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Keywords:

  • upper urinary tract urothelial cancer;
  • Canadian Upper Tract Collaboration;
  • radical nephroureterectomy;
  • survival

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. Conflict of Interest
  9. References

What's known on the subject? and What does the study add?

  • Open radical nephroureterectomy (ORNU) with excision of the ipsilateral bladder cuff is a standard treatment for upper tract urothelial carcinoma (UTUC). However, over the past decade laparoscopic RNU (LRNU) has emerged as a minimally invasive surgical alternative. Data comparing the oncological efficacy of ORNU and LRNU have reported mixed results and the equivalence of these surgical techniques have not yet been established.
  • We found that surgical approach was not independently associated with overall or disease-specific survival; however, there was a trend toward an independent association between LRNU and poorer recurrence-free survival (RFS). To our knowledge, this is the first large, multi-institutional analysis to show a trend toward inferior RFS in patients with UTUC treated with LRNU.

Objective

  • To examine the association between surgical approach for radical nephroureterectomy (RNU) and clinical outcomes in a large, multi-institutional cohort, as there are limited data comparing the oncological efficacy of open RNU (ORNU) and laparoscopic RNU (LRNU) for upper urinary tract urothelial carcinoma (UTUC).

Patients and Methods

  • Institutional RNU databases containing detailed information on patients with UTUC treated between 1994 and 2009 were obtained from 10 academic centres in Canada.
  • Data were collected on 1029 patients and combined into a relational database formatted with patient characteristics, pathological characteristics, and survival status.
  • Surgical approach was classified as ORNU (n = 403) or LRNU (n = 446).
  • The clinical outcomes were overall survival (OS), disease-specific survival (DSS), and recurrence-free survival (RFS). The Kaplan–Meier method and Cox proportional regression analysis were used to analyse survival data.

Results

  • Data were evaluable for 849 of 1029 (82.5%) patients.
  • The median (interquartile range) follow-up duration was 2.2 (0.6–5.0) years.
  • The predicted 5-year OS (67% vs 68%, log-rank P = 0.19) and DSS (73% vs 76%, log-rank P = 0.32) rates did not differ between the ORNU and LRNU groups; however, there was a trend toward an improved predicted 5-year RFS rate in the ORNU group (43% vs 33%, log-rank P = 0.06).
  • Multivariable Cox proportional regression analysis showed that surgical approach was not significantly associated with OS (hazard ratio [HR] 0.89, 95% confidence interval [CI] 0.63–1.27, P = 0.52) or DSS (HR 0.90, 95% CI 0.60–1.37, P = 0.64); however, there was a trend toward an independent association between surgical approach and RFS (HR 1.24, 95% CI 0.98–1.57, P = 0.08).

Conclusion

  • Surgical approach was not independently associated with OS or DSS but there was a trend toward an independent association between LRNU and poorer RFS. Further prospective evaluation is needed.

Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. Conflict of Interest
  9. References

Upper urinary tract urothelial carcinoma (UTUC) is a rare malignancy. In 2012, it is estimated to comprise 10% of all renal tumours and 5% of UCs overall [1]. Open radical nephroureterectomy (ORNU) with excision of the ipsilateral bladder cuff is the standard treatment for UTUC [2, 3]. However, over the past decade laparoscopic RNU (LRNU) has emerged as a minimally invasive surgical alternative. To date, several studies have compared the oncological efficacy of ORNU and LRNU in patients with UTUC [4-15]. Some studies have shown comparable oncological results between ORNU and LRNU [4-12] whereas other studies have shown a higher risk of recurrence with LRNU [13-15]. Unfortunately, these data are limited by relatively few laparoscopic cases, heterogeneous study populations, and varied surgical techniques [4-15]. As such, the oncological efficacy of LRNU and its equivalence to ORNU has not been established. Knowledge of the efficacy of LRNU is necessary for adequate patient counselling, informed decision making, development of clinical practice guidelines, and prospective clinical trial design. Based on this rationale, we assessed the association between surgical approach (ORNU vs LRNU) and clinical outcomes in a large, multi-institutional cohort of patients with UTUC treated at 10 academic centres in Canada. We hypothesised that there was no difference in clinical outcomes between ORNU and LRNU.

