surgery. PLND time was from the start of PLND till its completion. Cystectomy time was from the beginning of the cystectomy till its completion. Expected blood loss estimation was based on the number of gauze pieces and surgical sponges used, the degree of their soakage, and the blood sucked out. Pathological examination revealed the number of lymph nodes dissected. Surgical complications were classified according to the Clavien–Dindo system. For Group 1, the data were taken from the prospectively recorded case files, Operative notes, discharge summaries, and recorded operative videos. For Group 2, the required data were collected prospectively.
Data management and statistical analysis
The authors confirm the availability of, and access to, all original data reported in this study. Categorical data were represented as frequency (percentage), while quantitative data were presented as mean (standard deviation) for normal distribution or median (range) for skewed distribution. Student’s t-test was used for continuous variables with normal distribution and Mann–Whitney U test for skewed distribution. Chi-square (χ2) test/Fisher’s exact test was used for categorical variables. Statistical significance was set at P < 0.05. IBM Corp. SPSS Statistics version 25 software®, Armonk, NY, USA was utilized for data analysis.
RESULTS
A total of 31 patients underwent LRC with extracorporeal ileal conduit formation from January 2019 to August 2021. They were screened for inclusion in the retrospective arm of the study. All these patients underwent cystectomy followed by PLND (Group 1). Data on nine patients were incomplete and were excluded. After August 2021, we performed PLND before cystectomy (Group 2). Data on 22 consecutive patients were collected prospectively. A total of 44 patients were included in this study with workflow as mentioned below.
Baseline characteristics
The baseline characteristics of the patient in the two groups are provided in Table 1. All the baseline characteristics were statistically similar except for the prevalence of diabetes mellitus, which was more in Group 1 (36.4% vs. 6.06%, P = 0.02).
Table 1.
Comparing the baseline characteristics and tumor characteristics of the two groups
| Characteristics | Group 1 | Group 2 | P |
|---|---|---|---|
| Number of patients (n) | 22 | 22 | |
| Age (years), mean±SD | 57.95±9.97 | 57.95±12.0 | 1.0 (Student’s t-test) |
| Sex, n (%) | |||
| Male | 22 (100) | 19 (86) | 0.23 (Fisher’s exact test) |
| Female | 0 | 3 (13.6) | |
| BMI, mean±SD | 23.69±2.58 | 23.36±2.61 | 0.67 (Student’s t-test) |
| Diabetes mellitus, n (%) | 8 (36.4) | 1 (4.54) | 0.02 (Fisher’s exact test) |
| Hypertension, n (%) | 8 (36.4) | 5 (22.7) | 0.32 (Pearson’s Chi-Square test) |
| Stroke, n (%) | 0 | 0 | - |
| Coronary artery disease, n (%) | 0 | 0 | - |
| Chronic obstructive pulmonary disease, n (%) | 10 (45.5) | 4 (18.2) | 0.1 (Fisher’s exact test) |
| Smoking, n (%) | 14 (63.63) | 11 (50) | 0.36 (Pearson’s Chi-square test) |
| Smokeless tobacco use, n (%) | 9 (40.9) | 12 (54.54) | 0.35 (Pearson’s Chi-square test) |
| Aniline dye exposure, n (%) | 4 (18.18) | 0 (0) | 0.11 (Fisher’s exact test) |
| Pelvic radiation exposure, n (%) | 0 (0) | 0 (0) | - |
| Type of tumor, n (%) | |||
| Pure urothelial carcinoma | 18 (81.81) | 18 (81.81) | 0.57 (Fisher’s exact test) |
| Urothelial carcinoma with divergent differentiation | 3 (13.63) | 3 (13.63) | |
| Squamous cell carcinoma | 0 | 1 (4.54) | |
| Adenocarcinoma | 1 (4.54) | 0 (0) | |
| Tumor number, n (%) | |||
| Single | 15 (68.18) | 18 (81.82) | 0.48 (Fisher’s exact test) |
| Multiple | 7 (31.81) | 4 (18.18) | |
| Complete clearance | 10 (45.45) | 7 (31.81) | 0.35 (Pearson’s Chi-square test) |
| Bladder clot | 5 (22.72) | 2 (9.09) | 0.41 (Fisher’s exact test) |
| Pathological stage, n (%) | |||
| Ta | 1 (4.54) | 2 (9.09) | 0.62 (Fisher’s exact test) |
| T1 | 6 (27.27) | 4 (18.18) | |
| T2 | 12 (54.54) | 11 (50) | |
| T3a | 1 (4.54) | 4 (18.18) | |
| T3b | 1 (4.54) | 1 (4.54) | |
| T4a | 1 (4.54) | 0 | |
| Surgical margin positivity | 0 (0) | 0 (0) | - |
| Pathological lymph node positivity | 1 (4.54) | 0 | 1.0 (Fisher’s exact test) |
BMI=Body mass index, SD=Standard deviation
Tumor characteristics
Tumor characteristics are given in Table 1. Pure urothelial carcinomas predominated in both groups (81.81% in both groups), followed by urothelial carcinomas with different histologies (13.63% in both groups). Fifteen patients (68.18%) in Group 1 and 18 (81.82%) in Group 2presented with a single tumor. During the first transurethral resection of bladder tumor, only 10 patients (45.45%) in Group 1 and 7 (31.81%) in Group 2 had visual clearance of the tumor.
