{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,9]],"date-time":"2026-09-09T16:13:10Z","timestamp":1788970390551,"version":"build-2803163510"},"reference-count":22,"publisher":"Oxford University Press (OUP)","issue":"9","license":[{"start":{"date-parts":[[2026,5,12]],"date-time":"2026-05-12T00:00:00Z","timestamp":1778544000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,9,9]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Introduction<\/jats:title>\n                    <jats:p>Seeding and implantation are major mechanisms of intravesical recurrence (IVR) following the radical nephroureterectomy (RNU) of upper tract urothelial carcinoma (UTUC). We herein hypothesized that bladder biopsies (BB) may increase the IVR risk by promoting implantation in injured bladder mucosa.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Patients and methods<\/jats:title>\n                    <jats:p>This retrospective study included 172 patients with UTUC with no history of bladder UC who underwent RNU between January 2010 and December 2024 at two institutions. The primary endpoint was the association between BB and IVR-free survival (IVRFS) after RNU. A directed acyclic graph (DAG) was generated to identify potential confounders and guide multivariable analysis, and sensitivity analyses using propensity score matching were performed.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>Eighteen (10%) patients underwent BB prior to RNU due to a positive voided urine cytology finding and\/or the presence of erythematous mucosa. Patients receiving BB had significantly shorter IVRFS than those without BB (3-year IVRFS rate: 14% vs. 69%; P\u00a0&amp;lt;\u00a0.001). On both DAG-guided and stepwise multivariable models, BB was independently associated with an increased IVR risk (hazard ratio: 2.55 and 4.00, respectively; both P\u00a0&amp;lt;\u00a0.005). In the propensity score-matched cohort, BB was also associated with a shorter IVRFS. Notably, IVR developed at the BB sites in 60% of the cases of IVR following BB.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>BB is likely to increase the IVR risk in patients undergoing RNU for UTUC by promoting tumor cell implantation. Avoiding BB may be prudent unless both urine cytology and cystoscopic findings are highly suspicious for bladder carcinoma.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1093\/jjco\/hyag078","type":"journal-article","created":{"date-parts":[[2026,4,22]],"date-time":"2026-04-22T11:50:10Z","timestamp":1776858610000},"page":"1103-1110","source":"Crossref","is-referenced-by-count":0,"title":["Adverse impact of bladder biopsy on the rate of intravesical recurrences following radical nephroureterectomy for upper tract urothelial carcinoma"],"prefix":"10.1093","volume":"56","author":[{"given":"Tomonori","family":"Kanagawa","sequence":"first","affiliation":[{"name":"Department of Urology, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital , 3-18-22 Honkomagome, Bunkyo-ku, Tokyo 113-8677 ,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0001-2607-1013","authenticated-orcid":false,"given":"Ichiro","family":"Yonese","sequence":"additional","affiliation":[{"name":"Department of Urology, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital , 3-18-22 Honkomagome, Bunkyo-ku, Tokyo 113-8677 ,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takehiro","family":"Nakamura","sequence":"additional","affiliation":[{"name":"Department of Urology, Tokyo Metropolitan Ohtsuka Hospital , 2-8-1 Minami-Ohtsuka, Toshima-ku, Tokyo 170-8476 ,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mai","family":"Shimizu","sequence":"additional","affiliation":[{"name":"Department of Urology, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital , 3-18-22 Honkomagome, Bunkyo-ku, Tokyo 113-8677 ,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rie","family":"Tanaka","sequence":"additional","affiliation":[{"name":"Department of Urology, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital , 3-18-22 Honkomagome, Bunkyo-ku, Tokyo 113-8677 ,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hajime","family":"Kido","sequence":"additional","affiliation":[{"name":"Department of Urology, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital , 3-18-22 Honkomagome, Bunkyo-ku, Tokyo 113-8677 ,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tsukasa","family":"Shinoda","sequence":"additional","affiliation":[{"name":"Department of Urology, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital , 3-18-22 Honkomagome, Bunkyo-ku, Tokyo 113-8677 ,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ken","family":"Sekiya","sequence":"additional","affiliation":[{"name":"Department of