Diagnostic Histopathology
Volume 15, Issue 1 , Pages 42-50 , January 2009

Prognostic markers in low-grade papillary urothelial neoplasms of the urinary bladder: an update

References 

  1. Landis SH, Murray T, Bolden S, Wingo PA. Cancer statistics, 1998. CA Cancer J Clin. 1998;48:6–29
  2. Shinka T, Sawada Y, Morimoto S, Fujinaga T. Clinical study on urothelial tumors of dye workers in Wakayama City. J Urol. 1991;146:1504–1507
  3. Epstein JI, Amin MB, Reuter VR, Mostofi FK, Bladder Consensus Conference Committee . The World Health Organization/International Society of Urological Pathology consensus classification of urothelial (transitional cell) neoplasms of the bladder. Am J Surg Pathol. 1998;22:1435–1448
  4. Reuter VR, Epstein JI, Amin MB, Mostofi FK, Bladder Consensus Committee . A newly illustrated synopsis of the World Health Organization/International Society of Urological Pathology (WHO/ISUP) consensus classification of urothelial (transitional cell) neoplasms of the urinary bladder. J Urol Pathol. 1999;11:1–27
  5. Mostofi FK, Sobin LH, Torloni H. Histological typing of urinary bladder tumours. International classification of tumours 19. Geneva: World Health Organization; 1973;
  6. López-Beltrán A, Montironi R. Non-invasive urothelial neoplasms: according to the most recent WHO classification. Eur Urol. 2004;46:170–176
  7. MacLennan GT, Kirkali Z, Cheng L. Histologic grading of noninvasive papillary urothelial neoplasms. Eur Urol. 2007;51:889–898
  8. Hölmang S, Hedelin H, Anderstrom C, Holmberg E, Busch C, Johansson SL. Recurrence and progression in low grade papillary urothelial tumors. J Urol. 1999;162:702–707
  9. Desai S, Lim SD, Jiménez RE, et al. Relationship of cytokeratin 20 and CD44 protein expression with WHO/ISUP grade in pTa and pT1 papillary urothelial neoplasia. Mod Pathol. 2000;13:1315–1323
  10. Alsheikh A, Mohamedali Z, Jones E, Masterson J, Gilks CB. Comparison of the WHO-ISUP classification and cytokeratin 20 expression predicting the behavior of low grade papillary urothelial tumors. Mod Pathol. 2001;14:267–272
  11. Oosterhuis JWA, Schapers RFM, Jansen-Heijnen MLG, Pauwels RPE, Newling DW, Kate F. 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. 2002;55:900–905
  12. Cheng L, Neumann RM, Bostwick DG. Papillary urothelial neoplasms of low malignant potential. Cancer. 1999;86:2102–2108
  13. Curry JL, Wojcik EM. The effects of the current World Health Organization/International Society of Urologic Pathologists bladder neoplasm classification system on urine cytology results. Cancer. 2002;96:140–145
  14. Álvarez J, López-Beltrán A, Anglada F, et al. Clinico-pathologic differences between bladder neoplasms with low malignant potential and low-grade carcinomas. Actas Urol Esp. 2001;25:645–650
  15. Busch C, Algaba F. The WHO/ISUP 1998 and WHO 1999 systems for malignancy grading of bladder cancer. Scientific foundation and translation to one another and previous systems. Virchows Arch. 2002;441:105–108
  16. Epstein JI. The new World Health Organization/International Society of Urological Pathology (WHO/ISUP) classification for TA, T1 bladder tumors: is it an improvement?. Crit Rev Oncol Hematol. 2003;47:83–89
  17. Samaratunga H, Makarov DV, Epstein JI. Comparison of WHO/ISUP and WHO classification of non-invasive papillary urothelial neoplasms for risk of progression. Urology. 2002;60:315–319