Primary and secondary outcome measures
The mean total operative time was 344.23 ± 41.58 min in Group 1 and 326.95 ± 43.63 min in Group 2. The mean difference of 17.27 min (95% confidence interval [CI]: −8.8–43.2) was not statistically significant (P = 0.19). Cystectomy time had a skewed distribution; hence, the median was taken as a measure of central tendency. The median cystectomy times were 117 min (range: 85–245) in Group 1 and 118 min (range: 59–228) in Group 2, respectively, which were statistically similar (P = 0.53). Likewise, the PLND times were also similar (126.82 ± 18.75 min in Group 1 vs. 119.36 ± 23.34 min in Group 2, P = 0.25; mean difference 7.25 min [95% CI − 5.42–20.33]). The mean number of lymph nodes removed, the estimated blood loss, the median time to drain removal, and the median length of hospital stay were also statistically similar in both groups [Table 2].
Table 2.
Comparing the primary and secondary outcomes of the two groups
| Outcome measures | Group 1 | Group 2 | P |
|---|---|---|---|
| Total operative time (min) | |||
| Mean±SD | 344.23±41.58 | 326.95±43.63 | 0.19 (Student’s t-test) |
| Minimum–maximum | 275–429 | 233–389 | |
| Cystectomy time (min) | |||
| Mean±SD | 119.36±34.44 | 120.91±35.16 | 0.53 (Mann–Whitney U-test) |
| Median (minimum–maximum) | 117 (85–245) | 118 (59–228) | |
| PLND time (min) | |||
| Mean±SD | 126.82±18.75 | 119.36±23.34 | 0.25 (Student’s t-test) |
| Minimum–maximum | 94–169 | 74–176 | |
| Expected blood loss (mL) | |||
| Mean±SD | 620.45±96.23 | 642.27±131.81 | 0.2 (Student’s t-test) |
| Minimum–maximum | 450–900 | 330–900 | |
| Number of lymph nodes (n) | |||
| Mean±SD | 13.27±4.86 | 14.5±4.76 | 0.40 (Student’s t-test) |
| Minimum–maximum | 6–26 | 6–25 | |
| Time to drain removal (days) | |||
| Mean±SD | 12±2.51 | 12.33±3.4 | 0.96 (Mann–Whitney U-test) |
| Median (minimum–maximum) | 12 (7–17) | 11.5 (7–24) | |
| Length of hospital stay (days) | |||
| Mean±SD | 15.76±4.24 | 14.86±6.98 | 0.11 (Mann–Whitney U-test) |
| Median (minimum–maximum) | 11 (11–26) | 13 (11–45) | |
| Clavien–Dindo classification of complications | |||
| Grade 1 (n) | 9 | 8 | |
| Superficial wound infection | 2 | 1 | 0.75 (Pearson’s Chi-square test) |
| Lymphorrhea | 2 | 1 | |
| Postoperative paralytic ileus | 2 | 1 | |
| Postoperative fever | 3 | 4 | |
| Diarrhea | 0 | 1 | |
| Grade 2 (n) | 8 | 8 | |
| Pneumonia | 1 | 1 | 0.91 (Pearson’s Chi-square test) |
| Blood transfusions | 6 | 5 | |
| Parenteral nutrition | 0 | 1 | |
| Pyelonephritis | 1 | 1 | |
| Grade 3a (n) | 1 | 5 | |
| Lymphocele requiring pigtail drainage | 1 | 1 | 0.19 (Fisher’s exact test) |
| Stoma mucocutaneous dehiscence requiring suturing | 0 | 1 | |
| PCN insertion for urinary diversion | 0 | 1 | |
| Deep surgical site infection with wound dehiscence | 0 | 2 | |
| Grade 3b (n) | 1 | 1 | |
| Small bowel obstruction | 1 | 0 | 1.0 (Fisher’s exact test) |
