Histologic grading of urothelial carcinoma: A reappraisal

Human Pathology

Volumn 43, Issue 12, 2012, Pages 2097-2108

  Cheng, Liang ^a   MacLennan, Gregory T ^b   Lopez Beltran, Antonio ^c  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CÓRDOBA   (Spain)

Author keywords

Biomarkers; Differential diagnosis; Histologic grading; Molecular genetics; Papillary urothelial neoplasm of low malignant potential (PUNLMP); Urinary bladder; World Health Organization (WHO) International Society of Urological Pathology (ISUP) classification

Indexed keywords

CANCER CLASSIFICATION; CANCER GRADING; HISTOPATHOLOGY; HUMAN; REVIEW; TRANSITIONAL CELL CARCINOMA; WORLD HEALTH ORGANIZATION;

EID: 84869492821     PISSN: 00468177     EISSN: 15328392     Source Type: Journal    
DOI: 10.1016/j.humpath.2012.01.008     Document Type: Article

References (85)

1. F.K. Mostofi, L.H. Sobin, and H. Torloni Histological typing of urinary bladder tumours. Vol. 10 1973 World Health Organization Geneva International Histological Classification of Tumors
2. J.I. Epstein, M.B. Amin, V.R. Reuter, and F.K. Mostofi The World Health Organization/International Society of Urological Pathology consensus classification of urothelial (transitional cell) neoplasms of the urinary bladder. Bladder Consensus Conference Committee Am J Surg Pathol 22 1998 1435 1448
3. F.K. Mostofi, C.J. Davis, and I.A. Sesterhenn WHO histologic typing of urinary bladder tumors 1999 Springer Berlin
4. J.N. Eble, G. Sauter, J.I. Epstein, and I.A. Sesterhenn World Health Organization classification of tumours: pathology and genetics of tumours of the urinary system and male genital organs 2004 IARC Press Lyon
5. R. Montironi, A. Lopez-Beltran, R. Mazzucchelli, and D.G. Bostwick Classification and grading of the non-invasive urothelial neoplasms: recent advances and controversies J Clin Pathol 56 2003 91 95
6. G.T. MacLennan, Z. Kirkali, and L. Cheng Histologic grading of noninvasive papillary urothelial neoplasms Eur Urol 51 2007 889 898
7. T.D. Jones, and L. Cheng Papillary urothelial neoplasm of low malignant potential: evolving terminology and concepts J Urol 175 2006 1995 2003
8. D.G. Bostwick, and G. Mikuz Urothelial papillary (exophytic) neoplasms Virchows Arch 441 2002 109 116
9. A. Lopez-Beltran, and R. Montironi Non-invasive urothelial neoplasms: according to the most recent WHO classification Eur Urol 46 2004 170 176
10. R. Montironi, A. Lopez-Beltran, M. Scarpelli, R. Mazzucchelli, and L. Cheng 2004 World Health Organization classification of the noninvasive urothelial neoplasms: inherent problems and clinical reflections Eur Urol Suppl 8 2009 453 457
11. D.G. Bostwick, D. Ramnani, and L. Cheng Diagnosis and grading of bladder cancer and associated lesions Urol Clin North Am 26 1999 493 507
12. R. Montironi, A. Lopez-Beltran, M. Scarpelli, R. Mazzucchelli, and L. Cheng Morphological classification and definition of benign, preneoplastic and non-invasive neoplastic lesions of the urinary bladder Histopathology 53 2008 621 633
13. R. Montironi, R. Mazzucchelli, M. Scarpelli, A. Lopez-Beltran, and L. Cheng Morphological diagnosis of urothelial neoplasms J Clin Pathol 61 2008 3 10
14. A. Pich, L. Chiusa, and A. Formiconi Proliferative activity is the most significant predictor of recurrence in noninvasive papillary urothelial neoplasms of low malignant potential and grade 1 papillary carcinomas of the bladder Cancer 95 2002 784 790
15. J.S.R. Oosterhuis, M.L. Janssen-Heijnen, R.P. Pauwels, D.W. Newling, and F. ten Kate Histological grading of papillary urothelial carcinoma of the bladder: prognostic value of the 1998 WHO/ISUP classification system and comparison with conventional grading systems J Clin Pathol 55 2002 900 905