  18. Bircan S, Candir O, Serel TA. Comparison of WHO 1973, WHO/ISUP 1998, WHO 1999 grade and combined scoring systems in evaluation of bladder carcinoma. Urol Int. 2004;73:201–208
  19. Bostwick DG, Mikuz G. Urothelial papillary (exophitic) neoplasms. Virchows Arch. 2002;441:109–116
  20. Cheng L, Neumann RM, Nehra A, Spotts BE, Weaver AL, Bostwick DG. Cancer heterogeneity and its biologic implications in the grading of urothelial carcinoma. Cancer. 2000;88:1663–1670
  21. Yin H, Leong ASY. Histologic grading of noninvasive papillary urothelial tumors. Am J Clin Pathol. 2004;121:679–687
  22. Ramos D, Ruiz A, Morell L, et al. Prognostic value of morphometry in low-grade papillary urothelial bladder neoplasms. Analyt Quant Cytol Histol. 2004;26:285–294
  23. Prout GR, Barton BA, Griffin PP, Friedeel GH, National Bladder Cancer Group . Treated history of non-invasive grade 1 transitional cell carcinoma. J Urol. 1992;148:1413–1419
  24. Reading J, Hall R, Parmar MKB. The application of a prognostic factor analysis for Ta, T1 bladder cancer in routine urological practice. Br J Urol. 1995;75:604–607
  25. Busch C. Subjective and objective contexture based malignancy grading of bladder cancer. 13th Congress of Academic and Environmental Pathology, Nice, France, October 1998.
  26. Montironi R, Scarpelli M, Ansuini G, Pisani E, del Fiasco S, Mariuzzi GM. Quantitative evaluation of the progressive nuclear abnormalities in urothelial papillary lesions. Appl Pathol. 1986;4:65–73
  27. Ooms ECM, Kurver PHJ, Veldhuizen RW, Alons CL, Boon ME. Morphometric grading of bladder tumors in comparison with histologic grading by pathologists. Hum Pathol. 1983;14:144–150
  28. Lipponen PK, Eskelinen MJ, Kiviranta J, Pesonen E. Prognosis of transitional cell bladder cancer: a multivariate prognostic score for improved prediction. J Urol. 1991;146:1535–1540
  29. Blomjous ECM, Smeulders AWM, Baak JPA, Vos W, van Galen CM, Meijer CJ. A comparative study in morphometric grading of transitional cell carcinoma of the urinary bladder. Analyt Quant Cytol Histol. 1989;11:426–432
  30. Bol MG, Baak JP, van Diermen B, et al. Proliferation markers and DNA content analysis in urinary bladder TAT1 urothelial cell carcinomas: identification of subgroups with low and high grade progression risks. J Clin Pathol. 2003;56:447–452
  31. Hemstreet GP, Rollins S, Jones P, et al. Identification of a high risk subgroup of grade 1 transitional cell carcinoma using image analysis based DNA ploidy analysis of tumor tissue. J Urol. 1991;146:1525–1529
  32. Goulandris N, Karakitsos P, Georgoulakis J, Bellos CH, Deliveliotis CH, Legaki S. Deoxyribonucleic acid measurements in transitional cell carcinomas: comparison of flow and image cytometry techniques. J Urol. 1996;156:958–960
  33. Liukkonen TJO, Rajala P, Raitanen M, Rintala E, Kaasinen E, Lipponen P, et al. Prognostic value of MIB-1 score, p53, EGFr, mitotic index and papillary status in primary superficial (stage pTa/T1) bladder cancer: a prospective comparative study. Eur Urol. 1999;36:393–400
  34. Lipponen PK, Eskelinen MJ, Jauhrainen K, Terho R, Nordling S. Proliferation indices as independent prognostic factors in papillary Ta-T1 transitional cell bladder tumours. Br J Urol. 1993;72:451–457
