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Erschienen in: BMC Urology 1/2019

Open Access 01.12.2019 | Research article

Oncologic outcomes comparison of partial ureterectomy and radical nephroureterectomy for urothelial carcinoma

verfasst von: Shengxian Li, Yuchen Pan, Jinghai Hu

Erschienen in: BMC Urology | Ausgabe 1/2019

Abstract

Background

The appropriate application of various treatment for upper tract urothelial carcinomas (UTUCs) is the key to prolong the survival of UTUC patients. Herein, we used data in our database to assess the oncological outcomes between partial ureterectomy (PU) and radical nephroureterectomy (RNU).

Methods

From 2007 to 2014, 255 patients with UTUC undergoing PU or RNU in our hospital database were investigated. Perioperative, postoperative data, and pathologic outcomes were obtained from our database. Cancer-specific survival (CSS) was assessed through the Kaplan-Meier method with Cox regression models to test the effect of these two surgery types.

Results

The mean length of follow-up was 35.8 months (interquartile range 10–47 months). Patients with high pT stage (pT2–4) suffered shorter survival span (HR: 9.370, 95% CI: 2.956–29.697, P < 0.001). There were no significant differences in CSS between PU and RNU (P = 0.964). In the sub-analysis, CSS for RNU and PU showed no significant difference for pTa–1 or pT2–4 tumor patients (P = 0.516, P = 0.475, respectively).

Conclusions

PU is not inferior to RNU in oncologic outcomes. Furthermore, PU is generally recognized with less invasive and better renal function preservation compared with RNU. Thus, PU would be rational for specific patients with UTUCs.
Hinweise

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Abkürzungen
CSS
Cancer-specific survival
CT
Computed tomography
KSS
Kidney-sparing surgery
PU
Partial ureterectomy
RFS
Recurrence-free survival
RNU
Radical nephroureterectomy
UC
Urothelial carcinomas
UTUC
Upper tract urothelial carcinoma

Background

Upper tract urothelial carcinomas (UTUCs), as a kind of urothelial carcinomas (UCs), accounting for only 5–10% [1]. Generally, 60% of UTUCs are invasive [2]. Seventy to Ninety years old showed the highest morbid risk among all age groups and are three times more ordinary in men [2]. UTUC with pure nonurothelial histology is quite rare, but about 25% of cases have variants. Computed tomography (CT) is an available imaging technique with high diagnostic accuracy [3]. In about 90% of cases, the tumor grade can be determined with a low false negative rate [4]. Ureteroscopic biopsy combining with urinary cytology, and imaging findings such as hydronephrosis may contribute for the decision of surgical type like partial ureterectomy (PU) and radical nephroureterectomy (RNU) [5]. Tumor stage and grade, lymph node involvement, lymphovascular invasion, surgical margins, and pathological factors could be used to estimate prognosis [2]. Nowadays, the concept for preservation of renal function has been emphasized. For low-risk UTUC, kidney-sparing surgery (KSS) unlike radical surgery could preserve kidney function without compromising oncological outcomes. KSS such as PU are performed for the patients with solitary kidney, renal insufficiency, or low-risk tumors. RNU is still the standard treatment for high-risk UTUCs, no matter where the tumor location is [2, 6]. Herein, we used data in our database to assess the oncological outcomes between PU and RNU.

Methods

Study population and treatment

The research protocol was approved by the ethics committee of Jilin University’s Institutional Ethical Review Board, and written informed consent was obtained. Three hundred thirty two patients with UTUC from January 2007 to December 2014 in our database were included in First Hospital of Jilin University. Of them, 52 patients were excluded for suspected multifocal tumors in the upper urinary tract preoperatively. Another 25 patients were excluded for distant metastases (n = 14), no surgical treatment (n = 3), suffering previous or concurrent radical cystectomy (n = 8). Among the remaining 255 patients, 182 of them underwent RUN, 73 of them underwent PU. All Patients were evaluated disease progression by CT preoperatively. During the study period, ureteroscopy with biopsy was not routinely performed. The choice and surgical technique of RNU and PU could not be standardized. Surgeon preferences have a significant impact on the selection and surgical technique of RNU and PU. For RNU, the kidney and entire ureter with a bladder cuff were excised. PU was performed along with the excision of ureteral segment. There were no statistically differences between age at surgery, sex, tumor side, presence of hematuria, and presence of hydronephrosis. Clinical and pathological staging was in accordance with TNM classification 2002 [7, 8].

