Laparoscopic versus open nephroureterectomy to treat localized and/or locally advanced upper tract urothelial carcinoma: oncological outcomes from a multicenter study
Liu et al. BMC Surgery
Laparoscopic versus open nephroureterectomy to treat localized and/ or locally advanced upper tract urothelial carcinoma: oncological outcomes from a multicenter study
Jian-Ye Liu 0 1
Ying-Bo Dai 0 1
Zhi Long 0 1
Bin Liu 0 1
Jin Tang 0 1
Jing Tan 0 1
Kun Yao 0 1
Le-Ye He 0 1
0 Institute of Prostate Disease of Central South University , No.138, Tongzipo Road, Changsha 410013, Hunan , China
1 Department of Urology, The Third Xiangya Hospital of Central South University , No.138, Tongzipo Road, Changsha 410013, Hunan , China
Background: Many studies have reported the oncological outcomes between open radical nephroureterectomy (ONU) and laparoscopic radical nephroureterectomy (LNU) of upper tract urothelial carcinoma (UTUC). However, few data have focused on the oncological outcomes of LNU in the subgroup of localized and/or locally advanced UTUC (T1-4/N0-X). The purpose of this study was to compare the oncological outcomes of LNU vs. ONU for the treatment in patients with T1-4/N0-X UTUC. Methods: We collected and analyzed the data and clinical outcomes retrospectively for 265 patients who underwent radical nephroureterectomy for T1-4/N0-X UTUC between April 2000 and April 2013 at two Chinese tertiary hospitals. Survival was estimated using the Kaplan-Meier method. Cox's proportional hazards model was used for univariate and multivariate analysis. Results: The mean patient age was 62.0 years and the median follow-up was 60.0 months. Of the 265 patients, 213 (80.4%) underwent conventional ONU, and 52 (19.6%) patients underwent LNU. The groups differed significantly in their presence of previous hydronephrosis, presence of previous bladder urothelial carcinoma, and management of distal ureter (P < 0.05). The predicted 5-year intravesical recurrence- free survival (RFS) (79% vs. 88%, P = 0.204), overall RFS (47% vs. 59%, P = 0.076), cancer-specific survival (CSS) (63% vs. 70%, P = 0.186), and overall survival (OS) (61% vs. 55%, P = 0.908) rates did not differ between the ONU and LNU groups. Multivariable Cox proportional regression analysis showed that surgical approach was not significantly associated with intravesical RFS (odds ratio [OR] 1.23, 95% confidence interval [CI] 0.46-3.65, P = 0.622), Overall RFS (OR 0.99, 95% CI 0.54-1.83, P = 0.974), CSS (OR 1.38, 95% CI 0.616-3.13, P = 0.444), or OS (OR 1.61, 95% CI 0.81-3.17, P = 0.17). (Continued on next page) © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
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Conclusions: The results of this retrospective study showed no statistically significant differences in intravesical RFS,
overall RFS, CSS, or OS between the laparoscopy and the open groups. Thus, LNU can be an alternative to the open
procedure for T1–4/N0-X UTUC. Further studies, including a multi-institutional, prospective study are required to
confirm these findings.
Upper urinary tract urothelial carcinoma (UTUC) is a
relatively rare malignancy. It is estimated to comprise 10% of
all renal tumors and 5% of urothelial carcinomas overall
. Open radical nephroureterectomy (ONU), with
excision of the ipsilateral bladder cuff, is the standard treatment
for UTUC [2, 3]. However, laparoscopic radical
nephroureterectomy (LNU), first performed by Clayman et al. in
1991, has emerged as an accepted minimally invasive
treatment alternative to ONU . Subsequently, there have been
numerous retrospective reports comparing the oncological
outcomes between ONU and LNU [5–18] and one
prospective series . To date, none of the studies have
shown a significant difference between the techniques in
terms of overall survival (OS), recurrence-free survival
(RFS), and cancer-specific survival (CSS). Only one study
showed that there was a trend toward an independent
association between surgical approach and RFS , and three
studies showed a higher risk of intravesical RFS with LNU
[7, 20, 21]. However, these studies focused on the
oncological outcomes among the entire cohort of UTUC
patients. Especially, they included a great many pTa stage
and organ-confined UTUC. As experience with LNU
grows, case selection has expanded to include more
complex cases, resulting in carefully selected localized and/or
locally advanced UTUC and larger tumors being operated
on laparoscopically. However, until recently, only one study
has focused on the oncological outcomes of LNU in the
subgroup of localized and/or locally advanced UTUC .
