journal of men's health
Volume 6, Issue 4 , Pages 368-382 , December 2009

Critical review of biomarkers for the early detection and surveillance of bladder cancer

  • Daher C. Chade, MD, PhD

      Affiliations

    • Urology Service, Memorial Sloan-Kettering Cancer Center, New York, New York, USA
  • ,
  • Shahrokh F. Shariat, MD, PhD

      Affiliations

    • Division of Urology, Sidney Kimmel Center for Prostate and Urologic Cancer, Memorial Sloan-Kettering Cancer Center, York Avenue, New York, NY, USA
    • Corresponding Author InformationCorresponding author.
  • ,
  • Guilherme Godoy, MD

      Affiliations

    • Urology Service, Memorial Sloan-Kettering Cancer Center, New York, New York, USA
  • ,
  • Siegfried Meryn, MD

      Affiliations

    • Medical University of Vienna, Vienna, Austria
  • ,
  • Guido Dalbagni, MD

      Affiliations

    • Urology Service, Memorial Sloan-Kettering Cancer Center, New York, New York, USA

Received 25 June 2009 ,Accepted 27 July 2009.

References 

  1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, et al. Cancer statistics, 2008. CA Cancer J Clin. 2008;58(2):71–96
  2. Shariat SF, Karakiewicz PI, Palapattu GS, Lotan Y, Rogers CG, Amiel GE, et al. Outcomes of radical cystectomy for transitional cell carcinoma of the bladder: a contemporary series from the bladder cancer research consortium. J Urol. 2006;176(6):2414–2422
  3. Stein JP, Lieskovsky G, Cote R, Groshen S, Feng AC, Boyd S, et al. Radical cystectomy in the treatment of invasive bladder cancer: long-term results in 1,054 patients. J Clin Oncol. 2001;19(3):666–675
  4. Madersbacher S, Hochreiter W, Burkhard F, Thalmann GN, Danuser H, Markwalder R, et al. Radical cystectomy for bladder cancer today – a homogeneous series without neoadjuvant therapy. J Clin Oncol. 2003;21(4):690–696
  5. Prout GR, Barton BA, Griffin PP, Friedell GH The National Bladder Cancer Group. Treated history of noninvasive grade 1 transitional cell carcinoma. J Urol. 1992;148(5):1413–1419
  6. Pagano F, Bassi P, Galetti TP, Meneghini A, Milani C, Artibani W, et al. Results of contemporary radical cystectomy for invasive bladder cancer: a clinicopathological study with an emphasis on the inadequacy of the tumor, nodes and metastases classification. J Urol. 1991;145(1):45–50
  7. van der Poel HG, Debruyne FM. Can biological markers replace cystoscopy? An update. Curr Opin Urol. 2001;11(5):503–509
  8. Herr HW. The natural history of a T1 bladder cancer: life-long tumour diathesis. BJU Int. 1999;84(9):1102–1103
  9. Lotan Y, Roehrborn CG. Sensitivity and specificity of commonly available bladder tumor markers versus cytology: results of a comprehensive literature review and meta-analyses. Urology. 2003;61(1):109–118discussion 118
  10. Karakiewicz PI, Benayoun S, Zippe C, Ludecke G, Boman H, Sanchez-Carbayo M, et al. Institutional variability in the accuracy of urinary cytology for predicting recurrence of transitional cell carcinoma of the bladder. BJU Int. 2006;97(5):997–1001
  11. Lokeshwar V, Soloway M. Current bladder tumor tests: does their projected utility fulfill clinical necessity?. J Urol. 2001;165:1067–1077
  12. Svatek RS, Sagalowsky AI, Lotan Y. Economic impact of screening for bladder cancer using bladder tumor markers: a decision analysis. Urol Oncol. 2006;24(4):338–343
  13. Lotan Y, Svatek RS, Sagalowsky AI. Should we screen for bladder cancer in a high-risk population?: A cost per life-year saved analysis. Cancer. 2006;107(5):982–990
  14. Johnston B, Morales A, Emerson L, Lundie M. Rapid detection of bladder cancer: a comparative study of point of care tests. J Urol. 1997;158:2098–2101