16. A. Pich, L. Chiusa, A. Formiconi, D. Galliano, P. Bortolin, and R. Navone Biologic differences between noninvasive papillary urothelial neoplasms of low malignant potential and low-grade (grade 1) papillary carcinomas of the bladder Am J Surg Pathol 25 2001 1528 1533
17. S. Holmang, H. Hedelin, C. Anderstrom, E. Holmberg, C. Busch, and S.L. Johansson Recurrence and progression in low grade papillary urothelial tumors J Urol 162 1999 702 707
18. Y. Fujii, S. Kawakami, F. Koga, T. Nemoto, and K. Kihara Long-term outcome of bladder papillary urothelial neoplasms of low malignant potential BJU Int 92 2003 559 562
19. L. Cheng, G.T. MacLennan, S. Zhang, M. Wang, C.X. Pan, and M.O. Koch Laser capture microdissection analysis reveals frequent allelic losses in papillary urothelial neoplasm of low malignant potential of the urinary bladder Cancer 101 2004 183 188
20. T.R. Coblentz, S.E. Mills, and D. Theodorescu Impact of second opinion pathology in the definitive management of patients with bladder carcinoma Cancer 91 2001 1284 1290
21. G. Mikuz The reliability and reproducibility of the different classifications of bladder cancer S. Haupmann, M. Dietel, M. Sorbrinho-Simoes, Surgical pathology update 2001 2001 ABW-Wissenschaftsverlag Berlin 114 115
22. W. Otto, S. Denzinger, and H.M. Fritsche The WHO classification of 1973 is more suitable than the WHO classification of 2004 for predicting survival in pT1 urothelial bladder cancer BJU Int 107 2010 404 408
23. L. Cheng, and D.G. Bostwick World Health Organization and International Society of Urological Pathology classification and two-number grading system of bladder tumors: reply Cancer 88 2000 1513 1516
24. R.J. Sylvester, A.P. van der Meijden, and W. Oosterlinck Predicting recurrence and progression in individual patients with stage Ta T1 bladder cancer using EORTC risk tables: a combined analysis of 2596 patients from seven EORTC trials Eur Urol 49 2006 466 477 [discussion 475-7]
25. B.W. van Rhijn, M. Burger, and Y. Lotan Recurrence and progression of disease in non-muscle-invasive bladder cancer: from epidemiology to treatment strategy Eur Urol 56 2009 430 442
26. K. Yorukoglu, B. Tuna, and E. Dikicioglu Reproducibility of the 1998 World Health Organization/International Society of Urologic Pathology classification of papillary urothelial neoplasms of the urinary bladder Virchows Arch 443 2003 734 740
27. A.R. Schned, A.S. Andrew, C.J. Marsit, M.S. Zens, K.T. Kelsey, and M.R. Karagas Survival following the diagnosis of noninvasive bladder cancer: WHO/International Society of Urological Pathology versus WHO classification systems J Urol 178 2007 1196 1200
28. W.M. Murphy, K. Takezawa, and N.A. Maruniak Interobserver discrepancy using the 1998 World Health Organization/International Society of Urologic Pathology classification of urothelial neoplasms: practical choices for patient care J Urol 168 2002 968 972
29. M.G. Bol, J.P. Baak, and S. Buhr-Wildhagen Reproducibility and prognostic variability of grade and lamina propria invasion in stages Ta, T1 urothelial carcinoma of the bladder J Urol 169 2003 1291 1294
30. R. Engers Reproducibility and reliability of tumor grading in urological neoplasms World J Urol 25 2007 595 605
31. M. May, S. Brookman-Amissah, and J. Roigas Prognostic accuracy of individual uropathologists in noninvasive urinary bladder carcinoma: a multicentre study comparing the 1973 and 2004 World Health Organisation classifications Eur Urol 57 2010 850 858
