A contemporary update on pathology standards for bladder cancer: Transurethral resection and radical cystectomy specimens

European Urology

Volumn 63, Issue 2, 2013, Pages 321-332

  Hansel, Donna E ^a   Amin, Mahul B ^b   Comperat, Eva ^c   Cote, Richard J ^d   Knüchel, Ruth ^e   Montironi, Rodolfo ^f   Reuter, Victor E ^g   Soloway, Mark S ^d   Umar, Saleem A ^d   Van Der Kwast, Theodorus H ^h  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CEDARS SINAI MEDICAL CENTER   (United States)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^d UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^e RWTH AACHEN UNIVERSITY   (Germany)

^f United Hospitals   (Italy)

^g Memorial Sloan Kettering ^*  (United States)

^h UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Bladder cancer; Pathology; Review; Standards

Indexed keywords

ANTINEOPLASTIC AGENT; SMOOTHELIN;

ADJUVANT THERAPY; ANGIOLYMPHATIC INVASION; AUSTRIA; BLADDER BIOPSY; BLADDER CANCER; BLADDER EPITHELIUM; BLADDER NECK; CANCER DIAGNOSIS; CANCER INVASION; CANCER PROGNOSIS; CANCER STAGING; CANCER SURGERY; CANCER SURVIVAL; CARCINOMA IN SITU; CLINICAL FEATURE; CONNECTIVE TISSUE; CYSTECTOMY; CYTOLOGY; DETRUSOR MUSCLE; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; LAMINA PROPRIA; LYMPH NODE DISSECTION; LYMPH NODE METASTASIS; LYMPH VESSEL METASTASIS; PATHOLOGIST; PATHOLOGY; PATIENT CARE; PRIORITY JOURNAL; REVIEW; SMOOTH MUSCLE CONTRACTILITY; TRANSITIONAL CELL CARCINOMA; TRANSURETHRAL RESECTION; TREATMENT OUTCOME; TUMOR VOLUME; URETHRA;

CARCINOMA, TRANSITIONAL CELL; CYSTECTOMY; HUMANS; LYMPH NODE EXCISION; NEOPLASM STAGING; REFERENCE STANDARDS; URINARY BLADDER NEOPLASMS;

EID: 84871920558     PISSN: 03022838     EISSN: 18737560     Source Type: Journal    
DOI: 10.1016/j.eururo.2012.10.008     Document Type: Review

References (92)