Hence, the present study aimed to compare intravesical
RFS, overall RFS, CSS, and OS between ONU and LNU for
localized and/or locally advanced UTUC (T1–4/N0-X),
performed in two Chinese tertiary teaching hospitals.
After institutional review board approval was obtained, a
total of 265 consecutive patients, who were identified as
having localized and/or locally advanced UTUC (T1–4/
N0-X), and subsequently underwent ONU or LNU
between April 2000 and April 2013 in The Third Xiangya
Hospital of Central South University and the Sun
Yatsen University Cancer Center, were investigated in this
study. Exclusion criteria were the presence of any known
metastatic disease at the time of surgery, and radical
cystectomy with concomitant radical
nephroureterectomy (RNU). All patients had undergone computed
tomography, and/or intravenous urography, and/or
cystoscopy, and/or urine cytology. Diagnostic ureteroscopy
with biopsies has been used to stage tumors accurately
in some patients. In addition, none of the patients had
received preoperative chemotherapy.
Surgery was performed by surgeons according to the
standard criteria for RNU. The ONU was performed as
either a double-access incision: a loin incision and an
iliac incision; or a midline incision was performed from
the subxiphoid down to the pelvis. The kidney, Gerota
fascia, perinephric fat, the entire length of ureter, and
the bladder cuff were excised en bloc. Regional
lymphadenectomy was generally performed if lymph nodes were
abnormal on preoperative computed tomography or if
they were palpable intra-operatively. Extended
lymphadenectomy was not performed routinely. The LNU was
performed using the retroperitoneal or transperitoneal
approach. The range of resection was technically as the
same as in the ONU. The patients were fully informed
with regard to the surgical approach (laparoscopic vs.
open surgery) and its possible complications, and the
choice of choice of surgical procedure was
nonrandomized; it depended on patient and surgeon preference
and experience. In the laparoscopic group, only one
patient converted to open surgery. Distal ureter
management approaches were categorized as follows: (1)
extravesical ureter; (2) open intravesical; and (3) endoscopic.
Pathological and clinical evaluation
All surgical specimens were processed according to
standard pathological procedures and anatomical
pathologists at two institutions reviewed all slides. Centralized
pathological review and reclassification of specimens
was not performed. Tumors were staged according to
the 2002 American Joint Committee on Cancer TNM
classification system, and graded according to the 2004
World Health Organization/International Society of
Urologic Pathology (WHO/ISUP) consensus
classification. The tumor site was defined as renal pelvis, ureter,
or both renal pelvis and ureter. Tumor multifocality was
defined as the synchronous presence of two or more
pathologically confirmed tumors in any upper urinary
tract location (renal pelvis or ureter). Lymphovascular
invasion (LVI) was defined as the unequivocal presence
of tumor cells within an endothelium-lined space, with
no underlying muscular walls.
Patients were generally followed-up every 3 months for
2 years after RNU, every 6 months for the next 3 years,
and annually thereafter. Patients’ histories were taken,
and they underwent a physical examination, routine
blood evaluation, urinary cytology, chest radiography,
cystoscopic evaluation of the bladder, and radiographic
evaluation of the contralateral upper urinary tract at
each visit. Elective bone scans, computerized
tomography, or magnetic resonance imaging were performed
when indicated clinically.
Statistical analyses were performed using the statistical
software SPSS version 16.0 (SPSS, Inc., Chicago, IL). We
compared the clinical and pathological characteristics of
the two surgical technique groups (ONU vs. LNU) using
Student’s t-test for continuous variables and the
chisquared test for categorical variables. The primary
endpoints were intravesical RFS, overall RFS, CSS, and OS.
