International Journal of Clinical Oncology

, Volume 23, Issue 4, pp 726–733 | Cite as

Oncologic outcomes for open and laparoscopic radical nephroureterectomy in patients with upper tract urothelial carcinoma

  • Koichi Kido
  • Shingo Hatakeyama
  • Naoki Fujita
  • Hayato Yamamoto
  • Yuki Tobisawa
  • Tohru Yoneyama
  • Takahiro Yoneyama
  • Yasuhiro Hashimoto
  • Takuya Koie
  • Ikuya Iwabuchi
  • Masaru Ogasawara
  • Toshiaki Kawaguchi
  • Chikara Ohyama
Original Article



Oncologic benefits of laparoscopic radical nephroureterectomy (LNU) are unclear. We aimed to evaluate the impact of surgical approach for radical nephroureterectomy on oncologic outcomes in patients with locally advanced upper tract urothelial carcinoma (UTUC).


Of 426 patients who underwent radical nephroureterectomy at five medical centers between February 1995 and February 2017, we retrospectively investigated oncological outcomes in 229 with locally advanced UTUC (stages cT3-4 and/or cN+). The surgical approach was classified as open nephroureterectomy (ONU) or LNU, and oncologic outcomes, including intravesical recurrence-free survival (RFS), visceral RFS, cancer-specific survival (CSS), and overall survival (OS), were compared between the groups. The inverse probability of treatment weighting (IPTW)-adjusted Cox-regression analyses was performed to evaluate the impact of LNU on the prognosis.


Of the 229 patients, 48 (21%) underwent LNU. There were significant differences in patient backgrounds, including preoperative renal function, lymph-node involvement, lymphovascular invasion, and surgical margins, between the groups. Before the background adjustment, intravesical RFS, visceral RFS, CSS, and OS were significantly inferior in the ONU group than in the LNU group. However, in the IPTW-adjusted Cox-regression analysis, no significant differences were observed in intravesical RFS (hazard ratio [HR], 0.65; P = 0.476), visceral RFS (HR, 0.46; P = 0.109), CSS (HR, 0.48; P = 0.233), and OS (HR, 0.40; P = 0.147).


Surgical approaches were not independently associated with prognosis in patients with locally advanced UTUC.


Upper tract urothelial carcinoma Radical nephroureterectomy Laparoscopic Oncologic outcome 



Upper tract urothelial carcinoma


Open radical nephroureterectomy


Laparoscopic radical nephroureterectomy


Inverse probability of treatment weighting


Eastern Cooperative Oncology Group performance status




Cardiovascular disease


Diabetes mellitus


Estimated glomerular filtration rate


Chronic kidney disease


Neoadjuvant chemotherapy


Lymphovascular invasion


Recurrence-free survival


Cancer-specific survival


Overall survival


Hazard ratio


Confidence interval



The authors would like to thank Hiroyuki Ito, Kazuaki Yoshikawa, Atsushi Sasaki, Hiromichi Iwamura, Ken Fukushi, Jotaro Mikami, Takuma Narita, Toshikazu Tanaka, Itsuto Hamano, Yuki Fujita, Yukie Nishizawa, Satomi Sakamoto, and Yuriko Tanabe for their invaluable help with data collection. The authors would also like to thank Enago ( for the English language review.

Author contributions

Conception and design: Shingo Hatakeyama. Acquisition of data: Koichi Kido, Naoki Fujita, Shingo Hatakeyama, Takahiro Yoneyama, Yasuhiro Hashimoto, Takuya Koie, Ikuya Iwabuchi, Masaru Ogasawara, Toshiaki Kawaguchi. Analysis and interpretation of data: Shingo Hatakeyama, Yuki Tobisawa, Tohru Yoneyama. Drafting of the manuscript: Koichi Kido, Shingo Hatakeyama. Critical revision of the manuscript: Naoki Fujita, Takuya Koie, Chikara Ohyama. Statistical analysis: Shingo Hatakeyama, Tohru Yoneyama. Obtaining funding: Shingo Hatakeyama, Takuya Koie, Chikara Ohyama. Administrative, technical, or material support: Yuki Tobisawa, Tohru Yoneyama

Compliance with ethical standards

Conflict of interests

The authors declare no conflicts of interest.