| Ureteral-ileal conduit anastomotic leak | 0 | 1 | |
| Grade 4a | 0 | 0 | - |
| Grade 4b | 0 | 0 | - |
| Grade 5 | 0 | 0 | - |
SD=Standard deviation, PLND=Pelvic lymph node dissection, PCN=Percutaneous nephrostomy
Surgical complications
Forty-one complications were recorded in 21/44 patients (47.72%). Of the total complications, 19/41 (46.34%) were in Group 1 and 22/41 (53.65%) were in Group 2. Most complications belonged to low grades (Grades 1 and 2) in both groups. The complication rates were statistically similar in both groups across all the grades of complications [Table 2].
DISCUSSION
PLND is an integral part of radical cystectomy (RC) and can be done before or after cystectomy. However, its optimal timing during LRC is debatable. Both options have certain purported advantages, according to their proponents. Early PLND bares the lateral pedicles of the bladder, which might make the subsequent steps of cystectomy easier and without significant blood loss.[9] The disadvantages of performing PLND before RC result from the narrow space in the pelvis, especially in patients with sizeable solid bladder tumors, making the dissection difficult during PLND. On the other hand, performing PLND after cystectomy may give the advantage of a wide working area in the narrow pelvic cavity, and because the major blood vessels are easily identified, PLND can be performed easily.
In our study, a mean difference in the total operating time was 17.27 min (95% CI: −8.8–43.2) between the two groups. With a P value of 0.19, the timing of the lymphadenectomy had no impact on the total length of the surgery. The median cystectomy and mean PLND times were also statistically similar in both groups. Salih Boga et al., in their series on robotic RC, reported that the mean operating time was identical when PLND was done before versus when done after cystectomy (515.00 ± 75.024 min vs. 562.86 ± 35.923 min; P = 0.14).[10] Contrary to these findings, Ozen et al., in their study on open RC and ileal conduit formation, reported that the mean cystectomy time and the mean total operating time were significantly shorter when PLND was done first.[9] They also noted that performing PLND first required more time, though it was not statistically significant. The authors claimed that the full skeletonization of the bladder pedicles during PLND, which made the cystectomy simpler, was responsible for reducing the total operating time by 33 min and the cystectomy time by 40 min. We used THUNDERBEAT® (Olympus Medical and Surgical Systems, USA) vessel sealer for dissection and hemostasis. THUNDERBEAT reduced the need for meticulous dissection and ligation of the vascular pedicles. It is most likely the cause of the lack of a discernible difference between PNLD performed before cystectomy and PLND performed following cystectomy in terms of the mean total surgical time and cystectomy time.