Intravesical recurrences included recurrences within the
bladder only. Overall recurrent disease included
recurrences within the bladder, as well as contralateral
recurrences, tumor relapse in the operative field, regional
lymph nodes, port site metastasis, and/or distant
metastasis. CSS was defined as the time interval between the
date of RNU and the end point, including death or
censoring. We defined “OS time” as the period between
the date of the first operation for the original disease
and the date of patient death (from any cause). Survival
probabilities were estimated using the Kaplan-Meier
method, and the log-rank test was applied to compare
survival curves. Univariate and multivariate Cox
proportional hazards regression analyses were performed to
determine the association between surgical approach
and clinical outcomes. All reported P-values were
twosided, and statistical significance was set at P ≤ 0.05.
Characteristics of patients
The study cohort comprised 265 assessable patients. The
ONU was performed in 213 (80.4%) vs. LNU in 52
(19.6%) patients. The clinical and pathological details for
each of the groups are presented in Table 1. The open
surgery preferred the presence of previous
hydronephrosis, absence of previous bladder urothelial carcinoma,
and underwent extravesical management of the distal
ureter (P < 0.05 for all) (Table 1).
At last follow-up, there were 46 (17.4%) bladder
recurrences, including 40 (18.8%) in the ONU group and six
(11.5%) in the LNU group. The 5-year intravesical RFS
estimates for the ONU and LNU groups were 79% and 88%,
respectively (P = 0.204) (Fig. 1a). The total number of
recurrence in the ONU and LNU groups were 109 (51.1%)
and 20 (38.5%), respectively. Overall RFS for the ONU
and LNU groups at 5 years were 47% and 59%,
respectively (P = 0.076) (Fig. 1b). In all, 84 patients (31.7%)
patients suffered disease progression and metastasis
during the study period, including 71 (33.3%) in the ONU
group and 13 (25.0%) in the LNU group. Estimated 5-year
CSS estimates for ONU and LNU groups were 63% and
70%, respectively, which was non-significant (P = 0.186)
(Fig. 2a). In the open group, 84 (39.4%) patients died
(from any cause). The 5-year OS rate was 61%. Death
occurred (from any cause) in 23 patients (44.2%) in the
laparoscopy group. The 5-year OS rate was 55%. No
statistically significant difference was found for the OS
rate between the two groups (P = 0.908) (Fig. 2b).
Predictors of higher intravesical RFS rate on
multivariate analysis included concomitant bladder urothelial
carcinoma (odds ratio [OR] 2.71, 95% confidence
interval [CI] 1.22–5.99, P = 0.014), undergoing
extravesical management of distal ureter (P < 0.001), and not
having received adjuvant chemotherapy (OR 0.28, 95%
CI 0.09–0.90, P = 0.033) (Table 2). However, there was
no association between surgical approach and
intravesical RFS in multivariate cox regression (OR 1.23, 95% CI
0.46–3.65, P = 0.622) (Table 2).
Meanwhile, in the multivariate analysis, the type of
surgery was not an independent predictor of overall RFS (OR
0.99, 95% CI 0.54–1.83, P = 0.974) (Table 2). However, four
clinical pathological parameters were identified as probable
predictors of overall RFS in multivariate Cox regression
models: tumor location (P = 0.003), LVI (OR 2.03, 95% CI
1.39–2.96, P < 0.001), tumor grade (OR 2.47, 95% CI 1.51–
4.03, P < 0.001), and pT stage (P < 0.001) (Table 2).
Table 3 presents the results of the multivariate analysis
examining predictors of CSS and OS in the cohort. On
multivariate analysis, LVI, tumor grade, and pT stage
were the only independent predictors of CSS (P < 0.05
for all; Table 3). Similarly, LVI, tumor grade, and pT
stage were the independent predictors of OS (P < 0.05
for all; Table 3). The type of procedure, ONU or LNU,
was not an independent predictor of CSS (OR 1.38, 95%
CI 0.61–3.13, P = 0.444; Table 3) or OS (OR 1.61, 95%
CI 0.82–3.17, P = 0.17; Table 3).