1. American Cancer Society Cancer facts and figures 2012 2012 American Cancer Society Atlanta, GA
2. A. Jemal, F. Bray, M.M. Center, J. Ferlay, E. Ward, and D. Forman Global cancer statistics CA Cancer J Clin 61 2011 69 90
3. J.N. Eble, G. Sauter, J.I. Epstein, and I.A. Sesterhenn Pathology and genetics of tumours of the urinary system and male genital organs 2004 IARC Press Lyon, France
4. M. Soloway, and S. Khoury Bladder cancer. ed. 2. 2nd International Consultation on Bladder Cancer - Vienna 2012 International Consultation on Urological Diseases Bristol, UK
5. A. Lopez-Beltran, F. Algaba, and D.M. Berney Handling and reporting of transurethral resection specimens of the bladder in Europe: a web-based survey by the European Network of Uropathology (ENUP) Histopathology 58 2011 579 585
6. R. Ukai, K. Hashimoto, T. Iwasa, and H. Nakayama Transurethral resection in one piece (TURBO) is an accurate tool for pathological staging of bladder tumor Int J Urol 17 2010 708 714
7. A. Naselli, C. Introini, F. Germinale, B. Spina, and P. Puppo En bloc transurethral resection of bladder lesions: a trick to retrieve specimens up to 4.5 cm BJU Int 109 2012 960 963
8. Cancer Committee, College of American Pathologists Reporting on cancer specimens: case summaries and background documentation 2010 CAP Press Northfield, IL
9. L. Cheng, R. Montironi, D.D. Davidson, and A. Lopez-Beltran Staging and reporting of urothelial carcinoma of the urinary bladder Mod Pathol 22 Suppl 2 2009 S70 S95
10. A.T. Philip, M.B. Amin, P. Tamboli, T.J. Lee, C.E. Hill, and J.Y. Ro Intravesical adipose tissue: a quantitative study of its presence and location with implications for therapy and prognosis Am J Surg Pathol 24 2000 1286 1290
11. A. Stenzl, N.C. Cowan, and M. De Santis Treatment of muscle-invasive and metastatic bladder cancer: update of the EAU guidelines Eur Urol 59 2011 1009 1018
12. J.L. Gore, M.S. Litwin, and J. Lai Urologic Diseases in America Project. Use of radical cystectomy for patients with invasive bladder cancer J Natl Cancer Inst 102 2010 802 811
13. 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 (Pubitemid 36323769)
14. B.W. van Rhijn, T.H. van der Kwast, and D.M. Kakiashvili Pathological stage review is indicated in primary pT1 bladder cancer BJU Int 106 2010 206 211
15. Pathologists of the French Association of Urology Cancer Committee Lamina propria microinvasion of bladder tumors, incidence on stage allocation (pTa vs pT1): recommended approach World J Urol 11 1993 161 164
16. A. Van Der Meijden, R. Sylvester, L. Collette, A. Bono, and F. Ten Kate The role and impact of pathology review on stage and grade assessment of stages Ta and T1 bladder tumors: a combined analysis of 5 European Organization for Research and Treatment of Cancer trials J Urol 164 2000 1533 1537
17. G.M. Farrow, D.C. Utz, and C.C. Rife Morphological and clinical observations of patients with early bladder cancer treated with total cystectomy Cancer Res 36 1976 2495 2501
18. M.B. Amin, J.A. Gomez, and R.H. Young Urothelial transitional cell carcinoma with endophytic growth patterns: a discussion of patterns of invasion and problems associated with assessment of invasion in 18 cases Am J Surg Pathol 21 1997 1057 1068 (Pubitemid 27407290)
19. A. Lopez-Beltran, and L. Cheng Stage pT1 bladder carcinoma: diagnostic criteria, pitfalls and prognostic significance Pathology 35 2003 484 491 (Pubitemid 38041283)
20. H.E. Schaafsma, F.C. Ramaekers, and G.N. van Muijen Distribution of cytokeratin polypeptides in human transitional cell carcinomas, with special emphasis on changing expression patterns during tumor progression Am J Pathol 136 1990 329 343 (Pubitemid 20074608)