Ozen et al. reported that in open RC, the mean number of lymph nodes removed was lower in the group where ePLND was carried out before cystectomy than after cystectomy.[9] On subgroup analysis, the difference was found to be statistically significant only in the number of presacral lymph nodes. Contrary to this finding, Salih Boga et al., in their study on robotic RC, reported a lower lymph node yield when PLND was done after cystectomy.[10] The authors stated that the low yield of lymph nodes was possibly due to those surgeries during their early learning curve. In our study, the mean number of lymph nodes dissected in both groups was similar. We opted not to remove the presacral lymph nodes while using the EAU-extended PLND template due to a low risk of metastasis. Since presacral lymph nodes are excluded, the alleged advantageous effect of early cystectomy on the number of dissected lymph nodes was not observed. The average number of lymph nodes removed in both groups was >10, which is sufficient for accurate staging and to improve survival.[8]
The overall mean estimated blood loss was about 630 ml and was statistically similar in both groups. The blood loss in our patients was slightly more than that reported previously in many series, which is typically <500 ml. The most crucial elements impacting the length of hospital stay are the surgical technique, complication rates, and their severity. Our practice was to try ureteral stent removal 1 week following the procedure. If the drain output did not rise and was <50 ml/day, the abdominal drain was removed 1 day after the ureteral stent removal. Respecting the socioeconomic aspects and societal customs, patients were discharged home once fit and only after the abdominal drain was removed. The median time to drain removal and the length of hospital stay were similar in both groups. Our findings were comparable to those of a previous study by Patidar et al. and a systematic review by Tang et al. The majority of the complications were Grades 1 and 2 in severity in both groups.[11,12] Group 2 had higher Grade 3 problems, albeit this difference was not statistically significant. Our study’s overall incidence of high-grade complications (Grade 3 or more) was around 25%. A large multi-center study by Hirobe et al. also reported similar “high grade” complication rates of 22%.[13] Randomized studies and systematic review have demonstrated that minimally invasive RC results in less blood loss and a shorter hospital stay than open RC, but the incidence of significant complications is the same in both approaches.[11,14,15]
Our study has limitations. It is an observational study from a single center. Due to the ambispective nature, half of the patients came from the retrospective arm, which might be a portal for bias. Furthermore, female patients were present only in Group 2 and could have influenced the operative time. No questionnaire was used to document the operating surgeon’s opinion about the ease of performing surgery. Lymph nodes from each side were not sent separately by their respective stations for histopathological examination. Lymph node examination according to their stations improves yield and depicts disease spread pattern. However, our study sparks interest in determining the optimal timing of PLND during RC. Larger, multi-institutional studies in a randomized controlled trial setting may provide a definitive answer.
CONCLUSIONS
The timing of PLND during LRC had no discernible impact on the duration of the entire operation, the duration of cystectomy, or the duration of PLND. The operative outcomes, namely, the number of lymph nodes dissected, estimated blood loss, and the early complication rates, were also not influenced by the timing of PLND. Hence, we conclude that the ease of doing surgery and the operative outcomes are unaffected by the timing of PLND during LRC and could be left to surgeon’s discretion till better data from an RCT is available.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
SUPPLEMENTARY FILE
Sample size calculation- Detail
The sample size for the study was calculated for finding a meaningful difference in the total operating time as the primary outcome with PLND after cystectomy as Group 1 and PLND before cystectomy as Group 2.
The following assumptions were considered to calculate the sample size:
Anticipated mean total operating time in Group 1 (PLND after cystectomy) – 562 min. (Taken from a prior study by Mehmet Salih Boga et al. which is cited in the main article)
Anticipated mean total operating time in Group 2 (PLND before cystectomy) – 513 min. (i.e., Affect size of at least 45 min was set by the researchers as a meaningful difference)
Assumed pooled value of the standard deviations for both groups – 55 min (Taken from a prior study by Mehmet Salih Boga et al.)[10]
Confidence level - 95%
Power - 80%
Allocation ratio 1:1.
The sample size was calculated to compare two means “Statulator” online sample size calculator (Dhand, N. K., and Khatkar, M. S. (2014). Statulator: An online statistical calculator. Sample Size Calculator for Comparing Two Independent Means. Assessed at http://statulator.com/SampleSize/ss2M.html).
The calculated sample size was 22 in each group.
