Papillary urothelial neoplasm of low malignant potential (PUN-LMP): Still a meaningful histo-pathological grade category for Ta, noninvasive bladder tumors in 2019?

Anouk E. Hentschel; Bas W. G. van Rhijn; Johannes Bründl; Eva M. Compérat; Karin Plass; Oscar Rodríguez; Jose D. Subiela Henríquez; Virginia Hernández; Enrique de la Peña; Isabel Alemany; Diana Turturica; Francesca Pisano; Francesco Soria; Otakar Čapoun; Lenka Bauerová; Michael Pešl; H. Max Bruins; Willemien Runneboom; Sonja Herdegen; Johannes Breyer; Antonin Brisuda; Andrea Scavarda-Lamberti; Ana Calatrava; José Rubio-Briones; Maximilian Seles; Sebastian Mannweiler; Judith Bosschieter; Venkata R. M. Kusuma; David Ashabere; Nicolai Huebner; Juliette Cotte; Laura S. Mertens; Daniel Cohen; Luca Lunelli; Olivier Cussenot; Soha El Sheikh; Dimitrios Volanis; Jean-François Coté; Morgan Rouprêt; Andrea Haitel; Shahrokh F. Shariat; A. Hugh Mostafid; Jakko A. Nieuwenhuijzen; Richard Zigeuner; Jose L. Dominguez-Escrig; Jaromir Hacek; Alexandre R. Zlotta; Maximilian Burger; Matthias Evert; Christina A. Hulsbergen-van de Kaa; Antoine G. van der Heijden; Lambertus A. L. M. Kiemeney; Viktor Soukup; Luca Molinaro; Paolo Gontero; Carlos Llorente; Ferran Algaba; Joan Palou; James N'Dow; Marko Babjuk; Theo H. van der Kwast; Richard J. Sylvester

doi:https://doi.org/10.1016/j.urolonc.2019.10.002

Papillary urothelial neoplasm of low malignant potential (PUN-LMP): Still a meaningful histo-pathological grade category for Ta, noninvasive bladder tumors in 2019?

Anouk E. Hentschel, Bas W. G. van Rhijn, Johannes Bründl, Eva M. Compérat, Karin Plass, Oscar Rodríguez, Jose D. Subiela Henríquez, Virginia Hernández, Enrique de la Peña, Isabel Alemany, Diana Turturica, Francesca Pisano, Francesco Soria, Otakar Čapoun, Lenka Bauerová, Michael Pešl, H. Max Bruins, Willemien Runneboom, Sonja Herdegen, Johannes BreyerAntonin Brisuda, Andrea Scavarda-Lamberti, Ana Calatrava, José Rubio-Briones, Maximilian Seles, Sebastian Mannweiler, Judith Bosschieter, Venkata R. M. Kusuma, David Ashabere, Nicolai Huebner, Juliette Cotte, Laura S. Mertens, Daniel Cohen, Luca Lunelli, Olivier Cussenot, Soha El Sheikh, Dimitrios Volanis, Jean-François Coté, Morgan Rouprêt, Andrea Haitel, Shahrokh F. Shariat, A. Hugh Mostafid, Jakko A. Nieuwenhuijzen, Richard Zigeuner, Jose L. Dominguez-Escrig, Jaromir Hacek, Alexandre R. Zlotta, Maximilian Burger, Matthias Evert, Christina A. Hulsbergen-van de Kaa, Antoine G. van der Heijden, Lambertus A. L. M. Kiemeney, Viktor Soukup, Luca Molinaro, Paolo Gontero, Carlos Llorente, Ferran Algaba, Joan Palou, James N'Dow, Marko Babjuk, Theo H. van der Kwast, Richard J. Sylvester