Fig. 1 Intravesical recurrence-free survival (a) and Overall recurrence-free survival rates (b) in 265 patients treated with either ONU (n = 213) or
LNU (n = 52) for UTUC
Clayman et al. performed the first successful LNU in
1991 . Multiple reports have since described the
efficacy of LNU for favorable-risk UTUC patients regarding
cancer control [5–19]. In recent years, experienced
surgeons have expanded their criteria for LNU for large or
locally advanced UTUC, which indicated the
effectiveness of laparoscopic surgery. To compare the efficacy of
LNU and ONU in localized and/or locally advanced
UTUC, we performed the present study, including 265
patients with T1–4/N0-X UTUC (213 ONU vs. 52 LNU)
treated with RNU. The Kaplan-Meier plot illustrated no
significant difference in survival between the two groups
of different procedures. Multivariate analysis suggested
the equivalence of LNU and ONU in terms of
intravesical RFS, overall RFS, CSS, and OS. During the later
courses of our study, Kim et al.  reported that the
5-year OS and CSS rates were lower in the LNU group
than in the ONU group in patients with locally advanced
UTUC. Furthermore, on multivariable analysis, LNU
was found to be an independent predictor of poorer OS
and CSS than ONU. However, the study has some
limitations: On the one hand, the cohort patients included
N+ disease. On the other hand, the study did not
analyze the cigarette smoking status, despite the fact that
exposure to smoking is a significant risk factor for
bladder urothelial carcinoma as well as UTUC. Thus,
the comparison between Kim’s study and our study is
difficult to make.
It is essential to follow the oncological principles and
the established surgery procedure for laparoscopic surgery
in urothelial carcinomas [8, 11, 14]. According to
previously published papers, tumors cells may undergo
retroperitoneal metastatic dissemination and dissemination
Female 0.59 (0.28–1.3)
Yes 1.41 (0.76–2.58)
Yes 1.10 (0.59–2.03)
Previous bladder urothelial carcinoma
Yes 1.56 (0.56–4.7)
Concomitant bladder urothelial carcinoma
Yes 1.95 (1.01–3.76)
Right 1.38 (0.77–2.48)
Renal pelvis 1
Ureter 1.67 (0.89–3.17)
Renal pelvis and ureter 2.82 (1.02–7.78)
Tumor size, continuous 0.90 (0.76–1.06)
Multifocal 1.17 (0.65–2.09)
Table 2 Univariable and multivariable cox regression models predicting intravesical RFS and Overall RFS of 265 patients with UTUC
after radical nephroureterectomy (Continued)
Distal ureter management
Type of procedure
along the trocar pathway under pneumoperitoneal
circumstances during operation. Initial researchers despised
laparoscopic operation in urothelial carcinomas because
the high-pressure environment of pneumoperitoneum
was thought to promote tumor dissemination and
recurrence. To our best knowledge, only 12 cases of
laparoscopic port-site seeding are available in English literature
. In our study, only one case was seen in our early
experiences, which may be associated with the limited use
of laparoscopic bags in the early days. Nowadays,
precautionary measures have been taken into consideration to
prevent potential tumor spillage. It has been stressed that
direct contact between the instrument and the tumor
should be forbidden during dissection. Besides, LNU must
be accomplished in a closed system.
In patients with organ-confined UTUC, LNU has the
advantage of minimal invasiveness and has oncological
outcomes comparable to those of ONU. However, its
effectiveness in patients with localized and/or locally
advanced diseases remains to be proven, and the results
were contradictory. Our findings were consistent with
results from one single center study  and two recent
multi-institutional studies [4, 9], which showed no
independent association between surgical approach and
survival, in both organ-confined and advanced UTUC
patients. Unfortunately, some authors reported that
relative to ONU, LNU was associated with an adverse
prognosis in advanced stage patients. Fairey and colleagues
 published a multi-institutional retrospective study
comparing ONU and LNU in 849 patients. These
authors report equivalent OS and CSS for the surgical
approaches. However, there was a trend toward an
independent association between surgical approach and RFS
(OR 1.24, 95% CI 0.98–1.57, P = 0.08). Furthermore,
when stratifying by stage on multivariate Cox regression
models, LNU was independently associated with poorer
RFS in patients with ≤ pT2N0 and pTanyN1-3 disease:
however, there was no independent association between
surgical approach and RFS in patients with pT3-4 N0
disease. In the only prospective randomized study
published in the literature, Simone and colleagues 
reported 80 UTUC patients treated with ONU (n = 40)
and LNU (n=40). After a median follow-up of 44 months,
for organ-confined disease, the two groups did not differ
significantly in the rates of intravesical RFS and CSS.
However, when matched for pT3 and high-grade tumors,
CSS and metastasis-free survival were significantly
different between the two groups, in favor of ONU.
