A Comparison of 30-Day Perioperative Outcomes in Open Versus Minimally Invasive Nephroureterectomy for Upper Tract Urothelial Carcinoma: Analysis of 896 Patients from the American College of Surgeons-National Surgical Quality Improvement Program Database

Abstract

Background and Purpose:

Minimally invasive surgery for nephroureterectomy (MINU) in patients with upper tract urothelial carcinoma (UTUC) is increasingly used among urologists with reported equivalent oncologic outcomes compared with open nephroureterectomy (ONU). Population-level data comparing perioperative outcomes between these approaches remain limited, however. We sought to compare perioperative outcomes between MINU and ONU in a prospectively collected national cohort of patients.

Methods:

Between 2006 and 2012, patients who underwent nephroureterectomy for UTUC within the American College of Surgeons-National Surgical Quality Improvement Program database were categorized into MINU or ONU. Our primary outcome of interest was 30-day perioperative complications. Secondary outcomes included use of lymph node dissection (LND), transfusion, reintervention and readmission rate, operative time, length of stay (LOS), and perioperative mortality. Multivariable logistic regression analyses were used to examine the association between outcomes and surgical approach.

Results:

A total of 599 (66.9%) and 297 (33.1%) patients underwent MINU and ONU, respectively. Overall, 12.7% of patients experienced a complication within 30 days postoperatively, and the rate did not differ among surgical approaches. Patients in the MINU group, however, had a decreased LOS (P<0.001). On multivariable analysis, patients receiving MINU were less likely to undergo a LND (OR 0.13; P<0.001), had decreased risk of thromboembolic complications (odds ratio [OR] 0.13; P=0.018), decreased need for transfusion (OR 0.39; P=0.001), and decreased need for operative reintervention (OR 0.24; P=0.024).

Conclusions:

Patients receiving MINU have similar overall complication rates compared with ONU. MINU, however, was associated with a decreased risk of blood transfusions, thromboembolic events, reintervention, and overall LOS compared with ONU. MINU should be considered as a primary approach in select groups of patients with UTUC.

Introduction

The current “gold standard” for the management of localized upper tract urothelial carcinoma (UTUC) is open radical nephroureterectomy (ONU) with excision of bladder cuff.¹ Since the first description of laparoscopic nephroureterectomy in 1991, however, several prospective and retrospective studies have confirmed that a laparoscopic approach can be performed with equivalent oncologic outcomes.^2

–5 Added benefits of using a minimally invasive approach for nephroureterectomy (MINU) include decreased length of hospital stay, analgesic requirement, and need for blood transfusion.⁶

In this context, minimally invasive surgery, including laparoscopic and robot-assisted surgery, is increasingly being used among urologists for the management of UTUC.^7,8 Yet, questions prevail regarding the optimal surgical approach for patients with UTUC, and population-level data evaluating the perioperative outcomes of these approaches remains limited.

Several factors make the decision of choosing a particular surgical approach for the management of UTUC complicated and include: (1) Difficulty obtaining accurate preoperative staging, (2) unclear role of lymphadenectomy, (3) high rate of postoperative complications, and (4) lack of standardized guidelines for the role of neoadjuvant and adjuvant chemotherapy. Clinical staging is typically established via endoscopic biopsies and/or preoperative imaging with reported concordance between endoscopic and surgical stage of about 60% with the majority of cases being understaged preoperatively.⁹

Along the same lines, lymphadenectomy may improve staging and help risk-stratify patients postoperatively.¹⁰ Some retrospective studies, however, have demonstrated a lack of survival benefit for lymphadenectomy in UTUC.¹⁰ Lymphadenectomy is recommended in cases of invasive UTUC, but the extent of lymphadenectomy has not been established.¹ Furthermore, postoperative complication rates reported in retrospective studies after nephroureterectomy can be as high as 45% in some series, regardless of which surgical approach is used and can ultimately affect the ability of patients to receive adjuvant chemotherapy.¹¹

The primary aim of the present study is to compare the 30-day rate of postoperative complications in patients undergoing MINU versus ONU for UTUC in a prospectively collected national cohort of patients. In addition, we evaluated the likelihood of patients undergoing lymphadenectomy based on surgical approach, length of hospital stay, readmission rates, reintervention rate, and perioperative mortality among surgical approaches. Because of the low incidence of UTUC (only 5% of all urothelial carcinomas) and lack of prospective studies, the optimal surgical modality for treatment of UTUC has yet to be established.^1,12 We hypothesize that patients with UTUC undergoing laparoscopic surgery have more favorable perioperative outcomes.