Patients and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. Conflict of Interest
  9. References

Canadian Upper Tract Collaboration

This was an Institutional Review Board-approved study with all participating sites acquiring necessary institutional data use agreements before initiation of the study. In all, 10 Canadian academic centres (University of Alberta [n = 140], McGill University [n = 120], Dalhousie University [n = 172], University of Western Ontario [n = 100], McMaster University [n = 108], University of British Columbia [n = 99], University of Montreal [n = 61], University of Winnipeg [n = 50], University of Ottawa [n = 44], and Laval University [n = 135]) provided data from their institutional databases for analysis. A computerised database was generated for data transfer. At data transfer, initial reports were generated for each variable to identify data inconsistencies and other data integrity problems. Regular communication with participating sites permitted resolution of all identified anomalies before analysis. Before the final analysis, the data set was frozen from any additional modifications and the final data set was produced for the present analysis.

Study Cohort

We identified 1029 patients who underwent RNU with excision of the ipsilateral bladder cuff ± regional lymph node dissection for UTUC. Surgery was performed at each site according to surgeon preference. Excision of the distal ureter and ipsilateral bladder cuff was performed using one of three techniques: (i) extravesical, (ii) extravesical + open intravesical, or (iii) extravesical + endoscopic intravesical. Regional lymph node dissection was generally performed if lymph nodes were abnormal on preoperative CT or grossly abnormal on intraoperative examination. In all, 180 of 1029 (17.5%) patients were excluded due to incomplete data on surgical approach. The final study cohort included 849 patients with UTUC treated with ORNU (n = 403) or LRNU (n = 446) between 1994 and 2009.

Study Design

This investigation was a retrospective cohort study of database patients. The primary analysis examined the association between surgical approach and clinical outcomes. Collected variables included age, race, gender, presence of hydronephrosis, prior history of bladder cancer, prior history of upper tract cancer, clinical stage and nodal status, concomitant carcinoma in situ, histology, Eastern Cooperative Oncology Group (ECOG) performance status, smoking status, pelvic lymph node dissection, pathological stage and nodal status, grade, surgical margins, neoadjuvant chemotherapy/radiation, adjuvant chemotherapy/radiation, and salvage chemotherapy/radiation.

Pathological Evaluation

All surgical specimens were processed according to standard pathological procedures and all slides were reviewed by anatomical pathologists at each participating institution. Centralised pathological review and reclassification of specimens was not performed. UTUC was defined as cancer located in the renal pelvis, calyces, or ureter. Tumours were staged according to the American Joint Committee on Cancer TNM classification system [16] and graded according to the WHO/International Society of Urologic Pathology (WHO/ISUP) consensus classification [17]. In cases of concomitant renal pelvis and ureteric tumours, the dominating tumour was used to determine the primary location.

Follow-Up

Patients were followed in accordance with individual site surveillance protocols. In general, patients were observed in follow-up every 3–4 months in the first year, every 6 months from 2–5 years, and annually thereafter. At each visit, history, physical examination, routine blood work and serum chemistries, urinary cytology, chest radiography, cystoscopy, and radiological evaluation of the contralateral upper urinary tract were performed. Bone scans and CT of the chest, abdomen, and pelvis were performed when clinically indicated.

Outcome Measures

The outcome measures were overall survival (OS), disease-specific survival (DSS), and recurrence-free survival (RFS). OS was defined as the interval between the date of surgery and death from any cause. DSS was defined as the interval between the date of surgery and death from UC. RFS was defined as the interval between the date of surgery and first documented clinical recurrence or death. Patients alive at the end of the study period were censored at that point and contributed the time interval from their date of surgery to the end of the study in the survival analysis.

Sample Size Calculation and Statistical Analysis

A sample size calculation was not performed. The number of cases in the dataset during the study period determined the sample size.

The Fisher's exact test and chi-squared test were used to evaluate the association between categorical variables. The Kaplan–Meier method was used to estimate survival functions and differences were assessed with the log-rank statistic. Univariable and multivariable Cox proportional hazards regression analyses were performed to determine the association between surgical approach and clinical outcomes. A two-sided P ≤ 0.05 was considered to indicate statistical significance.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. Conflict of Interest
  9. References

Data on 1029 patients was submitted from 10 academic centres. In all, 849 of 1029 (82.5%) patients had complete data and were included in the present analyses. The median (interquartile range) follow-up duration was 2.2 (0.6–5.0 years).