Urology, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital , 3-18-22 Honkomagome, Bunkyo-ku, Tokyo 113-8677 ,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takahiko","family":"Soma","sequence":"additional","affiliation":[{"name":"Department of Urology, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital , 3-18-22 Honkomagome, Bunkyo-ku, Tokyo 113-8677 ,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Masahiro","family":"Toide","sequence":"additional","affiliation":[{"name":"Department of Urology, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital , 3-18-22 Honkomagome, Bunkyo-ku, Tokyo 113-8677 ,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Masaya","family":"Ito","sequence":"additional","affiliation":[{"name":"Department of Urology, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital , 3-18-22 Honkomagome, Bunkyo-ku, Tokyo 113-8677 ,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ryoji","family":"Takazawa","sequence":"additional","affiliation":[{"name":"Department of Urology, Tokyo Metropolitan Ohtsuka Hospital , 2-8-1 Minami-Ohtsuka, Toshima-ku, Tokyo 170-8476 ,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fumitaka","family":"Koga","sequence":"additional","affiliation":[{"name":"Department of Urology, Tokyo Metropolitan Cancer and Infectious Diseases Center, Komagome Hospital , 3-18-22 Honkomagome, Bunkyo-ku, Tokyo 113-8677 ,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2026,5,12]]},"reference":[{"key":"2026090910435671300_ref1","volume-title":"EAU guidelines on upper urinary tract urothelial carcinoma","author":"Gontero","year":"2023"},{"key":"2026090910435671300_ref2","doi-asserted-by":"publisher","first-page":"5629","DOI":"10.3390\/cancers14225629","article-title":"Intravesical recurrence after radical nephroureterectomy in patients with upper tract urothelial carcinoma is associated with flexible diagnostic ureteroscopy, but not with rigid diagnostic ureteroscopy","volume":"14","author":"Ha","year":"2022","journal-title":"Cancers (Basel)"},{"key":"2026090910435671300_ref3","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1111\/bju.13935","article-title":"Impact of diagnostic ureteroscopy on intravesical recurrence in patients undergoing radical nephroureterectomy for upper tract urothelial cancer: a systematic review and meta-analysis","volume":"120","author":"Marchioni","year":"2017","journal-title":"BJU Int"},{"key":"2026090910435671300_ref4","doi-asserted-by":"publisher","first-page":"1122","DOI":"10.1016\/j.eururo.2014.11.035","article-title":"A systematic review and meta-analysis of clinicopathologic factors linked to intravesical recurrence after radical nephroureterectomy to treat upper tract urothelial carcinoma","volume":"67","author":"Seisen","year":"2015","journal-title":"Eur Urol"},{"key":"2026090910435671300_ref5","doi-asserted-by":"publisher","first-page":"12975","DOI":"10.1038\/s41598-025-96267-1","article-title":"Phases of tight junction barrier disruption during transurothelial migration of invasive urothelial cancer cells","volume":"15","author":"Kuret","year":"2025","journal-title":"Sci Rep"},{"key":"2026090910435671300_ref6","doi-asserted-by":"publisher","first-page":"1087","DOI":"10.1016\/0140-6736(93)92066-3","article-title":"Metachronous multifocal development of urothelial cancers by intraluminal seeding","volume":"342","author":"Habuchi","year":"1993","journal-title":"Lancet."},{"key":"2026090910435671300_ref7","doi-asserted-by":"publisher","first-page":"981","DOI":"10.1002\/ijc.33327","article-title":"The clonal relation of primary upper urinary tract urothelial carcinoma and paired urothelial carcinoma of the bladder","volume":"148","author":"Doeveren","year":"2021","journal-title":"Int J Cancer"},{"key":"2026090910435671300_ref8","doi-asserted-by":"publisher","first-page":"184","DOI":"10.1111\/bju.14053","article-title":"Impact of ureteroscopy before radical nephroureterectomy for upper tract urothelial carcinomas on oncological outcomes: a meta-analysis","volume":"121","author":"Guo","year":"2018","journal-title":"BJU Int"},{"key":"2026090910435671300_ref9","doi-asserted-by":"publisher","first-page":"3121","DOI":"10.1245\/s10434-013-3000-z","article-title":"Diagnostic ureteroscopy independently correlates with intravesical recurrence after nephroureterectomy for upper urinary tract urothelial carcinoma","volume":"20","author":"Luo","year":"2013","journal-title":"Ann Surg Oncol"},{"key":"2026090910435671300_ref10","doi-asserted-by":"publisher","first-page":"558","DOI":"10.1097\/JU.0000000000001834","article-title":"The impact of upper tract urothelial carcinoma diagnostic modality on intravesical recurrence after radical nephroureterectomy: a single institution series and