Methods

Data source

The present study relied on the American College of Surgeons-National Surgical Quality Improvement Program (ACS-NSQIP) Participant User Files.¹³ This database contains risk-adjusted surgical patient data from member hospitals to facilitate the assessment of perioperative outcome measures after surgical procedures. Validated data from patients' medical charts allow quantification of 30-day risk-adjusted surgical outcomes, including postdischarge information. These data are collected and validated by trained surgical clinical reviewers. In 2012, the ACS-NSQIP included data from 374 participant institutions with more than 2.3 million cases having been contributed.

Study population

We extracted patients from 2006 to 2012 and identified them in the ACS-NSQIP database using Current Procedural Terminology (CPT) codes for nephroureterectomy. Patients were stratified according to MINU (50545, 50546, 50548) versus ONU (50220, 50225, 50230, 50234, 50236, 50650). Robot-assisted approaches could not be identified based on available CPT codes. Only patients with a diagnosis of UTUC were included (International Classification of Diseases, 9th edition, codes: 189.1, 189.2, 236.91, 753.20, 753.29). After extraction, 896 patients were available for the analysis.

Covariates

For each patient, age at surgery, sex, race, body mass index (BMI), smoking status, American Society of Anesthesiologists (ASA) score, and receipt of neoadjuvant chemotherapy (administered up to 30 days preoperatively) were recorded.

Outcomes

Our primary outcome of interest was 30-day postoperative complications. Complications were grouped according to organ system using previously reported methodology.¹⁴ Briefly, complications were categorized as the following: Cardiovascular (postoperative cardiac arrest and myocardial infarction), pulmonary (pneumonia, need for postoperative reintubation, and need for ventilatory support >48 hours), thromboembolic (deep venous thrombosis and pulmonary embolism), septic (sepsis and septic shock), renal (acute renal failure and progressive renal insufficiency), urinary tract infections, wound complications (superficial, deep, and organ space surgical site infections, and wound dehiscence). Overall complication rate was defined as the occurrence of any complication.

Furthermore, secondary outcomes examined were likelihood of undergoing a lymph node dissection (LND), need for intraoperative/postoperative blood transfusion, operative reintervention, prolonged operative time (pOT), prolonged length of stay (pLOS), rate of readmission, and perioperative mortality. Operative reintervention was defined as unplanned return to the operating room for a surgical procedure, for any reason, within 30 days of the principal procedure. Prolonged operative time and prolonged LOS were defined as an operative time and a hospital LOS greater than the 75th percentile (>282 min and >6 days, respectively). Perioperative mortality was defined as death within 30 days of surgery. Thirty-day readmission data in this study were available starting January 1, 2012.

Statistical analyses

Descriptive statistics of categoric variables focused on frequencies and proportions. Medians and interquartile ranges were reported for continuously coded variables. Multivariable regression models were used to analyze the association between outcomes and surgical approach. The reference group consisted of patients who underwent ONU. All models were adjusted for age, sex, race, BMI, smoking, ASA score, and neoadjuvant chemotherapy. We performed propensity-score weighting to account for potential selection biases inherent to a retrospective study. Propensity-score weighting did not significantly change our results (Supplementary Table 1; supplementary data are available online at www.liebertpub.com/end).

All statistical testing was two-sided with a level of significance set at P<0.05. Analyses were performed using SPSS, version 22 (IBM, Armonk, NY). An Institutional Review Board waiver was obtained before conducting this study, in accordance with institutional regulation when dealing with de-identified administrative data.