Research output: Contribution to journal › Article › Academic › peer-review

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Abstract

Background: Papillary urothelial neoplasm of low malignant potential (PUN-LMP) was introduced as a noninvasive, noncancerous lesion and a separate grade category in 1998. Subsequently, PUN-LMP was reconfirmed by World Health Organization (WHO) 2004 and WHO 2016 classifications for urothelial bladder tumors. Objectives: To analyze the proportion of PUN-LMP diagnosis over time and to determine its prognostic value compared to Ta-LG (low-grade) and Ta-HG (high-grade) carcinomas. To assess the intraobserver variability of an experienced uropathologist assigning (WHO) 2004/2016 grades at 2 time points. Materials and methods: Individual patient data of 3,311 primary Ta bladder tumors from 17 hospitals in Europe and Canada were available. Transurethral resection of the tumor was performed between 1990 and 2018. Time to recurrence and progression were analyzed with cumulative incidence functions, log-rank tests and multivariable Cox-regression stratified by institution. Intraobserver variability was assessed by examining the same 314 transurethral resection of the tumorslides twice, in 2004 and again in 2018. Results: PUN-LMP represented 3.8% (127/3,311) of Ta tumors. The same pathologist found 71/314 (22.6%) PUN-LMPs in 2004 and only 20/314 (6.4%) in 2018. Overall, the proportion of PUN-LMP diagnosis substantially decreased over time from 31.3% (1990–2000) to 3.2% (2000–2010) and to 1.1% (2010–2018). We found no difference in time to recurrence between the three WHO 2004/2016 Ta-grade categories (log-rank, P = 0.381), nor for LG vs. PUN-LMP (log-rank, P = 0.238). Time to progression was different for all grade categories (log-rank, P < 0.001), but not between LG and PUN-LMP (log-rank, P = 0.096). Multivariable analyses on recurrence and progression showed similar results for all 3 grade categories and for LG vs. PUN-LMP. Conclusions: The proportion of PUN-LMP has decreased to very low levels in the last decade. Contrary to its reconfirmation in the WHO 2016 classification, our results do not support the continued use of PUN-LMP as a separate grade category in Ta tumors because of the similar prognosis for PUN-LMP and Ta-LG carcinomas.

Original language	English
Article number	doi: 10.1016/j.urolonc.2019.10.002
Pages (from-to)	440-448
Number of pages	9
Journal	Urologic Oncology
Volume	38
Issue number	5
Early online date	5 Nov 2019
DOIs	https://doi.org/10.1016/j.urolonc.2019.10.002
Publication status	Published - 1 May 2020

Keywords

Bladder
Cancer
Carcinomas
Grade
Nonmuscle-invasive
Urothelial
WHO

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Hentschel, A. E., van Rhijn, B. W. G., Bründl, J., Compérat, E. M., Plass, K., Rodríguez, O., Henríquez, J. D. S., Hernández, V., de la Peña, E., Alemany, I., Turturica, D., Pisano, F., Soria, F., Čapoun, O., Bauerová, L., Pešl, M., Bruins, H. M., Runneboom, W., Herdegen, S., ... Sylvester, R. J. (2020). Papillary urothelial neoplasm of low malignant potential (PUN-LMP): Still a meaningful histo-pathological grade category for Ta, noninvasive bladder tumors in 2019? Urologic Oncology, 38(5), 440-448. Article doi: 10.1016/j.urolonc.2019.10.002. https://doi.org/10.1016/j.urolonc.2019.10.002

@article{74ad7efb36644d90b8c426063694260e,

title = "Papillary urothelial neoplasm of low malignant potential (PUN-LMP): Still a meaningful histo-pathological grade category for Ta, noninvasive bladder tumors in 2019?",

abstract = "Background: Papillary urothelial neoplasm of low malignant potential (PUN-LMP) was introduced as a noninvasive, noncancerous lesion and a separate grade category in 1998. Subsequently, PUN-LMP was reconfirmed by World Health Organization (WHO) 2004 and WHO 2016 classifications for urothelial bladder tumors. Objectives: To analyze the proportion of PUN-LMP diagnosis over time and to determine its prognostic value compared to Ta-LG (low-grade) and Ta-HG (high-grade) carcinomas. To assess the intraobserver variability of an experienced uropathologist assigning (WHO) 2004/2016 grades at 2 time points. Materials and methods: Individual patient data of 3,311 primary Ta bladder tumors from 17 hospitals in Europe and Canada were available. Transurethral resection of the tumor was performed between 1990 and 2018. Time to recurrence and progression were analyzed with cumulative incidence functions, log-rank tests and multivariable Cox-regression stratified by institution. Intraobserver variability was assessed by examining the same 314 transurethral resection of the tumorslides twice, in 2004 and again in 2018. Results: PUN-LMP represented 3.8% (127/3,311) of Ta tumors. The same pathologist found 71/314 (22.6%) PUN-LMPs in 2004 and only 20/314 (6.4%) in 2018. Overall, the proportion of PUN-LMP diagnosis substantially decreased over time from 31.3% (1990–2000) to 3.2% (2000–2010) and to 1.1% (2010–2018). We found no difference in time to recurrence between the three WHO 2004/2016 Ta-grade categories (log-rank, P = 0.381), nor for LG vs. PUN-LMP (log-rank, P = 0.238). Time to progression was different for all grade categories (log-rank, P < 0.001), but not between LG and PUN-LMP (log-rank, P = 0.096). Multivariable analyses on recurrence and progression showed similar results for all 3 grade categories and for LG vs. PUN-LMP. Conclusions: The proportion of PUN-LMP has decreased to very low levels in the last decade. Contrary to its reconfirmation in the WHO 2016 classification, our results do not support the continued use of PUN-LMP as a separate grade category in Ta tumors because of the similar prognosis for PUN-LMP and Ta-LG carcinomas.",

