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Complications After Robot-assisted Radical Cystectomy: Results from the International Robotic Cystectomy Consortium
European Urology, 1, 64, pages 52 - 57
Complication reporting is highly variable and nonstandardized. Therefore, it is imperative to determine the surgical outcomes of major oncologic procedures.
To describe the complications after robot-assisted radical cystectomy (RARC) using a standardized and validated reporting methodology.
Design, setting, and participants
Using the International Robotic Cystectomy Consortium (IRCC) database, we identified 939 patients who underwent RARC, had available complication data, and had at least 90 d of follow-up.
Outcome measurements and statistical analysis
Complications were analyzed and graded according to the Memorial Sloan-Kettering Cancer Center (MSKCC) system and were defined and stratified by organ system. Secondary outcomes included identification of preoperative and intraoperative variables predicting complications. Logistic regression models were used to define predictors of complications and readmission.
Results and limitations
Forty-one percent (n = 387) and 48% (n = 448) of patients experienced a complication within 30 and 90 d of surgery, respectively. The highest grade of complication was grade 0 in 52%, grade 1–2 in 29%, and grade 3–5 in 19% patients. Gastrointestinal, infectious, and genitourinary complications were most common (27%, 23%, and 17%, respectively). On multivariable analysis, increasing age group, neoadjuvant chemotherapy, and receipt of blood transfusion were independent predictors of any and high-grade complications, respectively. Thirty and 90-d mortality was 1.3% and 4.2%, respectively. As a multi-institutional database, a disparity in patient selection, operating standards, postoperative management, and reporting of complications can be considered a major limitation of the study.
Surgical morbidity after RARC is significant when reported using a standardized reporting methodology. The majority of complications are low grade. Strict reporting of complications is necessary to advocate for radical cystectomy (RC) and helps in patient counseling.
Keywords: Robot-assisted, Robotic, Robot, Radical cystectomy, Complications, Outcomes.
Surgical management has a significant role in determining the final outcome of patients with muscle-invasive and recurrent non–muscle-invasive bladder cancer (BCa)  . Radical cystectomy (RC) is considered the gold-standard treatment, and despite undergoing various modifications to achieve the optimal outcome for patients in terms of cost-effectiveness, cancer control, and postoperative complications, it remains a morbid procedure with a variable complication rate , , , , and . Early oncologic outcomes of robot-assisted RC (RARC) reported by a limited number of specialized centers appear similar to RC, with an effort to reduce procedure-related complications. In 2003, Menon first reported his series of RARC as a minimally invasive approach toward attaining this goal, followed by various case series with limited complication details , , and .
The reported complication rates following open RC vary from 24% to 64%, which likely results from a nonstandardized reporting method. More recently, however, most studies have adopted a uniform method of documenting complications  and  as a standardized approach toward postoperative complication reporting is essential to allow meaningful comparisons between minimally invasive and open techniques of RC and to appropriately counsel patients. This approach has been adopted in reporting RARC complications, and the rates vary between 34% and 52% , , and . These studies, however, represent a single institution or surgeon, where surgical volume and surgeon expertise may influence outcomes. For this reason, multi-institutional databases or population-based data are necessary to compare outcomes between surgical approaches. To this end, a recent observational cohort study using the US Nationwide Inpatient Sample found that the inpatient complication rate was lower with RARC, although costs were higher  . The purpose of this study was to characterize the incidence, type, and severity of postoperative complications after RARC using an international, multi-institutional database. In addition, we sought to identify risk factors for complications after RARC, readmission, and 90-d mortality.
2. Patients and methods
2.1. International Robotic Cystectomy Consortium database
A retrospectively reviewed, prospectively maintained institutional review board (I 97906)–approved database of the International Robotic Cystectomy Consortium (IRCC) is an effort of >20 institutions comprising >1200 patients treated with RARC for clinically localized BCa from 2003 to date. The IRCC collaborative effort enables all participating institutions to monitor their progress and share various aspects of evolving novel techniques.
2.2. Study design
Clinical, pathologic, and standardized complication data were available from 939 patients who underwent RARC at 16 participating institutions. Data were collected on clinical and pathologic characteristics. The technique used for RARC and pelvic lymph node dissection varied according to the individual surgeon and institution. Urinary diversion was performed via an extra- or intracorporeal approach.