Results

Baseline patient characteristics

Overall, 896 patients underwent nephroureterectomy between 2006 and 2012 in the ACS-NSQIP database. Patient characteristics stratified by surgical approach are shown in Table 1. During the study period, 599 (66.9%) patients underwent MINU. Patients undergoing MINU were older with a mean age of 71 years compared with 69 years for those undergoing ONU (P=0.015). Overall, the majority of patients were white (73.4%) and male (64%). Furthermore, 31.1% were obese, 23.4% smokers, and 65.4% had an ASA score of 3 or greater. There was no significant difference in comorbidities between the groups. Patients who underwent MINU received neoadjuvant chemotherapy less often compared with the ONU group (2.3% vs 6.1%, P=0.033).

Table 1.

Descriptive Characteristics of Patients Undergoing Nephroureterectomy for Upper Tract Urothelial Carcinoma Stratified According to Surgical Approach in the National Surgical Quality Improvement Program (NSQIP) Database from 2006 to 2012

Variables	Overall	MINU	ONU	P value
Patients, n (%)	896 (100)	599 (66.9)	297 (33.1)	-
Mean age, years (IQR)	71 (62–79)	71 (64–79)	69 (61–77)	0.015^a
Sex, n (%)				0.466
Male	573 (64.0)	388 (64.8)	185 (62.3)
Female	323 (36.0)	211 (35.2)	112 (37.7)
Race, n (%)				0.506
White	658 (73.4)	446 (74.5)	212 (71.4)
Black	39 (4.4)	23 (3.8)	16 (5.4)
Asian	34 (3.8)	19 (3.2)	15 (5.1)
Hispanic	33 (3.7)	23 (3.8)	10 (3.4)
Unknown	132 (14.7)	88 (14.7)	44 (14.8)
BMI (kg/m²), n (%)				0.935
<18.5	14 (1.6)	9 (1.5)	5 (1.7)
18.5–25.0	260 (29.2)	171 (28.6)	89 (30.4)
25.1–30.0	339 (38.1)	231 (38.7)	108 (36.9)
>30	277 (31.1)	186 (31.2)	91 (31.1)
Smoking, n (%)				0.570
Smoker	210 (23.4)	137 (22.9)	73 (24.6)
Nonsmoker	686 (76.6)	462 (77.1)	224 (75.4)
ASA score, n (%)
1-no disturbance	10 (1.1)	7 (1.2)	3 (1.0)	0.715
2-mild disturbance	300 (33.5)	201 (33.6)	99 (33.3)
3-severe disturbance	552 (61.7)	371 (62.0)	181 (60.9)
≥4-life threat	33 (3.7)	19 (3.2)	14 (4.7)
Neoadjuvant chemotherapy, n (%)	18 (3.7)	7 (2.3)	11 (6.1)	0.033

Kruskal-Wallis test.

MINU=minimally invasive nephroureterectomy; ONU=open nephroureterectomy; IQR=interquartile range; BMI=body mass index; ASA=American Society of Anesthesiologists.

Perioperative outcomes stratified by surgical approach are summarized in Table 2. The overall rate of 30-day postoperative complications was 12.7% for both cohorts and did not differ between ONU and MINU. Furthermore, no significant differences between MINU and ONU were observed with respect to readmission rate, pOT, and perioperative mortality. Yet, patients undergoing MINU had significantly lower transfusion rates (9.2% vs 21.5%, P<0.001) and need for operative reintervention (1.8% vs 4.7%, P<0.001) compared with ONU. Furthermore, patients who underwent MINU had a significant decrease in pLOS (22.9% vs 45.5%, P<0.001). Interestingly, patients who underwent MINU were less likely to undergo a LND compared with ONU (3.8% vs 26.6%, P<0.001).

Table 2.