Statistical analysis

Outcomes were measured by survival time (from the time of surgery to cancer specific mortality). Continuous variables were described as the median (interquartile range). T tests or nonparametric tests were carried out to assess the differences in variables with a continuous distribution. Categorical variables were described as the frequency (percentage) and analyzed by the Chi-square or Fisher exact test. The Cox proportional hazard models were employed for univariate and multivariate analyses to determine whether surgery type (RNU vs PU) and other variables was associated with CSS. The survival curves of each stratified variablewere plotted by the Kaplan-Meier method and compared by log-rank test. SPSS version 18.0 (SPSS Inc., Chicago, IL) was used for statistical analyses. All P values were two-tailed, and P value < 0.05 indicated statistical significance.

Results

Clinicopathological characteristics

The mean length of follow-up was 35.8 months (interquartile range 10–47 months). The baseline characteristics of the patients are shown in Table 1. The mean age and percent of male in RNU group were 66.74 ± 8.41 and 49.5%, respectively; 67.62 ± 10.09 and 41.4% in PU group, respectively. Smokers in RNU group were much more than in PU group (38.2% vs 15.6%, P = 0.021). In RNU group, half of the patients had tumor in the left kidney (54.1%). PU group is contrary to it (39.7%). The proportion of patients with hydronephrosis, hematuria or abnormal renal function in RNU group were close to PU group (P > 0.05). Compared with PU group,operation time of patients in RNU group was much longer (157.50 (116.25–180.00) vs 95.00 (76.25–126.25), P < 0.001). In RNU group, nearly half (42.0%) were diagnosed at pT stage1, 5.2% at pT stage a, 27.6% at pT stage 2, 23.6% at pT stage 3, and only 1.7% at pT stage4. In PU group, the proportion is 49.3, 3, 37.3, 9, and 1.5%, respectively.
Table 1
Clinical and pathologic characteristics of the two groups
Variables
RNU
PU
t/χ2
P
Age
66.74 ± 8.41
67.62 ± 10.09
−0.709
0.479
Sex
 Male
90 (49.5%)
30 (41.4%)
1.460
0.227
 Female
92 (50.5%)
43 (58.9%)
  
Smoking
 No
47 (61.8%)
27 (84.4%)
5.300
0.021
 Yes
29 (38.2%)
5 (15.6%)
  
Tumor side
 Left
98 (54.1%)
29 (39.7%)
4.325
0.038
 Right
83 (45.9%)
44 (60.3%)
  
Hydronephrosis
 No
18 (10.3%)
11 (16.4%)
1.727
0.189
 Yes
157 (89.7%)
56 (83.6%)
  
Hematuria
 No
59 (33.7%)
30 (44.1%)
2.283
0.131
 Yes
116 (66.3%)
38 (55.9%)
  
Renal function
 Normal
48 (43.6%)
20 (47.6%)
0.195
0.659
 Abnormal
63 (56.4%)
22 (52.4%)
  
Operation time
157.50 (116.25–180.00)
95.00 (76.25–126.25)
−4.476
< 0.001
pT stage
8.287
0.067
 pTa
9 (5.2%)
2 (3.0%)
  
 pT 1
73 (42.0%)
33 (49.3%)
  
 pT 2
48 (27.6%)
25 (37.3%)
  
 pT 3
41 (23.6%)
6 (9.0%)
  
 pT 4
3 (1.7%)
1 (1.5%)
  