All complications were retrospectively identified by review of inpatient and outpatient notes, imaging findings, and physician correspondence. Complications defined were graded according to the Memorial Sloan-Kettering Cancer Center (MSKCC) system  , an established five-grade modification of the Clavien system  . The criteria that Martin et al. proposed for reporting complications related to surgery were used  . Complications were further grouped into 12 categories by organ system and categorized into low grade (grades 1–2) and high grade (grades 3–5). The secondary outcome of the study was to identify preoperative and intraoperative variables that predicted any and high-grade complications as well as predictors of hospital readmission and 90-d mortality.
2.3. Statistical analysis
Statistical analysis was performed using the Fisher exact test to summarize categoric variables and the Wilcoxon rank sum test or Kruskal-Wallis test for continuous variables. Logistic regression analysis was performed to evaluate predictors of at least one complication of any grade. Separate analyses were performed for high-grade (grade 3–5) complications. Models were fitted separately for preoperative and intraoperative variables. Variables analyzed included gender, age (10-yr age group), body mass index (BMI), neoadjuvant chemotherapy, case number, overall operative time, estimated blood loss (EBL), transfusion status (yes/no), type of urinary diversion (continent vs conduit), location of urinary diversion (extra- vs intracorporeally), and American Society of Anesthesiologists (ASA) score (≤2 vs >2). Logistic regression analysis was also used to evaluate predictors of 90-d mortality and readmission within 90 d. Statistical analyses were performed using Stata v.11.0 (StataCorp, College Station, TX, USA).
Data from 939 patients were available at the time of final analysis. Preoperative characteristics, pathologic and perioperative outcomes are detailed in Table 1 . The median age was 68 yr of age (interquartile range [IQR]: 60–76), and median BMI was 27 kg/m2 (IQR: 24–30). Fifty-three percent had ASA scores ≥3. Thirty-two percent had a continent diversion. The mean EBL was 580 ml (range: 20–3900), and 15% of the patients received an intraoperative blood transfusion. The median hospital stay was 8 d (IQR: 6–12).
|Mean ± SD||67.4 ± 11|
|Median (range)||68 (26–92)|
|Gender, no. (%):|
|Mean ± SD||27.5 ± 5.4|
|Obese (>30), no. (%)||249 (27)|
|≥3, no. (%)||461 (53)|
|Prior abdominal surgery, no. (%)||416 (47)|
|Neoadjuvant chemotherapy, no. (%)||138 (16)|
|Preoperative radiation, no. (%)||15 (2)|
|Diversion type, no. (%):|
|Ileal conduit||613 (68)|
|Diversion location, no. (%):|
|Pathologic tumor stage, no. (%):|
|Organ confined:||423 (49)|
|pTa, T1, Tis||243 (28)|
|Non–organ confined:||351 (41)|
|Soft tissue margin positive, no. (%)||84 (9)|
|Lymph node yield:|
|Mean ± SD||18.1 ± 12.4|
|≥20, no. (%)||363 (42)|
|Lymph node positive, no. (%)||237 (26)|
|Mean ± SD||14 ± 15|
|Median (IQR)||9 (3–20)|
|Mean ± SD||580 ± 411|
|Median (IQR)||400 (200–600)|
|Intraoperative transfusion, no. (%)||133 (15)|
|ICU stay, d:|
|Mean ± SD||1 ± 2.8|
|Median (IQR)||0 (0–1)|
|Hospital stay, d:|
|Mean ± SD||11 ± 8|
|Median (IQR)||8 (6–12)|
|30-d readmission, no. (%)||120 (13)|
|90-d readmission, no. (%)||190 (20)|
SD = standard deviation; BMI = body mass index; ASA = American Society of Anesthesiologists; IQR = interquartile range; EBL = estimated blood loss; ICU = intensive care unit.