30-Day Perioperative Outcomes for Patients Undergoing Nephroureterectomy for Upper Tract Urothelial Carcinoma Stratified by Surgical Approach in the National Surgical Quality Improvement Program Database from 2006 to 2012

	Overall	MINU	ONU	P value
Patients, n (%)	896 (100)	599 (66.9)	297 (33.1)	-
Overall complications, n (%)	114 (12.7)	77 (12.9)	37 (12.5)	0.867
Complications by organ system, n (%)
Cardiovascular	12 (1.3)	7 (1.2)	5 (1.7)	0.528
Pulmonary	36 (4.0)	23 (3.8)	13 (4.4)	0.700
Thromboembolic	15 (1.7)	8 (1.3)	7 (2.4)	0.262
Sepsis/shock	22 (2.5)	13 (2.2)	9 (3.0)	0.434
Renal failure	25 (2.8)	15 (2.5)	10 (3.4)	0.460
UTI	31 (3.5)	23 (3.8)	8 (2.7)	0.377
Wound	27 (3.0)	15 (2.5)	12 (4.0)	0.205
Transfusion, n (%)	120 (13.4)	55 (9.2)	65 (21.5)	<0.001
Reintervention, n (%)	25 (2.8)	11 (1.8)	14 (4.7)	0.014
Readmission (2012), n (%)	23 (6.8)	15 (6.3)	8 (7.9)	0.588
pOT (>282 min),^a n (%)	226 (25.2)	160 (26.7)	66 (22.2)	0.145
pLOS (>6 days),^a n (%)	272 (30.4)	137 (22.9)	135 (45.5)	<0.001
Perioperative mortality, n (%)	16 (1.8)	10 (1.7)	6 (2.0)	0.709
LND, n (%)	102 (11.4)	23 (3.8)	79 (26.6)	<0.001

≥75th percentile.

UTI=urinary tract infection; pOT=prolonged operative time; pLOS=prolonged length of stay.

Results of the adjusted multivariate analyses are summarized in Table 3. Patients who underwent MINU had significantly decreased odds of thromboembolic complications (odds ratio [OR]=0.13; P=0.018), need for blood transfusions (OR=0.39; P=0.001), and operative reintervention rate (OR=0.24; P=0.024). Furthermore, patients undergoing MINU had a decreased risk of pLOS (OR=0.34; P<0.001). Once again, patients who underwent MINU were also less likely to undergo LND (OR=0.13; P<0.001).

Table 3.

Multivariable Logistic Regression Analysis for Risk of 30-day Perioperative Outcomes in Patients Undergoing Minimally Invasive Nephroureterectomy Versus Open Nephroureteretomy (Reference) in the National Surgical Quality Improvement Program Database from 2006 to 2012

	OR ^a	95% CI	P value
Overall complications	0.69	0.39–1.25	0.22
Complications by organ system:
Cardiovascular	0.81	0.17–3.81	0.79
Pulmonary	0.57	0.22–1.49	0.25
Thromboembolic	0.13	0.02–0.7	0.018
Sepsis/shock	0.46	0.15–1.46	0.19
Renal failure	0.64	0.2–1.93	0.43
UTI	1.36	0.42–4.45	0.61
Wound	0.44	0.12–1.57	0.21
Blood transfusion	0.39	0.2–0.69	0.001
Reintervention	0.24	0.07–0.83	0.024
pOT (>282 min)^b	1.13	0.73–1.75	0.58
pLOS (>6 days)^b	0.34	0.23–0.52	<0.001
Perioperative mortality	0.64	0.1–2.63	0.54
Readmission (2012)	1.21	0.06–24.27	0.90
LND, n (%)	0.31	0.06–0.25	<0.001

Model adjusted for surgical approach ([Ref. OP]; MINU), gender ([Ref. male]; female), race ([Ref. White]; Other), age (cont.), BMI ([Ref. <18.5]; 18.5-25.0, 25.1-30.0, >30.0), smoking ([Ref. non-smoker]), ASA score ([Ref. <3]; ≥3) and neoadjuvant chemotherapy ([Ref. no neoadjuvant chemotherapy]).

≥75th percentile.

OR=odds ratio; CI=confidence interval.

Discussion

In the present study, we compared the 30-day perioperative outcomes of patients undergoing MINU versus ONU in a prospectively collected cohort of patients in the ACS-NSQIP database. We found that a minimally invasive approach had an equivalent 30-day postoperative complication rate compared with those undergoing an open approach. In multivariable analysis, however, patients undergoing MINU had significantly decreased odds of postoperative thromboembolic events, need for blood transfusion, and need for operative reintervention within 30 days of surgery. Furthermore, patients who underwent MINU were less likely to experience a pLOS. Interestingly, patients undergoing MINU were less likely to receive a concomitant LND and to receive neoadjuvant chemotherapy.