keywords = "Bladder, Cancer, Carcinomas, Grade, Nonmuscle-invasive, Urothelial, WHO",

author = "Hentschel, {Anouk E.} and {van Rhijn}, {Bas W. G.} and Johannes Br{\"u}ndl and Comp{\'e}rat, {Eva M.} and Karin Plass and Oscar Rodr{\'i}guez and Henr{\'i}quez, {Jose D. Subiela} and Virginia Hern{\'a}ndez and {de la Pe{\~n}a}, Enrique and Isabel Alemany and Diana Turturica and Francesca Pisano and Francesco Soria and Otakar {\v C}apoun and Lenka Bauerov{\'a} and Michael Pe{\v s}l and Bruins, {H. Max} and Willemien Runneboom and Sonja Herdegen and Johannes Breyer and Antonin Brisuda and Andrea Scavarda-Lamberti and Ana Calatrava and Jos{\'e} Rubio-Briones and Maximilian Seles and Sebastian Mannweiler and Judith Bosschieter and Kusuma, {Venkata R. M.} and David Ashabere and Nicolai Huebner and Juliette Cotte and Mertens, {Laura S.} and Daniel Cohen and Luca Lunelli and Olivier Cussenot and Sheikh, {Soha El} and Dimitrios Volanis and Jean-Fran{\c c}ois Cot{\'e} and Morgan Roupr{\^e}t and Andrea Haitel and Shariat, {Shahrokh F.} and Mostafid, {A. Hugh} and Nieuwenhuijzen, {Jakko A.} and Richard Zigeuner and Dominguez-Escrig, {Jose L.} and Jaromir Hacek and Zlotta, {Alexandre R.} and Maximilian Burger and Matthias Evert and {Hulsbergen-van de Kaa}, {Christina A.} and {van der Heijden}, {Antoine G.} and Kiemeney, {Lambertus A. L. M.} and Viktor Soukup and Luca Molinaro and Paolo Gontero and Carlos Llorente and Ferran Algaba and Joan Palou and James N'Dow and Marko Babjuk and {van der Kwast}, {Theo H.} and Sylvester, {Richard J.}",

year = "2020",

month = may,

day = "1",

doi = "https://doi.org/10.1016/j.urolonc.2019.10.002",

language = "English",

volume = "38",

pages = "440--448",

journal = "Urologic Oncology",

issn = "1078-1439",

publisher = "Elsevier Inc.",

number = "5",

}

Hentschel, AE, van Rhijn, BWG, Bründl, J, Compérat, EM, Plass, K, Rodríguez, O, Henríquez, JDS, Hernández, V, de la Peña, E, Alemany, I, Turturica, D, Pisano, F, Soria, F, Čapoun, O, Bauerová, L, Pešl, M, Bruins, HM, Runneboom, W, Herdegen, S, Breyer, J, Brisuda, A, Scavarda-Lamberti, A, Calatrava, A, Rubio-Briones, J, Seles, M, Mannweiler, S, Bosschieter, J, Kusuma, VRM, Ashabere, D, Huebner, N, Cotte, J, Mertens, LS, Cohen, D, Lunelli, L, Cussenot, O, Sheikh, SE, Volanis, D, Coté, J-F, Rouprêt, M, Haitel, A, Shariat, SF, Mostafid, AH, Nieuwenhuijzen, JA, Zigeuner, R, Dominguez-Escrig, JL, Hacek, J, Zlotta, AR, Burger, M, Evert, M, Hulsbergen-van de Kaa, CA, van der Heijden, AG, Kiemeney, LALM, Soukup, V, Molinaro, L, Gontero, P, Llorente, C, Algaba, F, Palou, J, N'Dow, J, Babjuk, M, van der Kwast, TH & Sylvester, RJ 2020, 'Papillary urothelial neoplasm of low malignant potential (PUN-LMP): Still a meaningful histo-pathological grade category for Ta, noninvasive bladder tumors in 2019?', Urologic Oncology, vol. 38, no. 5, doi: 10.1016/j.urolonc.2019.10.002, pp. 440-448. https://doi.org/10.1016/j.urolonc.2019.10.002

Papillary urothelial neoplasm of low malignant potential (PUN-LMP): Still a meaningful histo-pathological grade category for Ta, noninvasive bladder tumors in 2019? / Hentschel, Anouk E.; van Rhijn, Bas W. G.; Bründl, Johannes et al.
In: Urologic Oncology, Vol. 38, No. 5, doi: 10.1016/j.urolonc.2019.10.002, 01.05.2020, p. 440-448.