Lymphovascular invasion
4 (2.2%)
0 (0%)
1.630
0.202
RUN Radical nephroureterectomy, PU Partial ureterectomy

Oncological outcome

Univariable and multivariable analyses for CSS after surgery were shown in Table 2. On multivariable analysis, pT stage was significantly associated with CSS. The results showed that patients with high pT stage (pT2–4) suffered shorter survival span (HR: 9.370, 95% CI: 2.956–29.697, P < 0.001). The independent predictors of CSS were higher pT (P < 0.001; Table 2). The specific results are exhibited in Table 2. Furthermore, there were no significant differences in CSS between PU and RNU (P = 0.964) (Fig. 1). In the sub-analysis, there was no significant difference in 3-year CSS probability between pTa–1 tumor patients treated with RNU (87.7%) and PU (82.9%) (P = 0.516). Similarly, for patients with pT2–4 tumors, 3-year CSS for RNU and PU showed no significant difference (38.0% vs 31.3%, P = 0.475, respectively) (Fig. 2).
Table 2
Cox regression analysis of factors associated with CSS
Variables
Univariate
Multivariate
HR
95% CI
P
HR
95% CI
P
Age (years)
  ≤ 70
1.000
  
1.000
  
  > 70
0.885
0.581–1.348
0.569
1.240
0.488–3.150
0.652
Sex
 Male
1.000
  
1.000
  
 Female
0.713
0.478–1.062
0.096
1.328
0.477–3.693
0.587
Smoking
 No
1.000
  
1.000
  
 Yes
1.095
0.548–2.190
0.797
0.695
0.225–2.147
0.527
Tumor side
 Left
1.000
  
1.000
  
 Right
0.726
0.486–1.084
0.117
1.136
0.451–2.861
0.787
Hydronephrosis
 No
1.000
  
1.000
  
 Yes
1.134
0.588–2.188
0.707
0.742
0.149–3.698
0.716
Hematuria
 No
1.000
  
1.000
  
 Yes
1.307
0.842–2.029
0.233
2.405
0.820–7.048
0.110
Renal function
 Normal
1.000
  
1.000
  
 Abnormal
1.130
0.688–1.911
0.650
1.503
0.613–3.686
0.374
pT stage
 pTa–1
1.000
  
1.000
  
 pT2–4
6.907
4.028–11.845
< 0.001
9.370
2.956–29.697
< 0.001
Surgical intervention
 RNU
1.000
  
1.000
  
 PU
1.010
0.651–1.567
0.964
1.705
0.608–4.778
0.310
RUN Radical nephroureterectomy, PU Partial ureterectomy