updated meta-analysis","volume":"206","author":"Sharma","year":"2021","journal-title":"J Urol"},{"key":"2026090910435671300_ref11","doi-asserted-by":"publisher","first-page":"1869","DOI":"10.1007\/s00345-023-04446-4","article-title":"Impact of diagnostic ureteral catheterization on intravesical tumour recurrence following radical nephroureterectomy for upper tract urothelial carcinoma","volume":"41","author":"Yonese","year":"2023","journal-title":"World J Urol"},{"key":"2026090910435671300_ref12","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1007\/978-4-431-54505-7_4","volume-title":"Gasless single-port RoboSurgeon surgery in urology","author":"Kihara","year":"2015"},{"key":"2026090910435671300_ref13","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1159\/000446270","article-title":"The Paris system for reporting urinary cytology: the quest to develop a standardized terminology","volume":"60","author":"Barkan","year":"2016","journal-title":"Acta Cytol"},{"key":"2026090910435671300_ref14","doi-asserted-by":"publisher","first-page":"271.e1","DOI":"10.1016\/j.clgc.2020.08.003","article-title":"Causal diagram techniques for urologic oncology research","volume":"19","author":"Shapiro","year":"2021","journal-title":"Clin Genitourin Cancer"},{"key":"2026090910435671300_ref15","doi-asserted-by":"publisher","first-page":"452","DOI":"10.1038\/bmt.2012.244","article-title":"Investigation of the freely available easy-to-use software `EZR' for medical statistics","volume":"48","author":"Kanda","year":"2013","journal-title":"Bone Marrow Transplant"},{"key":"2026090910435671300_ref16","first-page":"5835","article-title":"Clonal and chronological genetic analysis of multifocal cancers of the bladder and upper urinary tract","volume":"58","author":"Takahashi","year":"1998","journal-title":"Cancer Res"},{"key":"2026090910435671300_ref17","doi-asserted-by":"publisher","first-page":"6512","DOI":"10.1158\/1078-0432.CCR-05-0891","article-title":"Molecular evidence supporting field effect in urothelial carcinogenesis","volume":"11","author":"Jones","year":"2005","journal-title":"Clin Cancer Res"},{"key":"2026090910435671300_ref18","doi-asserted-by":"publisher","first-page":"590","DOI":"10.1016\/j.urolonc.2020.01.008","article-title":"Synchronous and metachronous urothelial carcinoma of the upper urinary tract and the bladder: are they clonally related? A systematic review","volume":"38","author":"Doeveren","year":"2020","journal-title":"Urol Oncol"},{"key":"2026090910435671300_ref19","doi-asserted-by":"publisher","first-page":"4197","DOI":"10.3390\/jcm10184197","article-title":"The impact of diagnostic ureteroscopy prior to radical nephroureterectomy on oncological outcomes in patients with upper tract urothelial carcinoma: a comprehensive systematic review and meta-analysis","volume":"10","author":"Nowak","year":"2021","journal-title":"J Clin Med"},{"key":"2026090910435671300_ref20","volume-title":"Edn. Presented at the EAU annual congress Madrid 2025","author":"European Association of Urology, ed","year":"2025"},{"key":"2026090910435671300_ref21","doi-asserted-by":"publisher","first-page":"548","DOI":"10.1097\/JU.0000000000001788","article-title":"Expression analysis of same-patient metachronous and synchronous upper tract and bladder urothelial carcinoma","volume":"206","author":"Petros","year":"2021","journal-title":"J Urol"},{"key":"2026090910435671300_ref22","doi-asserted-by":"publisher","first-page":"1422","DOI":"10.1200\/JCO.2012.45.2128","article-title":"Prospective randomized phase II trial of a single early intravesical instillation of pirarubicin (THP) in the prevention of bladder recurrence after nephroureterectomy for upper urinary tract urothelial carcinoma: the THP monotherapy study group trial","volume":"31","author":"Ito","year":"2013","journal-title":"J Clin Oncol"}],"container-title":["Japanese Journal of Clinical Oncology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jjco\/article-pdf\/56\/9\/1103\/68271109\/hyag078.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jjco\/article-pdf\/56\/9\/1103\/68271109\/hyag078.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,9]],"date-time":"2026-09-09T15:31:42Z","timestamp":1788967902000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jjco\/article\/56\/9\/1103\/8676261"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,5,12]]},"references-count":22,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2026,5,12]]},"published-print":{"date-parts":[[2026,9,9]]}},"URL":"https:\/\/doi.org\/10.1093\/jjco\/hyag078","relation":{},"ISSN":["1465-3621"],"issn-type":[{"value":"1465-3621","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2026,9]]},"published":{"date-parts":[[2026,5,12]]}}}