Forty-eight percent (n = 448) of patients had a complication within 90 d of surgery. Twenty-nine percent (n = 273) of patients had grade 1–2 (low-grade) and 19% (n = 175) had grade 3–5 (high-grade) as their highest grade of complication. Twenty-seven percent, 23%, and 17% of patients most commonly developed gastrointestinal, infectious, and genitourinary complications based on the specific organ system, respectively ( Table 2 ). Fifty-three patients required reoperation within 30 d of RARC. Data were available for 47 of the 53 patients who returned to the operating room. The indications for reoperation are listed in Table 3 . The most common reasons for reoperation include fascial dehiscence (n = 12), small bowel obstruction (SBO) or partial SBO (n = 8), urine leak (n = 7), and bleeding (n = 5).
|Organ system||Complications, no. (%)|
|Hematologic or vascular||97 (10)|
|Wound or skin||53 (5)|
|Head and neck||5 (1)|
|Fascial dehiscence (n = 12)|
|SBO or partial SBO (n = 8)|
|Urine leak (n = 7)|
|Bleeding (n = 5)|
|Bowel injury (n = 3)|
|Ureteral stent malposition (n = 3)|
|Compartment syndrome (n = 2)|
|Possible ischemic bowel—ex lap|
|Suspected bleeding—ex lap|
|Displaced stent—lap retrieval|
|Incision and drainage of wound infection|
SBO = small bowel obstruction.
On multivariable analysis, 10-yr age group and receipt of neoadjuvant chemotherapy were independent predictors of any and high-grade complications, respectively, while smoking was associated with high-grade complications alone. Using intraoperative variables, receipt of a blood transfusion was an independent predictor of any and high-grade complications ( Table 4 ). Type of lymph node dissection (none, standard, extended) was not associated with any (odds ratio [OR]: 1.17; 95% confidence interval [CI], 0.88–1.56; p = 0.275) or high-grade (OR: 1.21; 95% CI, 0.91–1.61; p = 0.194) complications. Twenty percent of patients required readmission within 90 d of surgery. The overall mortality rate was 1.3% and 4.2% for 30 and 90 d, respectively. On multivariable analysis, increasing age group and receipt of an intraoperative transfusion were found to be related to 90-d mortality ( Table 5 ). BMI was a predictor of hospital admission within 90 d (OR: 1.03; 95% CI, 1.00–1.06; p = 0.027).
|Any complication grade 1–5||Complication grade 3–5|
|OR (95% CI)||p value||OR (95% CI)||p value|
|(A) Preoperative variables—univariable analysis|
|Gender (female vs male)||0.94 (0.68–1.30)||0.723||0.71 (0.46–1.11)||0.132|
|Age at surgery (10-yr interval) §||1.27 (1.11–1.45)||0.001||1.23 (1.04–1.46)||0.016|
|BMI, kg/m2||1.02 (1.00–1.05)||0.032||1.02 (0.99–1.05)||0.138|
|Obese (BMI >30 kg/m2, yes/no)||1.26 (0.94–1.69)||0.119||1.14 (0.80–1.65)||0.463|
|Neoadjuvant chemotherapy (yes/no)||1.56 (1.08–2.24)||0.018||1.69 (1.10–2.58)||0.016|
|Current smoker (yes/no)||1.07 (0.78–1.47)||0.659||1.34 (0.91–1.97)||0.139|
|ASA score (3–4 vs 1–2)||1.33 (1.02–1.74)||0.036||1.44 (1.02–2.04)||0.038|
|(B) Preoperative variables—multivariable analysis|
|Gender (female vs male)||0.91 (0.65–1.29)||0.605||0.67 (0.42–1.07)||0.097|
|Age at surgery (10-yr interval)||1.34 (1.14–1.57)||<0.001||1.39 (1.13–1.71)||0.002|
|BMI, kg/m2||1.04 (1.01–1.07)||0.006||1.04 (1.00–1.07)||0.024|