Baseline Characteristics

Table 1 presents the baseline characteristics of the study cohort. Baseline characteristics were similar between the groups except the LRNU patients were older (70.5 vs 72.4 years, P = 0.02), more likely to be female (40% vs 32%, P = 0.02), less likely to undergo regional lymph node dissection (25% vs 34%, P < 0.01), less likely to have regional lymph node metastases (4% vs 10%, P < 0.01), had a lower total number of positive lymph nodes removed (0.9 vs 0.3, P < 0.01), and had different techniques used to excise the distal ureter (P < 0.01).

Table 1. Baseline characteristics.
VariableORNULRNUP
Number of patients403446 
Demographic:   
Median age, years70.572.40.02
Female gender, n (%)129 (32)178 (40)0.02
Clinical, n (%):   
Regional lymph node dissection135 (34)110 (25)<0.01
Adjuvant chemotherapy37 (9)57 (13)0.10
Management of distal ureter:   
Extravesical166 (42)150 (34) 
Extravesical + open intravesical199 (51)205 (46) 
Extravesical + endoscopic intravesical14 (4)83 (19) 
Other12 (3)3 (1)<0.01
Pathological:   
T Stage, n (%)   
≤T1186 (51)200 (52)0.95
T266 (18)66 (17) 
T389 (25)99 (26) 
T422 (6)21 (5) 
N Stage, n (%):   
NX275 (68)342 (77)<0.01
N086 (21)86 (19) 
N1–342 (10)18 (4) 
Mean (sd) total number of lymph nodes removed4.3 (5)4.2 (4)0.90
Mean (sd) total number positive lymph nodes removed0.9 (1.8)0.3 (0.9)<0.01
Grade, n (%):   
High274 (69)277 (64)0.12
Low123 (31)156 (36) 
Positive surgical margins, n (%)40 (11)42 (10)0.65
Concomitant carcinoma in situ, n (%)94 (10)107 (25)0.83
UTUC, n (%)378 (96)421 (96)0.76

Clinical Outcomes Stratified by Surgical Approach

Figures 1, 2, and 3 show the Kaplan–Meier estimates for OS, DSS, and RFS stratified by surgical approach in the overall cohort. The predicted 5-year OS (67% vs 68%, log-rank P = 0.19) and DSS (73% vs 76%, log-rank P = 0.32) rates did not differ between the ORNU and LRNU groups; however, there was a trend toward an improved predicted 5-year RFS rate in the ORNU group (43% versus 33%, log-rank P = 0.06).

figure

Figure 1. Kaplan–Meier estimate of OS stratified by surgical approach.

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figure

Figure 2. Kaplan–Meier estimate of DSS stratified by surgical approach.

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figure

Figure 3. Kaplan–Meier estimate of RFS stratified by surgical approach.

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Kaplan–Meier estimates for OS, DSS, and RFS stratified by surgical approach in three pathological risk groups (≤pT2N0, pT3–4N0, pTanyN1–3) were generated. There were no statistically significant OS or DSS differences between the ORNU and LRNU groups in any pathological risk group (data not shown). However, the predicted 5-year RFS rate differed between the ORNU and LRNU groups in patients with ≤pT2N0 (52% vs 37%, log-rank P = 0.01) and pTanyN1–3 (45% vs 33%, log-rank P = 0.03) disease. The predicted 5-year RFS rate did not differ between the ORNU and LRNU groups in patients with pT3–4N0 disease (31% vs 24%, log-rank P = 0.80).

Association between Surgical Approach and Clinical Outcomes

Table 2 presents the results of the univariable analysis examining predictors of clinical outcomes in the overall cohort. Surgical approach was not associated with OS (hazard ratio [HR] 0.83, 95% CI 0.62–1.10, P = 0.19) or DSS (HR 0.84, 95% CI 0.61–1.18, P = 0.32); however, there was a trend toward an association between surgical approach and RFS favouring ORNU (HR 1.20, 95% CI 0.99–1.46, P = 0.06).