Our study provides further support that MINU can be performed safely and offers important advantages over ONU that may have an impact on overall healthcare costs and patient quality of life.

Several studies have recently compared perioperative outcomes between laparoscopic nephroureterectomy (LNU) and ONU.^6,15 To date, it is well established that patients who undergo LNU have a decreased need for blood transfusion and decreased length of hospital stay compared with those undergoing ONU. Among the largest population-based series to date, Hanna and coworkers⁴ retrospectively evaluated 8155 patients who underwent ONU (90.8%) and LNU (9.2%) within the Nationwide Inpatient Sample. The study found that patients undergoing LNU were less likely to receive a blood transfusion (OR 0.39, P=0.001), to have any intraoperative complication (OR 0.4, P=0.002), and have a pLOS (OR 0.4, P<0.001).

Similar to our study, the rate of postoperative complications was similar between surgical approaches. They found a decreased risk of respiratory complications (OR 0.4, P=0.007) in those undergoing LNU, however. Although we did not find a difference in pulmonary complications in our study, we ascertained that patients undergoing MINU were 87% less likely to experience a thromboembolic event 30 days postoperatively. Our study is the first to demonstrate a difference in thromboembolic complications between these surgical approaches for UTUC.

Although this finding has not been shown in previous nephroureterectomy series, it was recently reported that patients who undergo LND during prostatectomy (open or robotic) have a significantly increased risk of postoperative thromboembolic events.¹⁶ Further investigation is needed to determine whether patients who undergo lymphadenectomy for UTUC are at higher risk of postoperative thromboembolic complications.

Overall, there was a low incidence of thromboembolic events (1.7%) in this patient cohort; however, patients receiving MINU were significantly less likely (OR 0.13; P=0.018) to have a thromboembolic complication compared with those undergoing ONU after adjusting for baseline patient characteristics. This phenomenon has been described previously in the general surgery literature where it has been postulated that patients who undergo minimally invasive surgery may have decreased pain and thus ambulate earlier compared with those who undergo open surgery.¹⁷

Alberts and associates¹⁸ reported the incidence and risk factors for thromboembolic events in 27,455 patients undergoing urologic oncologic procedures in ACS-NSQIP and found the overall incidence of thromboembolic events to be 1.4%. Among those undergoing surgery for upper tract cancers, a history of chronic obstructive pulmonary disease, low preoperative albumin level, and prolonged operative time were associated with thromboembolic events. In addition, patients undergoing nephroureterectomy were more likely to have postdischarge thromboembolic events.¹⁸

These findings, however, are limited because the use and duration of thromboembolic prophylaxis (pharmacologic or mechanical) was not an available variable in the ACS-NSQIP. Furthermore, thromboembolic events that occur after the 30-day postoperative period would not be recorded in this study. It is important to be aware of the potential increased risk of thromboembolic disease in patients undergoing ONU because this may prompt urologists to be more liberal about use of pharmacologic prophylaxis.

In accordance with previous studies, we found that patients undergoing MINU were 61% less likely to need a postoperative blood transfusion.^3,6 Previous studies have suggested that postoperative blood transfusions may impact oncologic outcomes in patients undergoing nephroureterectomy.¹⁹ Moreover, allogeneic blood transfusions have been previously demonstrated to increase the risk of postoperative bacterial infections.²⁰ Furthermore, studies evaluating perioperative outcomes in robotic versus laparoscopic nephroureterectomy have found that a robotic approach was associated with similar transfusion rates.⁷

The risk of pLOS was also significantly decreased in patients undergoing MINU. Decreasing LOS has important efficiency and cost considerations. Yu and colleagues⁸ demonstrated lower costs for laparoscopic nephrectomy ($11,153) and higher costs for robot-assisted nephrectomy ($13,894) compared with an open approach ($12,548).⁸ Although MINU may be a longer procedure as shown in our study, and potentially more costly because of costs for disposables in laparoscopic and especially robotic surgery, shortening length of stay may help bridge the cost difference between robot-assisted and open kidney surgery. Further studies are needed to assess the value of reduced LOS, as well as accelerated recovery and, consequently, reduced work absenteeism.