Research output: Contribution to journal › Article › Academic › peer-review

TY - JOUR

T1 - Papillary urothelial neoplasm of low malignant potential (PUN-LMP)

T2 - Still a meaningful histo-pathological grade category for Ta, noninvasive bladder tumors in 2019?

AU - Hentschel, Anouk E.

AU - van Rhijn, Bas W. G.

AU - Bründl, Johannes

AU - Compérat, Eva M.

AU - Plass, Karin

AU - Rodríguez, Oscar

AU - Henríquez, Jose D. Subiela

AU - Hernández, Virginia

AU - de la Peña, Enrique

AU - Alemany, Isabel

AU - Turturica, Diana

AU - Pisano, Francesca

AU - Soria, Francesco

AU - Čapoun, Otakar

AU - Bauerová, Lenka

AU - Pešl, Michael

AU - Bruins, H. Max

AU - Runneboom, Willemien

AU - Herdegen, Sonja

AU - Breyer, Johannes

AU - Brisuda, Antonin

AU - Scavarda-Lamberti, Andrea

AU - Calatrava, Ana

AU - Rubio-Briones, José

AU - Seles, Maximilian

AU - Mannweiler, Sebastian

AU - Bosschieter, Judith

AU - Kusuma, Venkata R. M.

AU - Ashabere, David

AU - Huebner, Nicolai

AU - Cotte, Juliette

AU - Mertens, Laura S.

AU - Cohen, Daniel

AU - Lunelli, Luca

AU - Cussenot, Olivier

AU - Sheikh, Soha El

AU - Volanis, Dimitrios

AU - Coté, Jean-François

AU - Rouprêt, Morgan

AU - Haitel, Andrea

AU - Shariat, Shahrokh F.

AU - Mostafid, A. Hugh

AU - Nieuwenhuijzen, Jakko A.

AU - Zigeuner, Richard

AU - Dominguez-Escrig, Jose L.

AU - Hacek, Jaromir

AU - Zlotta, Alexandre R.

AU - Burger, Maximilian

AU - Evert, Matthias

AU - Hulsbergen-van de Kaa, Christina A.

AU - van der Heijden, Antoine G.

AU - Kiemeney, Lambertus A. L. M.

AU - Soukup, Viktor

AU - Molinaro, Luca

AU - Gontero, Paolo

AU - Llorente, Carlos

AU - Algaba, Ferran

AU - Palou, Joan

AU - N'Dow, James

AU - Babjuk, Marko

AU - van der Kwast, Theo H.

AU - Sylvester, Richard J.

PY - 2020/5/1

Y1 - 2020/5/1

N2 - Background: Papillary urothelial neoplasm of low malignant potential (PUN-LMP) was introduced as a noninvasive, noncancerous lesion and a separate grade category in 1998. Subsequently, PUN-LMP was reconfirmed by World Health Organization (WHO) 2004 and WHO 2016 classifications for urothelial bladder tumors. Objectives: To analyze the proportion of PUN-LMP diagnosis over time and to determine its prognostic value compared to Ta-LG (low-grade) and Ta-HG (high-grade) carcinomas. To assess the intraobserver variability of an experienced uropathologist assigning (WHO) 2004/2016 grades at 2 time points. Materials and methods: Individual patient data of 3,311 primary Ta bladder tumors from 17 hospitals in Europe and Canada were available. Transurethral resection of the tumor was performed between 1990 and 2018. Time to recurrence and progression were analyzed with cumulative incidence functions, log-rank tests and multivariable Cox-regression stratified by institution. Intraobserver variability was assessed by examining the same 314 transurethral resection of the tumorslides twice, in 2004 and again in 2018. Results: PUN-LMP represented 3.8% (127/3,311) of Ta tumors. The same pathologist found 71/314 (22.6%) PUN-LMPs in 2004 and only 20/314 (6.4%) in 2018. Overall, the proportion of PUN-LMP diagnosis substantially decreased over time from 31.3% (1990–2000) to 3.2% (2000–2010) and to 1.1% (2010–2018). We found no difference in time to recurrence between the three WHO 2004/2016 Ta-grade categories (log-rank, P = 0.381), nor for LG vs. PUN-LMP (log-rank, P = 0.238). Time to progression was different for all grade categories (log-rank, P < 0.001), but not between LG and PUN-LMP (log-rank, P = 0.096). Multivariable analyses on recurrence and progression showed similar results for all 3 grade categories and for LG vs. PUN-LMP. Conclusions: The proportion of PUN-LMP has decreased to very low levels in the last decade. Contrary to its reconfirmation in the WHO 2016 classification, our results do not support the continued use of PUN-LMP as a separate grade category in Ta tumors because of the similar prognosis for PUN-LMP and Ta-LG carcinomas.