However, the conclusions based on previous results
are underpowered because of the different statistical
models used. The factors of UTUC tumor location [24, 25],
previous bladder tumor history [26, 27], and previous
hydronephrosis [28, 29] should be included in the model
because the predictive significance of these factors remains
controversial. Additionally, cigarette smoking status should
be included in the analysis because exposure to smoking is
a significant risk factor for bladder urothelial carcinoma as
well as UTUC . Furthermore, imbalances are apparent
in some of these important series [9, 11, 13]. The LNU
group contained tumors at lower stages and they had a
lower rate of LVI. These differences, were statistically
significant. This may be compensated for by the multivariate
analysis and further corrected using various statistical
techniques; nevertheless, it reflects significant patient selection
in which, generally speaking, LNU was avoided in the
higher stage cases. Thus, because of the smaller proportion
of higher stage cases performed laparoscopically, the overall
outcome was skewed by the good prognosis of the lower
stage cases. In comparison with previous results, our
groups were better matched for prognostic factors, such as
tumor stage, grade, and LVI, and we include some
controversial elements, such as tumor location, previous bladder
tumor history, and previous hydronephrosis. Therefore, we
could draw more relevant conclusions. In addition, several
Female 1.11 (0.68–1.80)
Yes 1.37 (0.87–2.14)
Yes 1.47 (0.91–2.38)
Previous bladder urothelial carcinoma
Yes 1.24 (0.54–2.86)
Concomitant bladder urothelial carcinoma
Yes 1.14 (0.66–1.97)
Right 0.87 (0.56–1.33)
Renal pelvis 1
Ureter 1.35 (0.85–2.15)
Renal pelvis and ureter 2.61 (1.28–5.34)
Tumor size, continuous 1.13 (1.03–1.26)
Multifocal 1.49 (0.97–2.28)
Table 3 Univariable and multivariable cox regression models predicting CSS and OS of 265 patients with UTUC after radical
Table 3 Univariable and multivariable cox regression models predicting CSS and OS of 265 patients with UTUC after radical
Distal ureter management
Type of procedure
Bold values indicate that P-value ≤ 0.05, and considered statistically significant. ONU open radical nephroureterectomy, LNU laparoscopic radical
nephroureterectomy, UTUC upper tract urothelial carcinoma, LVI lymphovascular invasion, CSS cancer specific survival, OS overall survival, OR odds ratio, CI
limitations of this study should be mentioned. First, the
data were collected retrospectively and reflect the
experiences of two institutions. Furthermore, different bladder
cuff managements were used between the LNU and ONU
groups. Second, the majority of patients were underwent
open procedures; moreover, the laparoscopic cohort
included those operated on using retroperitoneal and
transperitoneal approaches. Third, pathological specimens were
not subjected to a centralized review. In additon, the
follow-up period was relatively short.
In summary, after a median follow-up of 60.0 months,
oncological results were comparable between LNU and
ONU for the treatment of localized and/or locally
advanced UTUC (T1–4/N0-X). Our data could be used as
evidence for equivalent cancer control outcomes
between LNU and ONU in patients with T1–4/N0-X
UTUC. Further analyses, including randomized trials,
are needed to generalize these conclusions to patients
with more unfavorable disease characteristics.
CI: Confidence interval; CSS: Cancer-specific survival; LNU: Laparoscopic
radical nephroureterectomy; LVI: Lymphovascular invasion; ONU: Radical
nephroureterectomy; OR: Odds ratio; OS: Overall survival; RFS:
Recurrence-free survival; RNU: Radical nephroureterectomy; UTUC: Upper
tract urothelial carcinoma; WHO/ISUP: World Health Organization/
International Society of Urologic Pathology
Availability of data and materials
The datasets supporting the conclusions of this article are included within
LYH raised study concepts and participated in study design. JYL together
with LYH performed the study. JYL drafted the manuscript. ZL and JT
(Jing Tan) collected the clinical data and participated in statistical analysis. JT
(Jin Tang), BL, and KY participated in quality control of data and algorithms.
YBD, FJZ, YHL and DX critically revised the manuscript. All authors read and
approved the final manuscript.
The authors declare that they have no competing interests.
Ethics approval and consent to participate
The study was approved by the ethics committee of the Third Xiangya
Hospital of Central South University.
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