Intriguingly, we found that patients undergoing MINU were 69% less likely to undergo LND compared with ONU. This finding may reflect the fact that patients who undergo ONU have a more advanced clinical stage and are therefore more likely to undergo LND. Patients in the ONU group also received neoadjuvant chemotherapy at a higher rate compared with those undergoing MINU supporting the possibility that patients in that group may have had more advanced stages of disease.

In this context, the indication and optimal template for LND in UTUC has yet to be established. Up to 30% of patients with ≥cT₂ UTUC are found to have regional metastasis at the time of surgery and may show an improvement in cancer-specific and recurrence-free survival with LND.^21
–23 In addition, LND may help in risk-stratifying patients postoperatively to determine those who may benefit most from adjuvant chemotherapy. Although several predictive tools to assist in clinical decision-making for patients with UTUC have been reported, further studies are needed to address the indication for LND, optimal template, and preferred surgical approach.²⁴ Regardless, both of these findings more likely reflect surgeon preferences rather than technical considerations.

Despite its strengths, this study has several important limitations. First, clinical stage or grade for patients with cancer is not recorded in the ACS-NSQIP database. This has particular implications in our study, because oncologic clinical staging is likely to influence surgeon preference for a particular surgical approach. Equivalent oncologic outcomes, however, were reported in the only prospective randomized trial of open versus laparoscopic nephroureterectomy for patients with cT₁-T₂ disease.²

Second, in this cohort of patients, we were unable to account for the management of the distal ureter/bladder cuff at the time of the surgical procedure. A recent multi-institutional retrospective study evaluated the impact of distal ureter management on oncologic outcomes after nephroureterectomy for UTUC and reported that a laparoscopic approach was independently associated with higher rate of intravesical recurrence.²⁵ Furthermore, we were unable to account for patient performance status, hospital volume and/or academic status.

Finally, in this cohort, we are not able to comment on contralateral ureteral obstruction or urinary leak. Because these complications are rare, they are not likely to affect our current analyses. In addition, because NSQIP only provides 30-day follow-up data, we are not able to comment on long-term complications. In addition, we did not comment on trends of utilization of MINU versus ONU because NSQIP may not be representative of national trends. Recently, Hanna and colleagues⁴ reported that the use of MINU doubled from 7% in 1998 to 2001 to 15% in 2006 to 2009 in the National Inpatient Sample that approximates 20% of public hospitals and academic centers within the United States.⁴

Nonetheless, our study relies on rigorous methodologic data collection, rather than administrative claims. In comparison with administrative claims, the NSQIP database offers more perioperative patient-specific variables as well as postoperative outcomes within 30 days.²⁶ Taken together, the NSQIP database has been a better tool for predicting complications and death after surgery.²⁷

Conclusion

Patients undergoing MINU have similar overall complication rates compared with patients undergoing ONU. MINU, however, was associated with decreased odds of blood transfusions, thromboembolic events, operative reintervention, and pLOS compared with ONU. Such findings may impact patient convalescence, which is essential for reducing healthcare costs and getting patients to adjuvant chemotherapy in a timely manner.

Footnotes

Acknowledgments

The American College of Surgeons National Surgical Quality Improvement Program and the hospitals participating in the ACS NSQIP are the source of the data used herein; they have not verified and are not responsible for the statistical validity of the data analysis or the conclusions derived by the authors.

Quoc-Dien Trinh is supported by the Professor Walter Morris-Hale Distinguished Chair in Urologic Oncology at Brigham and Women's Hospital and by an unrestricted educational grant from the Vattikuti Urology Institute. Julian Hanske is supported by a grant from the Heinrich Hertz-Stiftung.

Author Disclosure Statement

No competing financial interests exist.

Abbreviations Used

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Supplementary Material

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