  35. Pfister C, Lacombe L, Vezina MC, et al. Prognostic value of the proliferative index determined by Ki-67 immunostaining in superficial bladder tumors. Hum Pathol. 1999;30:1350–1355
  36. Wu TT, Chen JH, Lee YH, Huang JK. The role of bcl-2, p53, and Ki-67 index in predicting tumor recurrence for the low-grade superficial transitional bladder carcinomas. J Urol. 2000;163:758–760
  37. Krüger S, Müller H. Correlation of morphometry, nucleolar organizer regions, proliferating cell nuclear antigen and Ki-67 antigen expression with grading and staging in urinary bladder carcinomas. Br J Urol. 1995;75:480–484
  38. Fontana D, Bellina M, Gubetta L, et al. Monoclonal antibody Ki-67 in the study of the proliferative activity of bladder carcinoma. J Urol. 1992;148:1149–1151
  39. Okamura K, Miyake K, Koshikawa T, Asai J. Growth fractions of transitional cell carcinomas of the bladder defined by the monoclonal antibody Ki-67. J Urol. 1990;144:875–878
  40. Pfister C, Buzelin F, Casse C, Bochereau G, Buzelin G, Bouchot O. Comparative analysis of MIB1 and p53 expression in human bladder tumors and their correlation with cancer progression. Eur Urol. 1998;33:278–284
  41. Pfister C, Moore L, Allard P, et al. Predictive value of cell cycle markers p53, MDM2, p21, and Ki-67 in superficial bladder tumor recurrence. Clin Cancer Res. 1999;5:4079–4084
  42. Koren R, Kugel V, Dekel Y, Weissman Y, Livne PM, Gal R. Human DNA topoisomerase-IIalpha expression as a prognostic factor for transitional cell carcinoma of the urinary bladder. BJU Int. 2003;91:489–492
  43. López-Guerrero JA, Pellín A, Noguera R, Carda C, Llombart-Bosch A. Molecular analysis of the 9p21 locus and p53 genes in Ewing family tumors. Lab Invest. 2001;81:803–814
  44. Cordón-Cardo C, Dalbagni D, Sáez GT. TP53 mutations in human bladder cancer: genotypic versus phenotypic patterns. Int J Cancer. 1994;56:347–353
  45. Dalbalgni G, Sáez GT, Oliva MR, et al. p53 mutations in bladder cancer: correlation between immunohistochemistry, single strands conformation polymorphism and sequencing. Congress of the AAU. J Urol. 1992;98:238a
  46. Sarkis AS, Bajorin DF, Reyter VE, et al. Prognostic value of p53 nuclear overexpression in patients with invasive bladder cancer treated with neoadjuvant MVAC. J Clin Oncol. 1995;13:1684–1690
  47. Sarkis AS, Dalbagni G, Cordón-Cardo C, et al. Nuclear overexpression of p53 protein in transitional cell bladder carcinoma: a marker for disease progression. J Natl Cancer Inst. 1993;85:53–59
  48. Soini Y, Turpeenniemi-Hujanen T, Kamel D, et al. p53 Immunohistochemistry in transitional cell carcinoma and dysplasia of the urinary bladder correlates with disease progression. Br J Cancer. 1993;68:1029–1035
  49. Lacombe L, Dalbagni G, Zhang ZF, et al. Overexpression of p53 protein in a high-risk population of patients with superficial bladder cancer before and after BCG therapy: correlation to clinical outcome. J Clin Oncol. 1996;14:2646–2652
  50. Serth J, Kuczyk MA, Bokemeyer C, et al. p53 immunohistochemistry as an independent prognostic factor for superficial transitional cell carcinoma of the bladder. Br J Cancer. 1995;71:201–205
  51. Casetta G, Gontero P, Russo R, Pachioni D, Tizzani A. p53 expression compared with other prognostic factors in OMS grade-I stage-Ta transitional cell carcinoma of the bladder. Eur Urol. 1997;2:229–236