Financial disclosure

This work was supported by a Grant-in-Aid for Scientific Research (No. 15H02563, 15K15579, 17K11118, 17K11119, 17K16768, 17K16770, and 17K16771) from the Japan Society for the Promotion of Science.

Ethical standards

This study was performed in accordance with the ethical standards of the Declaration of Helsinki and approved by an ethics review board of Hirosaki University School of Medicine (authorization numbers; 2017–089) and all other hospitals.

Informed consent

For this type of study, formal written consent is not required. Pursuant to the provisions of the ethics committee and the ethic guideline in Japan, written consent was not required in exchange for public disclosure of study information in the case of retrospective and/or observational study using a material such as the existing documentation. The study information was open for the public consumption at


  1. 1.
    Roupret M, Babjuk M, Comperat E et al (2015) European Association of Urology Guidelines on Upper Urinary Tract Urothelial Cell Carcinoma: 2015 Update. Eur Urol 68(5):868–879. CrossRefPubMedGoogle Scholar
  2. 2.
    Miyazaki J, Nishiyama H, Fujimoto H et al (2016) Laparoscopic versus open nephroureterectomy in muscle-invasive upper tract urothelial carcinoma: subanalysis of the Multi-Institutional National Database of the Japanese Urological Association. J Endourol 30(5):520–525. CrossRefPubMedGoogle Scholar
  3. 3.
    Capitanio U, Shariat SF, Isbarn H et al (2009) Comparison of oncologic outcomes for open and laparoscopic nephroureterectomy: a multi-institutional analysis of 1249 cases. Eur Urol 56(1):1–9. CrossRefPubMedGoogle Scholar
  4. 4.
    Simone G, Papalia R, Guaglianone S et al (2009) Laparoscopic versus open nephroureterectomy: perioperative and oncologic outcomes from a randomised prospective study. Eur Urol 56(3):520–526. CrossRefPubMedGoogle Scholar
  5. 5.
    Ariane MM, Colin P, Ouzzane A et al (2012) Assessment of oncologic control obtained after open versus laparoscopic nephroureterectomy for upper urinary tract urothelial carcinomas (UUT-UCs): results from a large French multicenter collaborative study. Ann Surg Oncol 19(1):301–308. CrossRefPubMedGoogle Scholar
  6. 6.
    Ni S, Tao W, Chen Q et al (2012) Laparoscopic versus open nephroureterectomy for the treatment of upper urinary tract urothelial carcinoma: a systematic review and cumulative analysis of comparative studies. Eur Urol 61(6):1142–1153. CrossRefPubMedGoogle Scholar
  7. 7.
    Fairey AS, Kassouf W, Estey E et al (2013) Comparison of oncological outcomes for open and laparoscopic radical nephroureterectomy: results from the Canadian Upper Tract Collaboration. BJU Int 112(6):791–797. CrossRefPubMedGoogle Scholar
  8. 8.
    Zhang S, Luo Y, Wang C et al (2016) Long-term oncologic outcomes of laparoscopic nephroureterectomy versus open nephroureterectomy for upper tract urothelial carcinoma: a systematic review and meta-analysis. PeerJ 4:e2063. CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Kamihira O, Hattori R, Yamaguchi A et al (2009) Laparoscopic radical nephroureterectomy: a multicenter analysis in Japan. Eur Urol 55(6):1397–1407. CrossRefPubMedGoogle Scholar
  10. 10.
    Kim HS, Ku JH, Jeong CW et al (2016) Laparoscopic radical nephroureterectomy is associated with worse survival outcomes than open radical nephroureterectomy in patients with locally advanced upper tract urothelial carcinoma. World J Urol 34(6):859–869. CrossRefPubMedGoogle Scholar
  11. 11.
    Oya M, Kikuchi E (2015) Evidenced-based clinical practice guideline for upper tract urothelial carcinoma (summary–Japanese Urological Association, 2014 edition). Int J Urol 22(1):3–13. CrossRefPubMedGoogle Scholar
  12. 12.
    Matsuo S, Imai E, Horio M et al (2009) Revised equations for estimated GFR from serum creatinine in Japan. Am J Kidney Dis 53(6):982–992. CrossRefPubMedGoogle Scholar
  13. 13.