21. E.F. Tamas, and J.I. Epstein Detection of residual tumor cells in bladder biopsy specimens: pitfalls in the interpretation of cytokeratin stains Am J Surg Pathol 31 2007 390 397 (Pubitemid 46673112)
22. M. Younes, J. Sussman, and L.D. True The usefulness of the level of the muscularis mucosae in the staging of invasive transitional cell carcinoma of the urinary bladder Cancer 66 1990 543 548 (Pubitemid 20233454)
23. S. Holmang, H. Hedelin, C. Anderstrom, E. Holmberg, and S.L. Johansson The importance of the depth of invasion in stage T1 bladder carcinoma: a prospective cohort study J Urol 157 1997 800 803 discussion 804
24. S. Bertz, S. Denzinger, and W. Otto Substaging by estimating the size of invasive tumour can improve risk stratification in pT1 urothelial bladder cancer-evaluation of a large hospital-based single-centre series Histopathology 59 2011 722 732
25. B.W. van Rhijn, T.H. van der Kwast, and S.S. Alkhateeb A new and highly prognostic system to discern T1 bladder cancer substage Eur Urol 61 2012 378 384
26. W.C. Chang, Y.H. Chang, and C.C. Pan Prognostic significance in substaging of T1 urinary bladder urothelial carcinoma on transurethral resection Am J Surg Pathol 36 2012 454 461
27. F.T. van der Loop, G. Schaart, E.D. Timmer, F.C. Ramaekers, and G.J. van Eys Smoothelin, a novel cytoskeletal protein specific for smooth muscle cells J Cell Biol 134 1996 401 411 (Pubitemid 26250708)
28. G.P. Paner, S.S. Shen, and S. Lapetino Diagnostic utility of antibody to smoothelin in the distinction of muscularis propria from muscularis mucosae of the urinary bladder: a potential ancillary tool in the pathologic staging of invasive urothelial carcinoma Am J Surg Pathol 33 2009 91 98
29. G.P. Paner, J.G. Brown, and S. Lapetino Diagnostic use of antibody to smoothelin in the recognition of muscularis propria in transurethral resection of urinary bladder tumor (TURBT) specimens Am J Surg Pathol 34 2010 792 799
30. D.E. Hansel, G.P. Paner, N. Nese, and M.B. Amin Limited smoothelin expression within the muscularis mucosae: validation in bladder diverticula Hum Pathol 42 2011 1770 1776
31. I.M. Bovio, S.Z. Al-Quran, C.J. Rosser, C.B. Algood, P.A. Drew, and R.W. Allan Smoothelin immunohistochemistry is a useful adjunct for assessing muscularis propria invasion in bladder carcinoma Histopathology 56 2010 951 956
32. L. Council, and O. Hameed Differential expression of immunohistochemical markers in bladder smooth muscle and myofibroblasts, and the potential utility of desmin, smoothelin, and vimentin in staging of bladder carcinoma Mod Pathol 22 2009 639 650
33. H. Miyamoto, R.B. Sharma, P.B. Illei, and J.I. Epstein Pitfalls in the use of smoothelin to identify muscularis propria invasion by urothelial carcinoma Am J Surg Pathol 34 2010 418 422
34. M.B. Amin, J.Y. Ro, and T. el-Sharkawy Micropapillary variant of transitional cell carcinoma of the urinary bladder. Histologic pattern resembling ovarian papillary serous carcinoma Am J Surg Pathol 18 1994 1224 1232 (Pubitemid 24362435)
35. E. Comperat, M. Roupret, and J. Yaxley Micropapillary urothelial carcinoma of the urinary bladder: a clinicopathological analysis of 72 cases Pathology 42 2010 650 654
36. A.M. Kamat, C.P. Dinney, and J.R. Gee Micropapillary bladder cancer: a review of the University of Texas M. D. Anderson Cancer Center experience with 100 consecutive patients Cancer 110 2007 62 67 (Pubitemid 46986419)
37. A.R. Sangoi, A.H. Beck, and M.B. Amin Interobserver reproducibility in the diagnosis of invasive micropapillary carcinoma of the urinary tract among urologic pathologists Am J Surg Pathol 34 2010 1367 1376
38. H. Samaratunga, and K. Khoo Micropapillary variant of urothelial carcinoma of the urinary bladder; a clinicopathological and immunohistochemical study Histopathology 45 2004 55 64 (Pubitemid 38969562)