Table 2. Univariable analysis examining predictors of clinical outcomes.
VariableOSDSSRFS
HR (95% CI)PHR (95% CI)PHR (95% CI)P
Surgical approach:
Open1.00 1.00 1.00 
Laparoscopic0.83 (0.62–1.10)0.190.84 (0.61–1.18)0.321.20 (0.99–1.46)0.06
Age1.03 (1.02–1.04)<0.011.02 (1.00–1.03)0.031.02 (1.01–1.03)<0.01
Gender:
Male1.00 1.00 1.00 
Female0.87 (0.69–1.10)0.250.86 (0.65–1.14)0.291.06 (0.89–1.27)0.50
Regional lymph node dissection:
No1.00 1.00 1.00 
Yes1.56 (1.23–1.98)<0.011.83 (1.38–2.42)<0.011.41 (1.17–1.71)<0.01
Adjuvant chemotherapy:
No1.00 1.00 1.00 
Yes1.66 (1.20–2.29)<0.012.19 (1.55–3.11)<0.012.50 (1.97–3.18)<0.01
pT stage:
T11.00 1.00 1.00 
T21.47 (1.03–2.10)0.031.76 (1.13–2.74)0.011.38 (1.07–1.79)0.01
T32.85 (2.16–3.75)<0.013.56 (2.53–5.02)<0.011.92 (1.55–2.37)<0.01
T45.76 (3.71–8.93)<0.017.47 (4.50–12.4)<0.013.56 (2.45–5.17)<0.01
pN stage:
N01.00 1.00 1.00 
NX1.48 (1.14–1.92)<0.011.46 (1.06–2.02)0.021.11 (0.91–1.37)0.31
N1–33.70 (2.64–5.20)<0.014.86 (3.33–7.09)<0.012.70 (2.04–3.58)<0.01
Grade:
Low1.00 1.00 1.00 
High2.31 (1.73–3.71)<0.012.60 (1.82–3.72)<0.011.46 (1.20–1.77)<0.01
Surgical margin status:
Negative1.00 1.00 1.00 
Positive2.34 (1.72–3.18)<0.012.56 (1.79–3.66)<0.012.26 (1.76–2.90)<0.01
Concomitant carcinoma in situ1.42 (1.07–1.88)0.021.54 (1.11–2.14)0.011.52 (1.24–1.86)<0.01
Histological type:
UC1.00 1.00 1.00 
Non-UC0.90 (0.50–1.60)0.710.79 (0.37–1.68)0.540.96 (0.62–1.49)0.85

Univariable Cox regression models examining the association between surgical approach and RFS in three pathological risk groups (≤pT2N0, pT3–4N0, pTanyN1–3) were generated. LRNU was associated with poorer RFS in patients with ≤pT2N0 (HR 1.45, 95% CI 1.08–1.94, P = 0.01) and pTanyN1–3 (HR 1.30, 95% CI 1.03–1.65, P = 0.03) disease; however, there was no association between surgical approach and RFS in patients with pT3–4N0 disease (HR 0.94, 95% CI 0.60–1.48, P = 0.80).

Table 3 presents the results of the multivariable analysis examining predictors of clinical outcomes in the overall cohort. Surgical approach was not independently associated with OS (HR 0.89, 95% CI 0.63–1.27, P = 0.52) or DSS (HR 0.90, 95% CI 0.60–1.37, P = 0.64); however, there was a trend toward an independent association between surgical approach and RFS (HR 1.24, 95% CI 0.98–1.57, P = 0.08).

Table 3. Multivariable analysis examining predictors of clinical outcomes.
VariableOSDSSRFS
HR (95% CI)PHR (95% CI)PHR (95% CI)P
Surgical approach:
Open1.00 1.00 1.00 
Laparoscopic0.89 (0.63–1.27)0.520.90 (0.60–1.37)0.641.24 (0.98–1.57)0.08
Age1.03 (1.01–1.05)<.011.02 (1.00–1.05)0.041.02 (1.01–1.03)<0.01
Gender:
Male1.00 1.00 1.00 
Female0.94 (0.67–1.33)0.720.97 (0.64–1.46)0.871.24 (0.97–1.58)0.08
Adjuvant chemotherapy:
No1.00 1.00 1.00 
Yes0.92 (0.52–1.63)0.781.09 (0.59–2.00)0.791.36 (0.92–2.01)0.13
pT stage:
T11.00 1.00 1.00 
T21.50 (0.93–2.43)0.102.09 (1.16–3.77)0.011.40 (1.01–1.95)0.40
T32.51 (1.68–3.75)<0.013.15 (1.90–5.20)<0.011.46 (1.09–1.97)0.01
T42.98 (1.51–5.91)<0.013.34 (1.51–7.58)<0.011.67 (0.96–2.92)0.07
pN stage:
NX1.00 1.00 1.00 
N00.78 (0.53–1.16)0.220.82 (0.50–1.34)0.420.83 (0.62–1.10)0.19
N1–31.76 (1.01–3.09)0.052.16 (1.14–4.09)0.021.74 (1.12–2.71)0.01
Grade:
Low1.00 1.00 1.00 
High1.92 (1.27–2.91)<0.012.22 (1.30–3.78)<0.011.12 (0.85–1.47)0.43
Surgical margin status:
Negative1.00 1.00 1.00 
Positive1.37 (0.87–2.15)0.181.62 (0.97–2.71)0.071.50 (1.06–2.11)0.02
Concomitant carcinoma in situ0.98 (0.68–1.43)0.930.96 (0.62–1.50)0.871.19 (0.90–1.56)0.22