    Sobin LH, Gospodarowicz MK, Wittekind C, International Union against Cancer., ebrary Inc. (2009) TNM classification of malignant tumours. 7th edn. Wiley-Blackwell, Chichester, West Sussex, UK; Hoboken, NJGoogle Scholar
  14. 14.
    Messer JC, Terrell JD, Herman MP et al (2013) Multi-institutional validation of the ability of preoperative hydronephrosis to predict advanced pathologic tumor stage in upper-tract urothelial carcinoma. Urol Oncol 31(6):904–908. CrossRefPubMedGoogle Scholar
  15. 15.
    Ito Y, Kikuchi E, Tanaka N et al (2011) Preoperative hydronephrosis grade independently predicts worse pathological outcomes in patients undergoing nephroureterectomy for upper tract urothelial carcinoma. J Urol 185(5):1621–1626. CrossRefPubMedGoogle Scholar
  16. 16.
    Clavien PA, Barkun J, de Oliveira ML et al (2009) The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg 250(2):187–196. CrossRefPubMedGoogle Scholar
  17. 17.
    Galsky MD, Hahn NM, Rosenberg J et al (2011) A consensus definition of patients with metastatic urothelial carcinoma who are unfit for cisplatin-based chemotherapy. Lancet Oncol 12(3):211–214. CrossRefPubMedGoogle Scholar
  18. 18.
    Fang Z, Li L, Wang X et al (2014) Total retroperitoneal laparoscopic nephroureterectomy with bladder-cuff resection for upper urinary tract transitional cell carcinoma. J Invest Surg 27(6):354–359. CrossRefPubMedGoogle Scholar
  19. 19.
    Kubota Y, Nakaigawa N, Committee for Establishment of the Clinical Practice Guideline for the Management of Bladder C, the Japanese Urological A (2016) Essential content of evidence-based clinical practice guidelines for bladder cancer: the Japanese Urological Association 2015 update. Int J Urol 23(8):640–645. CrossRefPubMedGoogle Scholar
  20. 20.
    Kusaka A, Hatakeyama S, Hosogoe S et al (2017) Risk-stratified surveillance and cost effectiveness of follow-up after radical cystectomy in patients with muscle-invasive bladder cancer. Oncotarget. Google Scholar
  21. 21.
    Kusaka A, Hatakeyama S, Hosogoe S et al (2017) Detecting asymptomatic recurrence after radical cystectomy contributes to better prognosis in patients with muscle-invasive bladder cancer. Med Oncol 34(5):90. CrossRefPubMedGoogle Scholar
  22. 22.
    Austin PC, Stuart EA (2015) Moving towards best practice when using inverse probability of treatment weighting (IPTW) using the propensity score to estimate causal treatment effects in observational studies. Stat Med 34(28):3661–3679. CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Walton TJ, Novara G, Matsumoto K et al (2011) Oncological outcomes after laparoscopic and open radical nephroureterectomy: results from an international cohort. BJU Int 108(3):406–412. CrossRefPubMedGoogle Scholar
  24. 24.
    Hosogoe S, Hatakeyama S, Kusaka A et al (2017) Platinum-based Neoadjuvant Chemotherapy Improves Oncological Outcomes in Patients with Locally Advanced Upper Tract Urothelial Carcinoma. Eur Urol Focus. PubMedGoogle Scholar
  25. 25.
    Kubota Y, Hatakeyama S, Tanaka T et al (2017) Oncological outcomes of neoadjuvant chemotherapy in patients with locally advanced upper tract urothelial carcinoma: a multicenter study. Oncotarget. Google Scholar

Copyright information

© Japan Society of Clinical Oncology 2018

Authors and Affiliations

  • Koichi Kido
    • 1
  • Shingo Hatakeyama
    • 1
  • Naoki Fujita
    • 1
  • Hayato Yamamoto
    • 1
  • Yuki Tobisawa
    • 1
  • Tohru Yoneyama
    • 2
  • Takahiro Yoneyama
    • 1
  • Yasuhiro Hashimoto
    • 2
  • Takuya Koie
    • 1
  • Ikuya Iwabuchi
    • 3
  • Masaru Ogasawara
    • 3
  • Toshiaki Kawaguchi
    • 3
  • Chikara Ohyama
    • 1
    • 3
  1. 1.Department of UrologyHirosaki University Graduate School of MedicineHirosakiJapan
  2. 2.Department of Advanced Transplant and Regenerative MedicineHirosaki University Graduate School of MedicineHirosakiJapan
  3. 3.Department of UrologyAomori Prefectural Central HospitalAomoriJapan

Personalised recommendations