39. J.B. Stern Unusual benign bladder tumor of Brunn nest origin Urology 14 1979 288 289 (Pubitemid 9257154)
40. M.L. Talbert, and R.H. Young Carcinomas of the urinary bladder with deceptively benign-appearing foci. A report of three cases Am J Surg Pathol 13 1989 374 381 (Pubitemid 19134067)
41. M.J. Wasco, S. Daignault, D. Bradley, and R.B. Shah Nested variant of urothelial carcinoma: a clinicopathologic and immunohistochemical study of 30 pure and mixed cases Hum Pathol 41 2010 163 171
42. R. Cox, and J.I. Epstein Large nested variant of urothelial carcinoma: 23 cases mimicking von Brunn nests and inverted growth pattern of noninvasive papillary urothelial carcinoma Am J Surg Pathol 35 2011 1337 1342
43. Y. Lotan, A. Gupta, and S.F. Shariat Lymphovascular invasion is independently associated with overall survival, cause-specific survival, and local and distant recurrence in patients with negative lymph nodes at radical cystectomy J Clin Oncol 23 2005 6533 6539 (Pubitemid 46190245)
44. M.J. Resnick, M. Bergey, L. Magerfleisch, J.E. Tomaszewski, S.B. Malkowicz, and T.J. Guzzo Longitudinal evaluation of the concordance and prognostic value of lymphovascular invasion in transurethral resection and radical cystectomy specimens BJU Int 107 2011 46 52
45. M.P. Larsen, G.D. Steinberg, C.B. Brendler, and J.I. Epstein Use of Ulex europaeus agglutinin I (UEAI) to distinguish vascular and " pseudovascular" invasion in transitional cell carcinoma of bladder with lamina propria invasion Mod Pathol 3 1990 83 88
46. L.P. Kunju, L. You, Y. Zhang, S. Daignault, J.E. Montie, and C.T. Lee Lymphovascular invasion of urothelial cancer in matched transurethral bladder tumor resection and radical cystectomy specimens J Urol 180 2008 1928 1932 discussion 1932
47. V.E. Reuter Lymphovascular invasion as an independent predictor of recurrence and survival in node-negative bladder cancer remains to be proven J Clin Oncol 23 2005 6450 6451 (Pubitemid 46190233)
48. S.B. Edge, C.C. Compton, A.G. Fritz, F.L. Greene, and A. Trotti III AJCC cancer staging handbook ed. 7. 2010 Springer New York, NY
49. G.S. Palapattu, S.F. Shariat, P.I. Karakiewicz Bladder Cancer Research Consortium Cancer specific outcomes in patients with pT0 disease following radical cystectomy J Urol 175 2006 1645 1649 discussion 1649
50. W. Kassouf, P.E. Spiess, and G.A. Brown P0 stage at radical cystectomy for bladder cancer is associated with improved outcome independent of traditional clinical risk factors Eur Urol 52 2007 769 776 (Pubitemid 47126162)
51. D. Tilki, R.S. Svatek, and G. Novara Stage pT0 at radical cystectomy confers improved survival: an international study of 4,430 patients J Urol 184 2010 888 894
52. M. Roupret, S.J. Drouin, and S. Larre Bladder Cancer Committee of the French National Association of Urology ("CC-AFU Vessie"). Oncologic outcomes and survival in pT0 tumors after radical cystectomy in patients without neoadjuvant chemotherapy: results from a large multicentre collaborative study Ann Surg Oncol 18 2011 3833 3838
53. M. Babjuk, W. Oosterlinck, R. Sylvester European Association of Urology (EAU) EAU guidelines on non-muscle-invasive urothelial carcinoma of the bladder, the 2011 update Eur Urol 59 2011 997 1008
54. H.M. Fritsche, M. Burger, and W. Dietmaier Multicolor FISH (UroVysion) facilitates follow-up of patients with high-grade urothelial carcinoma of the bladder Am J Clin Pathol 134 2010 597 603
55. R. Rosenblatt, A. Sherif, E. Rintala Nordic Urothelial Cancer Group Pathologic downstaging is a surrogate marker for efficacy and increased survival following neoadjuvant chemotherapy and radical cystectomy for muscle-invasive urothelial bladder cancer Eur Urol 61 2012 1229 1238