  52. Toktas G, Turkeri LN, Unluer LN, et al. Prognostic significance of p53 protein accumulation in stage pT1 transitional cell carcinoma of the bladder. Int Urol Nephrol. 1999;31:437–441
  53. Ramos D, Navarro S, Villamón R, Gil-Salóm M, Llombart-Bosch A. Comparative study of p53, bcl-2 and c-erbB-2 expression in low-grade papillary neoplasms of the bladder. Arch Esp Urol. 2003;56:277–285
  54. Shariat SF, Tokunaga H, Zhou J, et al. P53, p21 pRB, and p16 expression predict clinical outcome in cystectomy with bladder cancer. J Clin Oncol. 2004;22:1014–1024
  55. Lacoste-Collin L, Gomez-Brouchet A, Escourrou G, Delisle MB, Levad T, Uro-Coste E. Expression of p27(KIP1) in bladder cancers: immunohistochemical study and prognostic value in a series of 95 cases. Cancer Lett. 2002;186:115–120
  56. Sgambato A, Migaldi M, Faraglia B, et al. Cyclin D1 expression in papillary superficial bladder cancer: its association with other cell cycle-associated proteins, cell proliferation and clinical outcome. Int J Cancer. 2002;97:671–678
  57. Kamai T, Takagi K, Asami H, Ito Y, Oshima H, Yoshida KI. Decreasing of p27(KIP1) and cyclin E protein levels is associated with progression from superficial into invasive bladder cancer. Br J Cancer. 2001;84:1242–1251
  58. Korkopoulou P, Christodoulou P, Konstatinidou AE, Thomas-Tsagl E, Kapralos P, Davaris P. Cell cycle regulators in bladder cancer: a multivariate survival study with emphasis on p27KIP1. Hum Pathol. 2000;31:751–760
  59. Korkopoulou P, Konstatinidou AE, Thomas-Tsagl E, Christodoulou P, Kapralos P, Davaris P. WAF1/p21 protein expression is an independent prognostic indicator in superficial and invasive bladder cancer. Appl Immunohistochem Mol Morphol. 2000;8:285–292
  60. Santos LL, Amaro T, Pereira SA, et al. Expression of cell-cycle regulatory proteins and their prognostic value in superficial low-grade urothelial carcinoma of the bladder. Eur J Surg Oncol. 2003;29:74–80
  61. Shariat SF, Ashfaq R, Sagalowsky AI, Lotan Y. Predictive value of cell cycle biomarkers in nonmuscle invasive bladder transitional cell carcinoma. J Urol. 2007;177:481–487
  62. Kirsh EJ, Baunoch DA, Stadler WM. Expression of bcl-2 and bcl-x in bladder cancer. J Urol. 1998;159:1348–1353
  63. Lipponen PK, Aaltomaa S, Eskelinen M. Expression of the apoptosis suppressing bcl-2 protein in transitional cell bladder tumours. Histopathology. 1996;28:135–140
  64. Tzai TS, Chow NH, Lin JS, Yang WH, Tong YC. The expression of p53 and bcl-2 in superficial bladder transitional cell carcinoma and its role in the outcome of postoperative intravesical chemotherapy. Anticancer Res. 1998;18:4717–4721
  65. Vollmer RT, Humphrey PA, Swanson PE, Wick MR, Hudson ML. Invasion of the bladder by transitional cell carcinoma: its relation to histologic grade and expression of p53, MIB-1, c-erb B-2, epidermal growth factor receptor, and bcl-2. Cancer. 1998;82:715–723
  66. Karam JA, Lotan Y, Karakiewicz PI, et al. Use of combined apoptosis biomarkers for prediction of bladder cancer recurrence and mortality after radical cystectomy. Lancet Oncol. 2007;8:128–136
  67. McCann A, Dervan PA, Johnston PA, Gullick WJ, Desmond NC. C-erbB-2 oncoprotein expression in primary human tumors. Cancer. 1990;65:88–92