32. B.W. van Rhijn, G.J. van Leenders, and B.C. Ooms The pathologist's mean grade is constant and individualizes the prognostic value of bladder cancer grading Eur Urol 57 2010 1052 1057
33. I.I. Gonul, A. Poyraz, C. Unsal, C. Acar, and T. Alkibay Comparison of 1998 WHO/ISUP and 1973 WHO classifications for interobserver variability in grading of papillary urothelial neoplasms of the bladder. Pathological evaluation of 258 cases Urol Int 78 2007 338 344
34. L. Cheng, A. Lopez-Beltran, G.T. MacLennan, R. Montironi, and D.G. Bostwick Neoplasms of the urinary bladder D.G. Bostwick, L. Cheng, Urologic surgical pathology. 2nd ed. 2008 Elsevier/Mosby Philadelphia 259 352
35. L. Cheng, R. Montironi, D.D. Davidson, and A. Lopez-Beltran Staging and reporting of urothelial carcinoma of the urinary bladder Mod Pathol 22 Suppl2 2009 S70 S95
36. T. Hofmann, R. Knuchel-Clarke, and A. Hartmann Clinical implications of the 2004 WHO histological classification on non-invasive tumours of the urinary bladder EAU-EBU Update Series 4 2006 83 95
37. L. Cheng, M. Darson, and J.C. Cheville Urothelial papilloma of the bladder. Clinical and biologic implications Cancer 86 1999 2098 2101
38. P.U. Malmstrom, C. Bush, and B.J. Norlen Recurrence, progression, and survival in bladder cancer. A retrospective analysis of 232 patients with greater than or equal to 5-year follow-up Scand J Urol Nephrol 21 1987 185 195
39. G.R. Prout, B.A. Barton, P.P. Griffin, and G.H. Friedell Treated history of noninvasive grade 1 transitional cell carcinoma. The National Bladder Cancer Group J Urol 148 1992 1413 1419
40. S. Holmang, H. Hedelin, C. Anderstrom, and S.L. Johansson The relationship among multiple recurrences, progression and prognosis of patients with stages Ta and T1 transitional cell cancer of the bladder followed for at least 20 years J Urol 153 1995 1823 1827
41. H.R. England, A.M.I. Paris, and J.P. Blandy The correlation of T1 bladder tumour history with prognosis and follow-up requirements Br J Urol 53 1981 593 597
42. B. Leblanc, A.J. Duclos, and F. Benard Long-term followup of initial Ta grade 1 transitional cell carcinoma of the bladder J Urol 162 1999 1946 1960
43. R.D. Pocock, B.A.J. Ponder, J.P. O'Sullivan, S.K. Ibrahim, D.F. Easton, and R.J. Shearer Prognostic factors in non-infiltrating carcinoma of the bladder: a preliminary report Br J Urol 54 1982 711 715
44. H.A. Gilbert, J.L. Logan, and A.R. Kagan The natural history of papillary transitional cell carcinoma of the bladder and its treatment in any unselected population on the basis of histologic grading J Urol 119 1978 488 492
45. N.M. Heney, S. Ahmed, and M.J. Flanagan Superficial bladder cancer: progression and recurrence J Urol 130 1983 1083 1086
46. J.M. Fitzpatrick, A.B. West, M.R. Butler, V. Lane, and J.D. O'Flynn Superficial bladder tumors (stage pTa, grades 1 and 2): the importance of recurrence pattern following initial resection J Urol 135 1986 920 922
47. G.R. Prout, B. Bassil, and P. Griffin The treated histories of patients with Ta grade 1 transitional-cell carcinoma of the bladder Arch Surg 121 1986 1463 1468
48. G.P. Hemstreet III, S. Rollins, and P. Jones Identification of a high risk subgroup of grade 1 transitional cell carcinoma using image analysis based deoxyribonucleic acid ploidy analysis of tumor tissue J Urol 146 1991 1525 1529
49. G.R. Mufti, J.S. Virdi, and M. Singh 'Solitary' Ta-T1 G1 bladder tumour - history and long-term prognosis Eur Urol 18 1990 101 106