56. G. Griffiths, R. Hall, R. Sylvester, D. Raghavan, and M.K. Parmar International phase III trial assessing neoadjuvant cisplatin, methotrexate, and vinblastine chemotherapy for muscle-invasive bladder cancer: long-term results of the BA06 30894 trial J Clin Oncol 29 2011 2171 2177
57. J.A. Martinez-Pineiro, M. Gonzalez Martin, and F. Arocena Neoadjuvant cisplatin chemotherapy before radical cystectomy in invasive transitional cell carcinoma of the bladder: a prospective randomized phase III study J Urol 153 1995 964 973
58. P. Sagaster, J. Flamm, and M. Flamm Neoadjuvant chemotherapy (MVAC) in locally invasive bladder cancer Eur J Cancer 32A 1996 1320 1324 (Pubitemid 26246704)
59. T. Granfors, R. Tomic, and B. Ljungberg Downstaging and survival benefits of neoadjuvant radiotherapy before cystectomy for patients with invasive bladder carcinoma Scand J Urol Nephrol 43 2009 293 299
60. H.B. Grossman, R.B. Natale, and C.M. Tangen Neoadjuvant chemotherapy plus cystectomy compared with cystectomy alone for locally advanced bladder cancer N Engl J Med 349 2003 859 866 (Pubitemid 37025405)
61. S.M. Donat, E.M. Genega, H.W. Herr, and V.E. Reuter Mechanisms of prostatic stromal invasion in patients with bladder cancer: clinical significance J Urol 165 2001 1117 1120 (Pubitemid 32210215)
62. D. Esrig, J.A. Freeman, and D.A. Elmajian Transitional cell carcinoma involving the prostate with a proposed staging classification for stromal invasion J Urol 156 1996 1071 1076 (Pubitemid 26269831)
63. F. Pagano, P. Bassi, and G.L. Ferrante Is stage pT4a (D1) reliable in assessing transitional cell carcinoma involvement of the prostate in patients with a concurrent bladder cancer? A necessary distinction for contiguous or noncontiguous involvement J Urol 155 1996 244 247 (Pubitemid 126426473)
64. R. Mazzucchelli, F. Barbisan, and A. Santinelli Prediction of prostatic involvement by urothelial carcinoma in radical cystoprostatectomy for bladder cancer Urology 74 2009 385 390
65. K.L. Watts, B.T. Ristau, H.T. Yamase, and J.A. Taylor 3rd. Prognostic implications of lymph node involvement in bladder cancer: are we understaging using current methods? BJU Int 108 2011 484 492
66. I.G. Jeong, J.Y. Ro, and S.C. Kim Extranodal extension in node-positive bladder cancer: the continuing controversy BJU Int 108 2011 38 43
67. R. Seiler, M. von Gunten, G.N. Thalmann, and A. Fleischmann Extracapsular extension but not the tumour burden of lymph node metastases is an independent adverse risk factor in lymph node-positive bladder cancer Histopathology 58 2011 571 578
68. A.J. Stephenson, M.C. Gong, S.C. Campbell, A.F. Fergany, and D.E. Hansel Aggregate lymph node metastasis diameter and survival after radical cystectomy for invasive bladder cancer Urology 75 2010 382 386
69. J.B. Jensen, B.P. Ulhoi, and K.M. Jensen Size and volume of metastatic and non-metastatic lymph nodes in pelvis and lower abdomen in patients with carcinoma of the bladder undergoing radical cystectomy Scand J Urol Nephrol 44 2010 291 297
70. H.W. Herr, and S.M. Donat Outcome of patients with grossly node positive bladder cancer after pelvic lymph node dissection and radical cystectomy J Urol 165 2001 62 64 discussion 64
71. J. Leissner, M.A. Ghoneim, and H. Abol-Enein Extended radical lymphadenectomy in patients with urothelial bladder cancer: results of a prospective multicenter study J Urol 171 2004 139 144 (Pubitemid 37549109)
72. I.G. Jeong, D. You, and J.W. Kim Outcomes of single lymph node positive urothelial carcinoma after radical cystectomy J Urol 185 2011 2085 2090
73. J.P. Stein, J. Cai, S. Groshen, and D.G. Skinner Risk factors for patients with pelvic lymph node metastases following radical cystectomy with en bloc pelvic lymphadenectomy: concept of lymph node density J Urol 170 2003 35 41 (Pubitemid 36734405)