|Neoadjuvant chemotherapy (yes/no)||1.71 (1.16–2.53)||0.007||1.88 (1.20–2.94)||0.006|
|Current smoker (yes/no)||1.34 (0.95–1.89)||0.100||1.68 (1.09–2.57)||0.018|
|ASA score (3–4 vs 1–2)||1.05 (0.78–1.40)||0.752||1.10 (0.76–1.61)||0.611|
|(C) Intraoperative variables—univariable analysis|
|Operating room time (≤5, 5–7, >7 h)||1.29 (1.07–1.57)||0.008||1.15 (0.89–1.47)||0.276|
|EBL (≤300, 301–600, >601 ml)||1.22 (1.03–1.45)||0.020||1.16 (0.94–1.44)||0.165|
|Transfusion (yes/no)||2.23 (1.52–3.28)||<0.001||1.92 (1.25–2.95)||0.003|
|Type of urinary diversion (continent vs conduit)||1.26 (0.95–1.66)||0.107||1.13 (0.80–1.61)||0.479|
|Location of diversion (intra- vs extracorporeal)||0.67 (0.49–0.92)||0.012||1.03 (0.69–1.54)||0.868|
|(D Intraoperative variables—multivariable analysis|
|Operating room time (≤5, 5–7, >7 h)||1.14 (0.90–1.43)||0.288||1.04 (0.77–1.42)||0.782|
|EBL (≤300, 301–600, >601 ml)||1.06 (0.86–1.30)||0.592||1.01 (0.78–1.31)||0.947|
|Transfusion (yes/no)||1.84 (1.19–2.84)||0.006||1.94 (1.18–3.17)||0.009|
|Type of urinary diversion (continent vs conduit)||1.44 (1.02–2.03)||0.036||1.18 (0.77–1.80)||0.454|
|Location of diversion (intra- vs extracorporeal)||0.83 (0.57–1.21)||0.327||1.16 (0.72–1.86)||0.549|
§ Age categories (<60, 61–70, 71–80, ≥81); separate multivariable models fitted for preoperative variables (A, B) and intraoperative variables (C, D).
OR = odds ratio; CI = confidence interval; BMI = body mass index; ASA = American Society of Anesthesiologists; EBL = estimated blood loss.
|Variables analyzed *||Outcome|
|OR (95% CI)||p value|
|(A) Preoperative variables—univariable analysis|
|Gender (female vs male)||0.86 (0.37–1.99)||0.729|
|Age at surgery (10-yr interval)||1.53 (1.09–2.14)||0.013|
|BMI, kg/m2||0.95 (0.90–1.03)||0.222|
|Obese (BMI >30 kg/m2, yes/no)||0.57 (0.25–1.31)||0.188|
|Neoadjuvant chemotherapy (yes/no)||1.67 (0.78–3.61)||0.187|
|Current smoker (yes/no)||1.48 (0.73–2.97)||0.274|
|ASA score (3–4 vs 1–2)||2.53 (1.22–5.29)||0.013|
|(B) Preoperative variables—multivariable analysis|
|Gender (female vs male)||0.88 (0.38–2.05)||0.766|
|Age at surgery (10-yr interval)||1.62 (1.08–2.43)||0.018|
|BMI, kg/m2||0.97 (0.91–1.04)||0.362|
|Neoadjuvant chemotherapy (yes/no)||1.91 (0.86–4.28)||0.114|
|Current smoker (yes/no)||1.99 (0.91–4.37)||0.085|
|ASA score (3–4 vs 1–2)||2.01 (0.93–4.33))||0.075|
|(C) Intraoperative variables—univariable analysis|
|Operating room time (≤5, 5–7, >7 h)||1.00 (0.62–1.62)||0.985|
|EBL (≤300, 301–600, >601 ml)||1.58 (1.05–2.36)||0.027|
|Transfusion (yes/no)||4.43 (2.26–8.68)||<0.001|
|Type of urinary diversion (continent vs conduit)||0.46 (0.20–1.05)||0.066|
|Location of diversion (intra- vs extracorporeal)||0.66 (0.27–1.61)||0.363|
|(D) Intraoperative variables—multivariable analysis|
|Operating room time (≤5, 5–7, >7 h)||1.13 (0.63–2.02)||0.674|
|EBL (≤300, 301–600, >601 ml)||1.21 (0.74–1.98)||0.457|
|Transfusion (yes/no)||4.20 (1.86–9.45)||0.001|
|Type of urinary diversion (continent vs conduit)||0.52 (0.21–1.27)||0.148|
|Location of diversion (intra- vs extracorporeal)||1.16 (0.46–2.96)||0.753|
* Separate multivariable models fitted for preoperative variables (A, B) and intraoperative variables (C, D).