Multivariable Cox regression models examining the association between surgical approach and RFS in three pathological risk groups (≤pT2N0, pT3–4N0, pTanyN1–3) were generated. LRNU was independently associated with poorer RFS in patients with ≤pT2N0 (HR 1.68, 95% CI 1.23–2.31, P < 0.01) and pTanyN1–3 (HR 1.29, 95% CI 1.00–1.66, P = 0.05) disease; however, there was no independent association between surgical approach and RFS in patients with pT3–4N0 disease (HR 0.91, 95% CI 0.56–1.48, P = 0.71).

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. Conflict of Interest
  9. References

In the present study from the Canadian Upper Tract Collaboration, we evaluated the associations between surgical approach and clinical outcomes in patients with UTUC. We found that surgical approach was not independently associated with OS or DSS; however, there was a trend toward an independent association between LRNU and poorer RFS.

One finding of the present study was that surgical approach was not independently associated with OS or DSS. This finding supports our hypothesis and extends previous data. In an analysis of 324 consecutive patients with UTUC who underwent RNU at the Memorial Sloan-Kettering Cancer Centre, Favaretto et al. [4] reported that surgical approach was not associated with DSS. Similarly, two large multi-institutional studies of patients who underwent RNU for UTUC failed to show an independent association between surgical approach and DSS [9, 10]. Taken together, these data suggest equivalent cancer-specific control between ORNU and LRNU.

However, in contrast to our hypothesis we found that there was a trend toward an independent association between surgical approach and RFS. Specifically, we found that LRNU may be associated with poorer RFS compared with ORNU. In addition, subset analysis showed that the survival difference may be evident in patients with both organ-confined and pathologically advanced disease. To our knowledge, this is the first large, multi-institutional analysis to show a trend toward inferior RFS in patients with UTUC treated with LRNU. This finding is consistent with results from a small randomised controlled trial comparing ORNU and LRNU that showed inferior DSS and metastasis-free survival in patients with pathologically-advanced UTUC treated with LRNU [11]. However, this finding is contrary to data gleaned from three recent multi-institutional studies that showed no independent association between surgical approach and RFS [9, 10, 12]. Explanations for this discrepant finding are unclear but may include differences in baseline clinical and pathological characteristics, use and extent of regional lymph node dissection, and/or surgical expertise and experience. Nonetheless, the present finding mandates consideration and challenges the current European Association of Urology UTUC Guideline which advocates the oncological equivalence of ORNU and LRNU in patients with UTUC (grade of recommendation B) [3].

The present results have implications for future research. There is a clear need for an adequately powered, randomised controlled trial comparing surgical approaches in patients with UTUC. However, given the low incidence of the disease, it is unlikely that such a trial will ever be completed. Support for this assertion can be found in the prostate cancer literature where, despite more than a decade of debate, no randomised trial has yet been performed to compare the oncological and functional outcomes of minimally invasive and open radical prostatectomy [18]. Nonetheless, a multi-institutional randomised trial should be strongly encouraged.

The strengths and limitations of our data merit comment. Strengths include the large sample size from multiple institutions and a large number of LRNU cases (n = 446). Limitations include the retrospective study design, possible selection bias, lack of control for patient comorbidity status, differences in surgical expertise, lack of standardised follow-up, and short follow-up duration.

In summary, the present study represents the fourth, large multi-institutional analysis examining the oncological efficacy of ORNU and LRNU in patients with UTUC. Surgical approach was not independently associated with OS or DSS; however, there was a trend toward an independent association between LRNU and poorer RFS. Further prospective evaluation of surgical approach in the setting of UTUC is warranted.

Acknowledgement

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. Conflict of Interest
  9. References

The authors acknowledge Dr Hassan Behlouli for assistance with statistical analysis.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. Conflict of Interest
  9. References
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Abbreviations
DSS

disease-specific survival

HR

hazard ratio

OS

overall survival

RFS

recurrence-free survival

(UT)UC

(upper urinary tract) urothelial carcinoma

(L)(O)RNU

(laparoscopic) (open) radical nephroureterectomy