74. W. Kassouf, P.K. Agarwal, and H.W. Herr Lymph node density is superior to TNM nodal status in predicting disease-specific survival after radical cystectomy for bladder cancer: analysis of pooled data from MDACC and MSKCC J Clin Oncol 26 2008 121 126
75. Simone G, Papalia R, Ferriero M, et al. Development and external validation of lymph node density cut-off points in prospective series of radical cystectomy and pelvic lymph node dissection. Int J Urol. In press. http://dx.doi.org/10.1111/j.1442-2042.2012.03103.x.
76. V. Parkash, C. Bifulco, R. Feinn, J. Concato, and D. Jain To count and how to count, that is the question: interobserver and intraobserver variability among pathologists in lymph node counting Am J Clin Pathol 134 2010 42 49
77. B.H. Bochner, H.W. Herr, and V.E. Reuter Impact of separate versus en bloc pelvic lymph node dissection on the number of lymph nodes retrieved in cystectomy specimens J Urol 166 2001 2295 2296 (Pubitemid 33065278)
78. J.P. Stein, D.F. Penson, and J. Cai Radical cystectomy with extended lymphadenectomy: evaluating separate package versus en bloc submission for node positive bladder cancer J Urol 177 2007 876 881
79. J. Gordetsky, E. Scosyrev, and H. Rashid Identifying additional lymph nodes in radical cystectomy lymphadenectomy specimens Mod Pathol 25 2012 140 144
80. J.B. Jensen, S. Hoyer, and K.M. Jensen Incidence of occult lymph-node metastasis missed by standard pathological examination in patients with bladder cancer undergoing radical cystectomy Scand J Urol Nephrol 45 2011 419 424
81. Fajkovic H, Cha EK, Jeldres C, et al. Extranodal extension is a powerful prognostic factor in bladder cancer patients with lymph node metastasis. Eur Urol. In press. http://dx.doi.org/10.1016/j.eururo.2012.07.026.
82. R. Knuchel, and K. Lindemann-Docter Urine-based tumour diagnostics for bladder cancer: effects of the new histopathological classification - food for thought [in German] Urologe A 48 2009 598 608
83. L. Bubendorf, P. Dalquen, and S. Savic Cytology of the urinary tract: Between uncertainty and clarity [article in German] Pathologe 30 Suppl 2 2009 173 178
84. F. Strittmatter, A. Buchner, and A. Karl Individual learning curve reduces the clinical value of urinary cytology Clin Genitourin Cancer 9 2011 22 26
85. A. Karl, S. Tritschler, and P. Stanislaus Positive urine cytology but negative white-light cystoscopy: an indication for fluorescence cystoscopy? BJU Int 103 2009 484 487
86. G. Gakis, S. Kruck, and A. Stenzl Can the burden of follow-up in low-grade noninvasive bladder cancer be reduced by photodynamic diagnosis, perioperative instillations, imaging, and urine markers? Curr Opin Urol 20 2010 388 392
87. S. Tritschler, M.L. Sommer, and J. Straub Urinary cytology in era of fluorescence endoscopy: redefining the role of an established method with a new reference standard Urology 76 2010 677 680
88. S. Sadek, M.S. Soloway, S. Hook, and F. Civantos The value of upper tract cytology after transurethral resection of bladder tumor in patients with transitional cell cancer J Urol 161 1999 77 79
89. A.S. Brems-Eskildsen, K. Zieger, and H. Toldbod Prediction and diagnosis of bladder cancer recurrence based on urinary content of hTERT, SENP1, PPP1CA, and MCM5 transcripts BMC Cancer 10 2010 646
90. D. Tilki, M. Burger, and G. Dalbagni Urine markers for detection and surveillance of non-muscle-invasive bladder cancer Eur Urol 60 2011 484 492
91. R. Montironi, L. Cheng, and A. Lopez-Beltran Joint appraisal of the radical prostatectomy specimen by the urologist and the uropathologist: together, we can do it better Eur Urol 56 2009 951 955
92. K.T. Adiyat, D. Katkoori, C.T. Soloway, R. De los Santos, M. Manoharan, and M.S. Soloway Complete transurethral resection of bladder tumor": are the guidelines being followed? Urology 75 2010 365 367