OR = odds ratio; CI = confidence interval; BMI = body mass index; ASA = American Society of Anesthesiologists; EBL = estimated blood loss.
This multi-institutional study delineates analysis of complications by using the largest cohort of patients undergoing RARC, advocating a standardized method of complication reporting. We report an overall complication rate of 48%; however, most of the complications were low grade when stratified according to the MSKCC grading system. The gastrointestinal system was the most common organ system involved. Age group, BMI, and neoadjuvant chemotherapy were identified as predictors of both any and high-grade complications. Among the intraoperative variables, blood transfusion was a significant predictor for experiencing a high-grade complication. Transfusion could be a surrogate marker for intraoperative blood loss, however EBL was not associated with an increased risk of postoperative complications. The 90-d mortality rate was 4.2%, with high ASA scores and intraoperative transfusion identified as significant predictors. BMI was also significantly associated with 90-d readmission.
The postoperative complication rates after RARC vary between 34% and 52%  and . Although our overall complication rate is lower, high-grade complications and 90-d mortality are higher than the rates reported for the open cystectomy  . Because IRCC is a multi-institutional data set, the operative expertise, patient selection, and quality of perioperative care could possibly be the confounding factors. In one of the largest reported multi-institutional series of RARC patients (227 patients), Smith et al. reported an overall complication rate of 30% at 30 d. The high-grade complication rate in their study was 7%, with no mortality at 30 d  . Hayn et al. reported a 52% 90-d complication rate in 156 patients, with 61% low-grade (grade 1–2) complications, using the MSKCC grading system  . In other series, the rate of low-grade complications varies from 24% to 79%  and . Ng et al. compared 104 open RC and 83 RARC cases and reported a higher complication rate in the open RC group (62% vs 48%; p = 0.07)  . On multivariable analysis, RARC was associated with an almost 50% lower risk of having any complication (p = 0.049) and an almost 60% lower risk of having a high-grade complication (p = 0.041). The study was not randomized and was therefore subject to numerous biases  . Nix et al. reported a prospective, randomized, controlled trial of robotic versus open RC and found no difference in the absolute number of complications, although the study was designed as a noninferiority study, with the primary end point of lymph node yield  . Recently, Styn et al. performed a matched comparison of RARC and open RC and found no difference in the rate of 30-d minor or major Clavien complications, length of stay, and 30-d readmissions between groups  .
With any new and innovative technology, the potential benefits must be weighed against the costs. Smith et al. performed a cost analysis and found that RARC cost $1640 more than RC  . Martin et al. developed a cost model to compare RC and RARC. In their model, which was based on their institutional data, RARC was more expensive when operating room time was >361 min, hospital length of stay (LOS) was >6.6 d, or robotic operating room supply cost exceeded $5853  . In their series, however, the mean LOS was 5 d for RARC and 10 d for open RC, which may not be applicable to many institutions. Lee et al. used a linear cost model that incorporated the indirect costs of complications and found that RC was more cost efficient for ileal conduit ($4846), but the cost benefit diminished for continent catheterizable diversion ($609) and disappeared for neobladder (−$1966)  . Yu et al. used the US Nationwide Inpatient Sample to compare RARC and open RC in 2009 and found that patients undergoing RARC experience fewer inpatient complications, deaths, and parenteral nutrition use. However, there was no difference in LOS between the groups, and RARC was $3797 most costly  .
In our study, we identified several risk factors for development of any or high-grade complications, including increasing age group, receipt of neoadjuvant chemotherapy, smoking history, and receipt of blood transfusion. Smith et al. identified lower age and high ASA score to be predictors of major complications. They attributed the higher complication rate among younger patients to the receipt of neoadjuvant chemotherapy  . The present study also identified that neoadjuvant chemotherapy was a risk factor for any and high-grade complications; however, this impact was not reported in other RC and RARC series , , , , and . Increasing age has also been associated with any and high-grade complications in other RARC and RC series  and . Guillotreau et al., however, reported on outcomes of laparoscopic RC and RARC in elderly patients and did not find a difference in complication rates between the age groups, which were defined as ≥70 yr of age and <70 yr of age  . Similar to the present study, smoking has been identified as a risk factor for postoperative morbidity in other disciplines  and . Our series recorded a mortality rate of 4.2% at 90 d, with identification of ASA scores ≥ 3 and perioperative blood transfusion as the risk factors. Other series have reported a mortality rate between 2% and 3%; however, no risk factors could be identified  and .