Discussion

UTUC is a kind of rare malignancy. The main treatments for URUC are RNU and KSS like PU. Recent data indicated that patients with low grade UTUC could be treated by PU effectively. The guidelines of the European Association of Urology suggested that PU is a legitimate therapy for small, unifocal, low grade UTUC with no signs of infiltration [2, 7, 9], and indicated that RNU is still the standard treatment for high-risk UTUCs [2, 10]. However, Bagrodia et al. compared the prognosis of UTUC patients who suffered either RNU or PU. They suggested that PU seemed to possess oncologic efficacy equal to RNU. Meanwhile, PU could preserve the renal function to the maximum extent [9]. Similar results were also demonstrated in the investigation from Fukushima et al. [11]. Colin et al. conducted a multicenter cohort study of UTUC which suggested that surgical interventions was not the independent prognostic factor for recurrence-free survival (RFS) and CSS [6]. The investigation from Hung et al. indicated that the local recurrences, bladder recurrences, distant metastasis, and CSS showed no significant differences between RNU and PU [12]. These findings mentioned above would show the ability of PU to maximize the preservation of renal function in carefully selected patients.
In the current study, we noticed that pathological stage remained the most important predictor for the CSS of patients with UTUCs. The results also revealed that CSS showed no significant differences between RNU and PU in both low pT stage (pTa–1) and high pT stage (pT2–4) UTUCs. The probable reason is that the number of patients involved in our study is not large enough, thus this study may not be powerful enough to show significance [6]. Furthermore, there were some selection biases that RNU group seemed to have more aggressive pathological features compared with PU group, because there was not the standardized indication for PU and surgeon preferred PU for lower stage UTUCs [13, 14]. Selection biases can lead to better survival in PU group compared with RNU group, though the difference was not significant in our analysis. Our findings, and similar findings from other researchers, indicated that PU could act as a selectable treatment for selected UTUC patients [15]. In addition, pathologists with expertise rechecked all the pathologic specimens, and all pathologic results were collected standardly.
This study is retrospective study, and the number of involved patients is relatively small. These two characteristics are the main limitations of this study. Because a prospective randomized controlled study of PU compared with RNU is difficult due to the rarity of UTUC. Secondly, we could not ascertain whether PU was done imperatively or electively. Furthermore, surgeon preferences have a great impact on the surgical technique and indication for RNU and PU, which could not be determined standardly. Nor can we assess which cases are suitable for endoscopic treatment when receiving RNU therapy [16, 17].. Multiple surgeons were employed to operate on the investigated patients. This situation might lead to a selection bias and variable surgical techniques. Finally, another limitation of our research is that we could not provide the information about tumor grade and metastases due to the sample problem.

Conclusion

In conclusion, PU and RNU might possess equivalent long-term oncologic outcomes. Furthermore, PU could reduce the adverse outcomes of nephron loss caused by RNU. PU could be rational selection for selected patients with UTUCs. Further randomized researches compared with PU and RNU are still necessary to support the results. Prospective trials with large sample sizes are essential to more accurately assess the role of PU in UTUC.

Acknowledgments

Not applicable.
All procedures were approved by the Ethics Committee of First Hospital of Jilin University. Permission was obtained to access the data of First Hospital of Jilin University.
The data do not contain any information that could identify the patient. A copy of the written consent is available for review by the Editor of this journal.