Previous intravesical therapy
| Type of Intravesical therapy | Group 1 | Group 2 |
|---|---|---|
| Intravesical BCG (n) | 3 | 3 |
| Intravesical chemotherapy (n) | 0 | 0 |
BCG=Bacillus–calmette Guerin
REFERENCES
- 1.Bi L, Huang H, Fan X, Li K, Xu K, Jiang C, et al. Extended versus non-extended pelvic lymph node dissection and their influence on recurrence-free survival in patients undergoing radical cystectomy for bladder cancer: A systematic review and meta-analysis of comparative studies. BJU Int. 2014;113:E39–48. doi: 10.1111/bju.12371. [DOI] [PubMed] [Google Scholar]
- 2.Stein JP, Lieskovsky G, Cote R, Groshen S, Feng AC, Boyd S, et al. Radical cystectomy in the treatment of invasive bladder cancer: Long-term results in 1,054 patients. J Clin Oncol. 2001;19:666–75. doi: 10.1200/JCO.2001.19.3.666. [DOI] [PubMed] [Google Scholar]
- 3.Zehnder P, Moltzahn F, Mitra AP, Cai J, Miranda G, Skinner EC, et al. Radical cystectomy with super-extended lymphadenectomy: Impact of separate versus en bloc lymph node submission on analysis and outcomes. BJU Int. 2016;117:253–9. doi: 10.1111/bju.12956. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Poulsen AL, Horn T, Steven K. Radical cystectomy: Extending the limits of pelvic lymph node dissection improves survival for patients with bladder cancer confined to the bladder wall. J Urol. 1998;160:2015–9. [PubMed] [Google Scholar]
- 5.Simone G, Papalia R, Ferriero M, Guaglianone S, Castelli E, Collura D, et al. Stage-specific impact of extended versus standard pelvic lymph node dissection in radical cystectomy. Int J Urol. 2013;20:390–7. doi: 10.1111/j.1442-2042.2012.03148.x. [DOI] [PubMed] [Google Scholar]
- 6.Holmer M, Bendahl PO, Davidsson T, Gudjonsson S, Månsson W, Liedberg F. Extended lymph node dissection in patients with urothelial cell carcinoma of the bladder: Can it make a difference? World J Urol. 2009;27:521–6. doi: 10.1007/s00345-008-0366-9. [DOI] [PubMed] [Google Scholar]
- 7.Rai BP, Bondad J, Vasdev N, Adshead J, Lane T, Ahmed K, et al. Robotic versus open radical cystectomy for bladder cancer in adults. Cochrane Database Syst Rev. 2019;4 doi: 10.1002/14651858.CD011903.pub2. CD011903. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Wright JL, Lin DW, Porter MP. The association between extent of lymphadenectomy and survival among patients with lymph node metastases undergoing radical cystectomy. Cancer. 2008;112:2401–8. doi: 10.1002/cncr.23474. [DOI] [PubMed] [Google Scholar]
- 9.Ozen H, Ugurlu O, Baltaci S, Adsan O, Aslan G, Can C, et al. Extended pelvic lymph node dissection: Before or after radical cystectomy?. A multicenter study of the Turkish society of urooncology. Korean J Urol. 2012;53:451–6. doi: 10.4111/kju.2012.53.7.451. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Salih Boga M, Ates M. Timing of lymphadenectomy during robot-assisted radical cystectomy: Before or after cystectomy?. Fifteen cases with totally intracorporeal urinary diversions. Wideochir Inne Tech Maloinwazyjne. 2020;15:596–601. doi: 10.5114/wiitm.2020.93793. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Tang K, Li H, Xia D, Hu Z, Zhuang Q, Liu J, et al. Laparoscopic versus open radical cystectomy in bladder cancer: A systematic review and meta-analysis of comparative studies. PLoS One. 2014;9:e95667. doi: 10.1371/journal.pone.0095667. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Patidar N, Yadav P, Sureka SK, Mittal V, Kapoor R, Mandhani A. An audit of early complications of radical cystectomy using Clavien-Dindo classification. Indian J Urol. 2016;32:282–7. doi: 10.4103/0970-1591.191244. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Hirobe M, Tanaka T, Shindo T, Ichihara K, Hotta H, Takahashi A, et al. Complications within 90 days after radical cystectomy for bladder cancer: Results of a multicenter prospective study in Japan. Int J Clin Oncol. 2018;23:734–41. doi: 10.1007/s10147-018-1245-z. [DOI] [PubMed] [Google Scholar]
- 14.Khan MS, Omar K, Ahmed K, Gan C, Van Hemelrijck M, Nair R, et al. Long-term oncological outcomes from an early phase randomised controlled three-arm trial of open, robotic, and laparoscopic radical cystectomy (CORAL) Eur Urol. 2020;77:110–8. doi: 10.1016/j.eururo.2019.10.027. [DOI] [PubMed] [Google Scholar]
- 15.Parekh DJ, Reis IM, Castle EP, Gonzalgo ML, Woods ME, Svatek RS, et al. Robot-assisted radical cystectomy versus open radical cystectomy in patients with bladder cancer (RAZOR): An open-label, randomised, phase 3, non-inferiority trial. Lancet. 2018;391:2525–36. doi: 10.1016/S0140-6736(18)30996-6. [DOI] [PubMed] [Google Scholar]