The overall positive margin rate in this series was 9%, which is slightly higher than contemporary open RC series. A recent multicenter RC series evaluated 4400 patients treated at 12 academic institutions (an average of 368 cases per institution) from 1980 to 2008. The group demonstrated an overall soft tissue surgical margin rate of 6.3%  . We were not able to differentiate between positive soft tissue surgical margins and positive urethral or ureteral margins within the IRCC database, and this may have contributed to the higher positive margin rate. In addition, these cases were at the beginning of the learning curve for some surgeons performing RARC.
The use of the IRCC multi-institutional database allowed us to gather RARC outcomes on a much larger scale. A prospectively maintained database of a large number of patients belonging to various institutions provides a diverse cohort of patients for better analysis. The variety of surgical expertise and operative techniques again makes this data set unique; however, this study has limitations. First, this database may contain disparities in patient selection, operating standards, postoperative management, and reporting of complications. Second, complications treated at outside institutions may have been underreported. Finally, the results cannot be translated for all urologists, as most of the cases were performed in tertiary care hospitals, where the majority of surgeons had fellowship training. Multi-institutional randomized controlled trials are needed for a detailed account of preoperative and postoperative variables. Until trial outcomes become available, prospective collection of data across various institutions needs to be developed and maintained.
Surgical morbidity after RARC is significant when reported using a standardized reporting methodology. The majority of complications are low grade. Strict reporting of complications is necessary to advocate for RC and helps in patient counseling.
Author contributions: Khurshid A. Guru had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.
Study concept and design: Guru, Hayn, Peabody.
Acquisition of data: Stegemann, Agarwal, Nepple, Pattaras, Redorta, Rha, Hemal, Weizer, Yuh, Schanne, Muhletaler.
Analysis and interpretation of data: Richstone, Saar, Scherr, Siemer, Stoekle, Woods, Wiklund, Balbay.
Drafting of the manuscript: Johar, Hayn, Stegemann, Guru.
Critical revision of the manuscript for important intellectual content: Wilson, Kibel, Nepple, Ahmed, Wiklund, Weizer, Hemal, Peabody, Hayn.
Statistical analysis: Hayn.
Obtaining funding: None.
Administrative, technical, or material support: None.
Supervision: Guru, Wiklund, Peabody.
Other (specify): None.
Financial disclosures: Khurshid A. Guru certifies that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the manuscript (eg, employment/affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: Dr Guru is a board member of Simulated Surgical Systems, LLC.
Funding/Support and role of the sponsor: None.
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a Roswell Park Cancer Institute, Buffalo, NY, USA
b Maine Medical Center, Portland, Maine, USA
c Guy's and St Thomas’ Hospitals, London, United Kingdom
d Henry Ford Health System, Detroit, MI, USA
e Ankara Ataturk Training and Research Hospital, Ankara, Turkey
f Wake Forest University, Winston-Salem, NC, USA
g Washington University School of Medicine, St. Louis, MO, USA
h Emory University School of Medicine, Atlanta, GA, USA
i Fundacio Puigvert, Barcelona, Spain
j Yonsei University Health System Severance Hospital, Seoul, South Korea
k Arthur Smith Institute for Urology, Long Island, NY, USA
l Saarland University Clinic, Homburg, Germany
m Urology Associates of Delaware, Wilmington, DE, USA
n Weil Cornell Medical College, New York, NY, USA
o University of Michigan, Ann Arbor, MI, USA
p Karolinska University, Stockholm, Sweden
q City of Hope, Duarte, CA, USA
r Loyola University Medical Center, Maywood, IL, USA
1 These authors are both first authors.
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© 2013 European Association of Urology, Published by Elsevier B.V.