{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T15:57:18Z","timestamp":1792079838152,"version":"4.4.0"},"reference-count":50,"publisher":"Wiley","license":[{"start":{"date-parts":[[2026,8,10]],"date-time":"2026-08-10T00:00:00Z","timestamp":1786320000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,8,10]],"date-time":"2026-08-10T00:00:00Z","timestamp":1786320000000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Histopathology"],"abstract":"<jats:sec>\n                    <jats:title>Objective<\/jats:title>\n                    <jats:p>Histological grading is a key predictor of progression in non\u2010muscle\u2010invasive bladder cancer (NMIBC). The WHO 1973 three\u2010tier system is limited by heterogeneity within the G2 category, whereas the WHO 2004\/2016 binary classification reduces prognostic resolution by grouping biologically diverse tumours into broad low\u2010grade (LG) and high\u2010grade (HG) categories. We aimed to evaluate the prognostic performance of hybrid grading systems compared with WHO 2004\/2016, while further characterizing the histomorphological continuum of non\u2010invasive papillary urothelial carcinoma.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>\n                      Non\u2010invasive papillary urothelial carcinomas (2012\u20132023;\n                      <jats:italic>n<\/jats:italic>\n                      \u2009=\u2009472) were reviewed and reclassified by two urological pathologists according to WHO 2004\/2016, hybrid three\u2010tier and four\u2010tier systems, and an investigational five\u2010tier framework (Grades I, IIA, IIB, IIIA, IIIB) integrating architectural, cytological and proliferative features. Primary endpoints were recurrence, grade progression and T1+ stage progression, assessed using ROC analysis, Cox proportional hazards regression and model\u2010performance metrics (AIC, BIC, C\u2010index).\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      Increasing morphological atypia was associated with larger tumour size, greater multifocality and progressively higher progression risk, with events concentrated in Grades IIIA and IIIB. All systems showed limited recurrence discrimination (C\u2010index 0.54\u20130.56). For T1+ progression, discrimination improved with increasing stratification (AUC 0.754 for WHO 2004\/2016 vs. 0.815, 0.828 and 0.827 for the hybrid three\u2010tier, four\u2010tier and five\u2010tier systems, respectively; all\n                      <jats:italic>P<\/jats:italic>\n                      \u2009&lt;\u20090.001). The Hybrid 3\u2010Tier model achieved the most favourable AIC and BIC, while the five\u2010tier model yielded the highest C\u2010index (0.818).\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>Hybrid grading systems improve progression\u2010risk stratification in non\u2010invasive papillary urothelial carcinoma compared with WHO 2004\/2016, with most benefit achieved by the Hybrid 3\u2010Tier framework. These findings support the concept of a histomorphological continuum of progression risk and favour continued refinement of biologically informed hybrid grading for NMIBC risk stratification.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1111\/his.70260","type":"journal-article","created":{"date-parts":[[2026,8,10]],"date-time":"2026-08-10T08:05:15Z","timestamp":1786349115000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Hybrid grading systems improve progression risk stratification in non\u2010invasive papillary urothelial carcinoma and support a histomorphological continuum of disease progression"],"prefix":"10.1111","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1653-4942","authenticated-orcid":false,"given":"Jane K","family":"Nguyen","sequence":"first","affiliation":[{"name":"Robert J. Tomsich Pathology and Laboratory Medicine Institute Cleveland Clinic  Cleveland Ohio USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marcello P","family":"Toscano","sequence":"additional","affiliation":[{"name":"Robert J. Tomsich Pathology and Laboratory Medicine Institute Cleveland Clinic  Cleveland Ohio USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jianbo","family":"Li","sequence":"additional","affiliation":[{"name":"Department of Quantitative Health Sciences Cleveland Clinic  Cleveland Ohio USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3898-1460","authenticated-orcid":false,"given":"Sean R","family":"Williamson","sequence":"additional","affiliation":[{"name":"Robert J. Tomsich Pathology and Laboratory Medicine Institute Cleveland Clinic  Cleveland Ohio USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9426-7272","authenticated-orcid":false,"given":"Christopher G","family":"Przybycin","sequence":"additional","affiliation":[{"name":"Robert J. Tomsich Pathology and Laboratory Medicine Institute Cleveland Clinic  Cleveland Ohio USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6609-2567","authenticated-orcid":false,"given":"Chia\u2010Sui","family":"Kao","sequence":"additional","affiliation":[{"name":"Robert J. Tomsich Pathology and Laboratory Medicine Institute Cleveland Clinic  Cleveland Ohio USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3130-5475","authenticated-orcid":false,"given":"Jonathan L","family":"Myles","sequence":"additional","affiliation":[{"name":"Robert J. Tomsich Pathology and Laboratory Medicine Institute Cleveland Clinic  Cleveland Ohio USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9553-0105","authenticated-orcid":false,"given":"Krist\u00fdna","family":"Pivovar\u010d\u00edkov\u00e1","sequence":"additional","affiliation":[{"name":"Sikl's Department of Pathology, Medical Faculty in Pilsen Charles University  Pilsen Czech Republic"},{"name":"Bioptical Laboratory  Pilsen Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8052-4741","authenticated-orcid":false,"given":"Mari\u00e1n","family":"\u0160vajdler","sequence":"additional","affiliation":[{"name":"Sikl's Department of Pathology, Medical Faculty in Pilsen Charles University  Pilsen Czech Republic"},{"name":"Bioptical Laboratory  Pilsen Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marek","family":"Brousil","sequence":"additional","affiliation":[{"name":"Sikl's Department of Pathology, Medical Faculty in Pilsen Charles University  Pilsen Czech Republic"},{"name":"Bioptical Laboratory  Pilsen Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2947-179X","authenticated-orcid":false,"given":"Mohamed","family":"Eltemamy","sequence":"additional","affiliation":[{"name":"Glickman Urological and Kidney Institute Cleveland Clinic  Cleveland Ohio USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7129-6230","authenticated-orcid":false,"given":"Laura","family":"Bukavina","sequence":"additional","affiliation":[{"name":"Glickman Urological and Kidney Institute Cleveland Clinic  Cleveland Ohio USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Venkatesh","family":"Krishnamurthi","sequence":"additional","affiliation":[{"name":"Glickman Urological and Kidney Institute Cleveland Clinic  Cleveland Ohio USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9381-959X","authenticated-orcid":false,"given":"Christopher","family":"Weight","sequence":"additional","affiliation":[{"name":"Glickman Urological and Kidney Institute Cleveland Clinic  Cleveland Ohio USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rebecca A","family":"Campbell","sequence":"additional","affiliation":[{"name":"Glickman Urological and Kidney Institute Cleveland Clinic  Cleveland Ohio USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nima","family":"Almassi","sequence":"additional","affiliation":[{"name":"Glickman Urological and Kidney Institute Cleveland Clinic  Cleveland Ohio USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6708-5032","authenticated-orcid":false,"given":"Reza","family":"Alaghehbandan","sequence":"additional","affiliation":[{"name":"Robert J. Tomsich Pathology and Laboratory Medicine Institute Cleveland Clinic  Cleveland Ohio USA"},{"name":"Glickman Urological and Kidney Institute Cleveland Clinic  Cleveland Ohio USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,8,10]]},"reference":[{"key":"e_1_2_11_2_1","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1016\/j.euo.2020.12.002","article-title":"Prognostic value of the WHO1973 and WHO2004\/2016 classification Systems for Grade in primary Ta\/T1 non\u2010muscle\u2010invasive bladder cancer: A multicenter European Association of Urology non\u2010muscle\u2010invasive bladder cancer guidelines panel study","volume":"4","author":"Rhijn BWG","year":"2021","journal-title":"Eur. Urol. 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