  68. Moriyama M, Akiyama T, Yamamoto T, et al. Expression of c-erbB-2 gene product in urinary bladder cancer. J Urol. 1991;145:423–427
  69. Koyuncuoglu M, Kargi A, Cingöz S, Kirkali Z. Investigation of p53, c-erbB-2, PCNA immunoreactivity, DNA content, AgNOR, and apoptosis in bladder carcinoma as prognostic parameters. Cancer Lett. 1998;126:143–148
  70. Neal DE, Marsh C, Bennett MK, et al. Epidermal-growth-factor receptors in human bladder cancer: comparison of invasive and superficial tumors. Lancet. 1985;1:366–368
  71. Southgate J, Harnden P, Trejdosiewicz LK. Cytokeratin expression patterns in normal and malignant urothelium: a review of the biological and diagnostic implications. Histol Histopathol. 1999;14:657–664
  72. Harnden P, Allam A, Joyce AD, Patel A, Selby P, Southgate J. Cytokeratin 20 expression by non-invasive transitional cell carcinomas: potential for distinguishing recurrent from non-recurrent disease. Histopathology. 1995;27:169–174
  73. Harnden P, Mahmood N, Southgate J. Expression of cytokeratin 20 redefines urothelial papillomas of the bladder. Lancet. 1999;353:974–977
  74. Helpap B, Köllermann J. Assessment of basal cell status and proliferative patterns in flat and papillary urothelial lesions: a contribution to the new WHO classification of urothelial tumors of the urinary bladder. Hum Pathol. 2000;31:745–750
  75. Ramos D, Navarro S, Villamón R, Gil-Salóm M, Llombart-Bosch A. Cytokeratin expression patterns in low-grade papillary urothelial neoplasms of the urinary bladder. Cancer. 2003;97:1876–1883
  76. Bhatia A, Dey P, Kumar Y, et al. Expression of cytokeratin 20 in urine cytology smears: a potential marker for the detection of urothelial carcinoma. Cytopathology. 2007;18:84–86
  77. Hartmann A, Rösner U, Schlake G, et al. Clonality and genetic divergence in multifocal low-grade superficial urothelial carcinoma as determined by chromosome 9 and p53 deletion analysis. Lab Invest. 2000;80:709–718
  78. Díaz-Cano SJ, Blanes A, Rubio J, Matilla A, Wolfe HJ. Molecular evolution and intratumor heterogeneity by topographic compartments in muscle-invasive transitional cell carcinoma of the urinary bladder. Lab Invest. 2000;80:279–289
  79. Baithun SI, Naase M, Blanes A, Díaz-Cano J. Molecular and kinetic features of transitional cell carcinomas of the bladder: biological and clinical implications. Virchows Arch. 2001;438:289–297
  80. Knowles MA. What we could do now: molecular pathology of bladder cancer. Mol Pathol. 2001;54:215–221
  81. Knowles MA. Molecular subtypes of bladder cancer: Jekyll and Hyde or chalk and cheese?. Carcinogenesis. 2006;27:361–373
  82. Blanes A, Rubio J, García I, Sanchez-Carrillo JJ, Matilla A, Díaz-Cano SJ. Genetic changes of cell cycle regulators define topographic compartments in muscle-invasive transitional cell carcinoma of the urinary bladder (abstract). J Pathol. 1999;187:12
  83. Niehans GA, Kratzke RA, Froberg MK, Aeppli DM, Nguten PL, Geradts J. G1 checkpoint protein and p53 abnormalities occur in most invasive transitional cell carcinomas of the urinary bladder. Br J Cancer. 1999;80:1175–1184

PII: S1756-2317(08)00206-5

doi: 10.1016/j.mpdhp.2008.11.002

Diagnostic Histopathology
Volume 15, Issue 1 , Pages 42-50 , January 2009

Article Tools

* Image Usage & Resolution