AB - Background: Papillary urothelial neoplasm of low malignant potential (PUN-LMP) was introduced as a noninvasive, noncancerous lesion and a separate grade category in 1998. Subsequently, PUN-LMP was reconfirmed by World Health Organization (WHO) 2004 and WHO 2016 classifications for urothelial bladder tumors. Objectives: To analyze the proportion of PUN-LMP diagnosis over time and to determine its prognostic value compared to Ta-LG (low-grade) and Ta-HG (high-grade) carcinomas. To assess the intraobserver variability of an experienced uropathologist assigning (WHO) 2004/2016 grades at 2 time points. Materials and methods: Individual patient data of 3,311 primary Ta bladder tumors from 17 hospitals in Europe and Canada were available. Transurethral resection of the tumor was performed between 1990 and 2018. Time to recurrence and progression were analyzed with cumulative incidence functions, log-rank tests and multivariable Cox-regression stratified by institution. Intraobserver variability was assessed by examining the same 314 transurethral resection of the tumorslides twice, in 2004 and again in 2018. Results: PUN-LMP represented 3.8% (127/3,311) of Ta tumors. The same pathologist found 71/314 (22.6%) PUN-LMPs in 2004 and only 20/314 (6.4%) in 2018. Overall, the proportion of PUN-LMP diagnosis substantially decreased over time from 31.3% (1990–2000) to 3.2% (2000–2010) and to 1.1% (2010–2018). We found no difference in time to recurrence between the three WHO 2004/2016 Ta-grade categories (log-rank, P = 0.381), nor for LG vs. PUN-LMP (log-rank, P = 0.238). Time to progression was different for all grade categories (log-rank, P < 0.001), but not between LG and PUN-LMP (log-rank, P = 0.096). Multivariable analyses on recurrence and progression showed similar results for all 3 grade categories and for LG vs. PUN-LMP. Conclusions: The proportion of PUN-LMP has decreased to very low levels in the last decade. Contrary to its reconfirmation in the WHO 2016 classification, our results do not support the continued use of PUN-LMP as a separate grade category in Ta tumors because of the similar prognosis for PUN-LMP and Ta-LG carcinomas.

KW - Bladder

KW - Cancer

KW - Carcinomas

KW - Grade

KW - Nonmuscle-invasive

KW - Urothelial

KW - WHO

UR - https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=85075511712&origin=inward

UR - https://www.ncbi.nlm.nih.gov/pubmed/31704141

UR - http://www.scopus.com/inward/record.url?scp=85075511712&partnerID=8YFLogxK

U2 - https://doi.org/10.1016/j.urolonc.2019.10.002

DO - https://doi.org/10.1016/j.urolonc.2019.10.002

M3 - Article

C2 - 31704141

SN - 1078-1439

VL - 38

SP - 440

EP - 448

JO - Urologic Oncology

JF - Urologic Oncology

IS - 5

M1 - doi: 10.1016/j.urolonc.2019.10.002

ER -

Hentschel AE, van Rhijn BWG, Bründl J, Compérat EM, Plass K, Rodríguez O et al. Papillary urothelial neoplasm of low malignant potential (PUN-LMP): Still a meaningful histo-pathological grade category for Ta, noninvasive bladder tumors in 2019? Urologic Oncology. 2020 May 1;38(5):440-448. doi: 10.1016/j.urolonc.2019.10.002. Epub 2019 Nov 5. doi: https://doi.org/10.1016/j.urolonc.2019.10.002

Papillary urothelial neoplasm of low malignant potential (PUN-LMP): Still a meaningful histo-pathological grade category for Ta, noninvasive bladder tumors in 2019?

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Keywords

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