50. A.M. Jordan, J. Weingarten, and W.M. Murphy Transitional cell neoplasms of the urinary bladder. Can biologic potential be predicted from histologic grading Cancer 60 1987 2766 2774
51. J.M. Fitzpatrick Superficial bladder carcinoma World J Urol 11 1993 142 147
52. L. Greene, K. Hanash, and G. Farrow Benign papilloma or papillary carcinoma of the bladder J Urol 110 1973 205 207
53. D.G. Bostwick Natural history of early bladder cancer J Cell Biochem 161 suppl 1992 31 38
54. R.P.E. Pauwels, R.F.M. Schapers, A.W.G.B. Smeets, F.M.J. Debruyne, and J.P.M. Geraedts Grading in superficial bladder cancer: morphological criteria Br J Urol 61 1988 129 134
55. R.F. Schapers, R.P. Pauwels, and J.T. Wijnen A simplified grading method of transitional cell carcinoma of the urinary bladder: reproducibility, clinical significance and comparison with other prognostic parameters Br J Urol 73 1994 625 631
56. B. Carbin, P. Ekman, H. Gustafson, N.J. Christensen, B. Sandstedt, and C. Silfversward Grading of human urothelial carcinoma based on nuclear atypia and mitotic frequency. I. Histological description J Urol 145 1991 968 971
57. P.K. Lipponen, M.J. Eskelinen, J. Kiviranta, and E. Pesonen Prognosis of transitional cell bladder cancer: a multivariate prognostic score for improved prediction J Urol 146 1991 1535 1540
58. D.G. Bostwick, and A. Lopez-Beltran Bladder biopsy interpretation 1999 United Pathologists Press Washington DC
59. A. Alsheikh, Z. Mohamedali, E. Jones, J. Masterson, and C.B. Gilks Comparison of the WHO/ISUP classification and cytokeratin 20 expression in predicting the behavior of low-grade papillary urothelial tumors. World Health Organization/International Society of Urologic Pathology Mod Pathol 14 2001 267 272
60. K.J. Alvarez, A. Lopez-Beltran, and C.F. Anglada Clinico-pathologic differences between bladder neoplasm with low malignant potential and low-grade carcinoma Actas Urol Esp 25 2001 645 650
61. R. Montironi, and A. Lopez-Beltran The 2004 WHO classification of bladder tumors: a summary and commentary Int J Surg Pathol 13 2005 143 153
62. L. Cheng, R.M. Neumann, and D.G. Bostwick Papillary urothelial neoplasms of low malignant potential. Clinical and biologic implications Cancer 86 1999 2102 2108
63. C.C. Pan, Y.H. Chang, K.K. Chen, H.J. Yu, C.H. Sun, and D.M. Ho Prognostic significance of the 2004 WHO/ISUP classification for prediction of recurrence, progression, and cancer-specific mortality of non-muscle-invasive urothelial tumors of the urinary bladder: a clinicopathologic study of 1,515 cases Am J Clin Pathol 133 2010 788 795
64. H. Samaratunga, D.V. Makarov, and J.I. Epstein Comparison of WHO/ISUP and WHO classification of noninvasive papillary urothelial neoplasms for risk of progression Urology 60 2002 315 319
65. S. Holmang, P. Andius, H. Hedelin, K. Wester, C. Busch, and S.L. Johansson Stage progression in Ta papillary urothelial tumors: relationship to grade, immunohistochemical expression of tumor markers, mitotic frequency and DNA ploidy J Urol 165 2001 1124 1130
66. T.K. Lee, A. Chaux, and S. Karram Papillary urothelial neoplasm of low malignant potential of the urinary bladder: clinicopathologic and outcome analysis from a single academic center Hum Pathol 42 2011 1799 1803
67. R. Oyasu World Health Organization and International Society of Urological Pathology classification and two-number grading system of bladder tumors Cancer 88 2000 1509 1512
68. L. Cheng, R.M. Neumann, and A.L. Weaver Grading and staging of bladder carcinoma in transurethral resection specimens. Correlation with 105 matched cystectomy specimens Am J Clin Pathol 113 2000 275 279