Competing interests

The authors declare that they have no competing interests.
Open AccessThis 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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Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Literatur
1.
Zurück zum Zitat Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018;68(1):7–30.CrossRef Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018;68(1):7–30.CrossRef
2.
Zurück zum Zitat Roupret M, Babjuk M, Comperat E, Zigeuner R, Sylvester RJ, Burger M, et al. European Association of Urology guidelines on upper urinary tract urothelial carcinoma: 2017 update. Eur Urol. 2018;73(1):111–22.CrossRef Roupret M, Babjuk M, Comperat E, Zigeuner R, Sylvester RJ, Burger M, et al. European Association of Urology guidelines on upper urinary tract urothelial carcinoma: 2017 update. Eur Urol. 2018;73(1):111–22.CrossRef
3.
Zurück zum Zitat Zigeuner R, Shariat SF, Margulis V, Karakiewicz PI, Roscigno M, Weizer A, et al. Tumour necrosis is an indicator of aggressive biology in patients with urothelial carcinoma of the upper urinary tract. Eur Urol. 2010;57(4):575–81.CrossRef Zigeuner R, Shariat SF, Margulis V, Karakiewicz PI, Roscigno M, Weizer A, et al. Tumour necrosis is an indicator of aggressive biology in patients with urothelial carcinoma of the upper urinary tract. Eur Urol. 2010;57(4):575–81.CrossRef
5.
Zurück zum Zitat Clements T, Messer JC, Terrell JD, Herman MP, Ng CK, Scherr DS, et al. High-grade ureteroscopic biopsy is associated with advanced pathology of upper-tract urothelial carcinoma tumors at definitive surgical resection. J Endourol. 2012;26(4):398–402.CrossRef Clements T, Messer JC, Terrell JD, Herman MP, Ng CK, Scherr DS, et al. High-grade ureteroscopic biopsy is associated with advanced pathology of upper-tract urothelial carcinoma tumors at definitive surgical resection. J Endourol. 2012;26(4):398–402.CrossRef
6.
Zurück zum Zitat Colin P, Ouzzane A, Pignot G, Ravier E, Crouzet S, Ariane MM, et al. Comparison of oncological outcomes after segmental ureterectomy or radical nephroureterectomy in urothelial carcinomas of the upper urinary tract: results from a large French multicentre study. BJU Int. 2012;110(8):1134–41.CrossRef Colin P, Ouzzane A, Pignot G, Ravier E, Crouzet S, Ariane MM, et al. Comparison of oncological outcomes after segmental ureterectomy or radical nephroureterectomy in urothelial carcinomas of the upper urinary tract: results from a large French multicentre study. BJU Int. 2012;110(8):1134–41.CrossRef
7.
Zurück zum Zitat Amin MB, Greene FL, Edge SB, Compton CC, Gershenwald JE, Brookland RK, et al. The eighth edition AJCC cancer staging manual: continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. CA Cancer J Clin. 2017;67(2):93–9.CrossRef Amin MB, Greene FL, Edge SB, Compton CC, Gershenwald JE, Brookland RK, et al. The eighth edition AJCC cancer staging manual: continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. CA Cancer J Clin. 2017;67(2):93–9.CrossRef
8.
Zurück zum Zitat Mostofi FK, Sobin LH, Torloni H, Organization WH. Histological typing of urinary bladder tumours; 1973. Mostofi FK, Sobin LH, Torloni H, Organization WH. Histological typing of urinary bladder tumours; 1973.
9.
Zurück zum Zitat Bagrodia A, Kuehhas FE, Gayed BA, Wood CG, Raman JD, Kapur P, et al. Comparative analysis of oncologic outcomes of partial ureterectomy vs radical nephroureterectomy in upper tract urothelial carcinoma. Urology. 2013;81(5):972–7.CrossRef Bagrodia A, Kuehhas FE, Gayed BA, Wood CG, Raman JD, Kapur P, et al. Comparative analysis of oncologic outcomes of partial ureterectomy vs radical nephroureterectomy in upper tract urothelial carcinoma. Urology. 2013;81(5):972–7.CrossRef
10.
Zurück zum Zitat Seisen T, Peyronnet B, Dominguez-Escrig JL, Bruins HM, Yuan CY, Babjuk M, et al. Oncologic outcomes of kidney-sparing surgery versus radical Nephroureterectomy for upper tract urothelial carcinoma: a systematic review by the EAU non-muscle invasive bladder cancer guidelines panel. Eur Urol. 2016;70(6):1052–68.CrossRef Seisen T, Peyronnet B, Dominguez-Escrig JL, Bruins HM, Yuan CY, Babjuk M, et al. Oncologic outcomes of kidney-sparing surgery versus radical Nephroureterectomy for upper tract urothelial carcinoma: a systematic review by the EAU non-muscle invasive bladder cancer guidelines panel. Eur Urol. 2016;70(6):1052–68.CrossRef
11.
Zurück zum Zitat Fukushima H, Saito K, Ishioka J, Matsuoka Y, Numao N, Koga F, et al. Equivalent survival and improved preservation of renal function after distal ureterectomy compared with nephroureterectomy in patients with urothelial carcinoma of the distal ureter: a propensity score-matched multicenter study. Int J Urol. 2014;21(11):1098–104.CrossRef Fukushima H, Saito K, Ishioka J, Matsuoka Y, Numao N, Koga F, et al. Equivalent survival and improved preservation of renal function after distal ureterectomy compared with nephroureterectomy in patients with urothelial carcinoma of the distal ureter: a propensity score-matched multicenter study. Int J Urol. 2014;21(11):1098–104.CrossRef
12.
Zurück zum Zitat Hung SY, Yang WC, Luo HL, Hsu CC, Chen YT, Chuang YC. Segmental ureterectomy does not compromise the oncologic outcome compared with nephroureterectomy for pure ureter cancer. Int Urol Nephrol. 2014;46(5):921–6.CrossRef Hung SY, Yang WC, Luo HL, Hsu CC, Chen YT, Chuang YC. Segmental ureterectomy does not compromise the oncologic outcome compared with nephroureterectomy for pure ureter cancer. Int Urol Nephrol. 2014;46(5):921–6.CrossRef
13.
Zurück zum Zitat Pedrosa JA, Masterson TA, Rice KR, Kaimakliotis HZ, Monn MF, Bihrle R, et al. Oncologic outcomes and prognostic impact of urothelial recurrences in patients undergoing segmental and total ureterectomy for upper tract urothelial carcinoma. Can Urol Assoc J. 2015;9(3–4):E187–92.CrossRef Pedrosa JA, Masterson TA, Rice KR, Kaimakliotis HZ, Monn MF, Bihrle R, et al. Oncologic outcomes and prognostic impact of urothelial recurrences in patients undergoing segmental and total ureterectomy for upper tract urothelial carcinoma. Can Urol Assoc J. 2015;9(3–4):E187–92.CrossRef
14.
Zurück zum Zitat Simhan J, Smaldone MC, Egleston BL, Canter D, Sterious SN, Corcoran AT, et al. Nephron-sparing management vs radical nephroureterectomy for low- or moderate-grade, low-stage upper tract urothelial carcinoma. BJU Int. 2014;114(2):216–20.CrossRef Simhan J, Smaldone MC, Egleston BL, Canter D, Sterious SN, Corcoran AT, et al. Nephron-sparing management vs radical nephroureterectomy for low- or moderate-grade, low-stage upper tract urothelial carcinoma. BJU Int. 2014;114(2):216–20.CrossRef
15.
Zurück zum Zitat Dalpiaz O, Ehrlich G, Quehenberger F, Pummer K, Zigeuner R. Distal ureterectomy is a safe surgical option in patients with urothelial carcinoma of the distal ureter. Urol Oncol. 2014;32(1):34 e31–8.CrossRef Dalpiaz O, Ehrlich G, Quehenberger F, Pummer K, Zigeuner R. Distal ureterectomy is a safe surgical option in patients with urothelial carcinoma of the distal ureter. Urol Oncol. 2014;32(1):34 e31–8.CrossRef
16.
Zurück zum Zitat Fajkovic H, Klatte T, Nagele U, Dunzinger M, Zigeuner R, Hubner W, et al. Results and outcomes after endoscopic treatment of upper urinary tract carcinoma: the Austrian experience. World J Urol. 2013;31(1):37–44.CrossRef Fajkovic H, Klatte T, Nagele U, Dunzinger M, Zigeuner R, Hubner W, et al. Results and outcomes after endoscopic treatment of upper urinary tract carcinoma: the Austrian experience. World J Urol. 2013;31(1):37–44.CrossRef
17.
Zurück zum Zitat Cutress ML, Stewart GD, Tudor EC, Egong EA, Wells-Cole S, Phipps S, et al. Endoscopic versus laparoscopic management of noninvasive upper tract urothelial carcinoma: 20-year single center experience. J Urol. 2013;189(6):2054–60.CrossRef Cutress ML, Stewart GD, Tudor EC, Egong EA, Wells-Cole S, Phipps S, et al. Endoscopic versus laparoscopic management of noninvasive upper tract urothelial carcinoma: 20-year single center experience. J Urol. 2013;189(6):2054–60.CrossRef
Metadaten
Titel
Oncologic outcomes comparison of partial ureterectomy and radical nephroureterectomy for urothelial carcinoma
verfasst von
Shengxian Li
Yuchen Pan
Jinghai Hu
Publikationsdatum
01.12.2019
Verlag
BioMed Central
Erschienen in
BMC Urology / Ausgabe 1/2019
Elektronische ISSN: 1471-2490
DOI
https://doi.org/10.1186/s12894-019-0557-2

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