69. H.W. Herr, S.M. Donat, and V.E. Reuter Management of low grade papillary bladder tumors J Urol 178 2007 1201 1205
70. H. Miyamoto, F. Brimo, and L. Schultz Low-grade papillary urothelial carcinoma of the urinary bladder: a clinicopathologic analysis of a post-World Health Organization/International Society of Urological Pathology classification cohort from a single academic center Arch Pathol Lab Med 134 2010 1160 1163
71. F. Pellucchi, M. Freschi, and B. Ibrahim Clinical reliability of the 2004 WHO histological classification system compared with the 1973 WHO system for Ta primary bladder tumors J Urol 186 2011 2194 2199
72. T. Habuchi, O. Ogawa, and Y. Kakehi Accumulated allelic losses in the development of invasive urothelial cancer Int J Cancer 53 1993 5093 5095
73. A. Chaux, S. Karram, and J.S. Miller High-grade papillary urothelial carcinoma of the urinary tract: a clinicopathologic analysis of a post-World Health Organization/International Society of Urological Pathology classification cohort from a single academic center Hum Pathol 43 2012 115 120
74. R.E. Whisnant, S.I. Bastacky, and N.P. Ohori Cytologic diagnosis of low-grade papillary urothelial neoplasms (low malignant potential and low-grade carcinoma) in the context of the 1998 WHO/ISUP classification Diagn Cytopathol 28 2003 186 190
75. S. Bircan, O. Candir, and T.A. Serel Comparison of WHO 1973, WHO/ISUP 1998, WHO 1999 grade and combined scoring systems in evaluation of bladder carcinoma Urol Int 73 2004 201 208
76. H. Yin, and A.S. Leong Histologic grading of noninvasive papillary urothelial tumors: validation of the 1998 WHO/ISUP system by immunophenotyping and follow-up Am J Clin Pathol 121 2004 679 687
77. J.L. Curry, and E.M. Wojcik The effects of the current World Health Organization/International Society of Urologic Pathologists bladder neoplasm classification system on urine cytology results Cancer 96 2002 140 145
78. D. Ramos, S. Navarro, R. Villamon, M. Gil-Salom, and A. Llombart-Bosch Cytokeratin expression patterns in low-grade papillary urothelial neoplasms of the urinary bladder Cancer 97 2003 1876 1883
79. M. Burger, S. Denzinger, W.F. Wieland, C.G. Stief, A. Hartmann, and D. Zaak Does the current World Health Organization classification predict the outcome better in patients with noninvasive bladder cancer of early or regular onset? BJU Int 102 2008 194 197
80. P. Campbell, R.J. Conrad, C.M. Campbell, D.L. Nicol, and P. MacTaggart Papillary urothelial neoplasm of low malignant potential: reliability of diagnosis and outcome BJU Int 93 2004 1228 1231
81. S. Desai, S.D. Lim, and R.E. Jimenez Relationship of cytokeratin 20 and CD44 protein expression with WHO/ISUP grade in pTa and pT1 papillary urothelial neoplasia Mod Pathol 13 2000 1315 1323
82. L. Cheng, R.M. Neumann, A. Nehra, B.E. Spotts, A.L. Weaver, and D.G. Bostwick Cancer heterogeneity and its biologic implications in the grading of urothelial carcinoma Cancer 88 2000 1663 1670
83. J.N. Eble, and R.H. Young Benign and low grade papillary lesions of the urinary bladder: a review of the papilloma-papillary carcinoma controversy and a report of five typical papillomas Sem Diagn Pathol 6 1989 351 371
84. M. Burger, M.N. van der Aa, and J.M. van Oers Prediction of progression of non-muscle-invasive bladder cancer by WHO 1973 and 2004 grading and by FGFR3 mutation status: a prospective study Eur Urol 54 2008 835 843
85. L. Cheng, S. Zhang, G.T. MacLennan, S.R. Williamson, A. Lopez-Beltran, and R. Montironi Bladder cancer: translating molecular genetic insights into clinical practice Hum Pathol 42 2011 455 481