  15. Kinders R, Jones T, Root R, Bruce C, Murchison H, Corey M, et al. Complement factor H or a related protein is a marker for transitional cell cancer of the bladder. Clin Cancer Res. 1998;4(10):2511–2520
  16. Wiener HG, Mian C, Haitel A, Pycha A, Schatzl G, Marberger M. Can urine bound diagnostic tests replace cystoscopy in the management of bladder cancer?. J Urol. 1998;159(6):1876–1880
  17. Takashi M, Schenck U, Kissel K, Leyh H, Treiber U. Use of diagnostic categories in urinary cytology in comparison with the bladder tumour antigen (BTA) test in bladder cancer patients. Int Urol Nephrol. 1999;31(2):189–196
  18. Sharma S, Zippe CD, Pandrangi L, Nelson D, Agarwal A. Exclusion criteria enhance the specificity and positive predictive value of NMP22 and BTA stat. J Urol. 1999;162(1):53–57
  19. Gutierrez Banos JL, Martin Garcia B, Hernandez Rodriguez R, Portillo Martin JA, Correas Gomez MA, del Valle Schaan JI, et al. Utilidad del BTA Stat Test (Bard) en el diagnóstico del cáncer vesical. Resultados preliminares y comparación con citología y cistoscopia. Arch Esp Urol. 1998;51(8):778–782
  20. Landman J, Chang Y, Kavaler E, Droller MJ, Liu BC. Sensitivity and specificity of NMP-22, telomerase, and BTA in the detection of human bladder cancer. Urology. 1998;52(3):398–402
  21. Leyh H, Mazeman E. Bard BTA test compared with voided urine cytology in the diagnosis of recurrent bladder cancer. Eur Urol. 1997;32:425–428
  22. Leyh H, Marberger M, Conort P, Sternberg C, Pansadoro V, Pagano F, et al. Comparison of the BTA stat test with voided urine cytology and bladder wash cytology in the diagnosis and monitoring of bladder cancer. Eur Urol. 1999;35(1):52–56
  23. Nasuti JF, Gomella LG, Ismial M, Bibbo M. Utility of the BTA stat test kit for bladder cancer screening. Diagn Cytopathol. 1999;21(1):27–29
  24. Oge O, Kozaci D, Gemalmaz H. The BTA stat test is nonspecific for hematuria: an experimental hematuria model. J Urol. 2002;167(3):1318–1319discussion 1319-20
  25. Raitanen MP. The role of BTA stat test in follow-up of patients with bladder cancer: results from FinnBladder studies. World J Urol. 2008;26(1):45–50
  26. Malkowicz SB. The application of human complement factor H-related protein (BTA TRAK) in monitoring patients with bladder cancer. Urol Clin of North Am. 2000;27(1):63–73
  27. Thomas L, Leyh H, Marberger M, Bombardieri E, Bassi P, Pagano F, et al. Multicenter trial of the quantitative BTA TRAK assay in the detection of bladder cancer. Clin Chem. 1999;45(4):472–477
  28. Mahnert B, Tauber S, Kriegmair M, Schmitt UM, Hasholzner U, Reiter W, et al. BTA-TRAK – a useful diagnostic tool in urinary bladder cancer?. Anticancer Res. 1999;19(4A):2615–2619
  29. Irani J, Desgrandchamps F, Millet C, Toubert ME, Bon D, Aubert J, et al. BTA stat and BTA TRAK: a comparative evaluation of urine testing for the diagnosis of transitional cell carcinoma of the bladder. Eur Urol. 1999;35(2):89–92
  30. Heicappell R, Wettig IC, Schostak M, Muller M, Steiner U, Sauter T, et al. Quantitative detection of human complement factor H-related protein in transitional cell carcinoma of the urinary bladder. Eur Urol. 1999;35(1):81–87
  31. Ellis WJ, Blumenstein BA, Ishak LM, Enfield DL The Multi Center Study Group. Clinical evaluation of the BTA TRAK assay and comparison to voided urine cytology and the Bard BTA test in patients with recurrent bladder tumors. Urology. 1997;50(6):882–887
  32. Abbate I, D’Introno A, Cardo G, Marano A, Addabbo L, Musci M, et al. Comparison of nuclear matrix protein 22 and bladder tumor antigen in urine of patients with bladder cancer. Anticancer Res. 1998;18(5B):3803–3805
  33. Babjuk M, Soukup V, Pesl M, Kostirova M, Drncova E, Smolova H, et al. Urinary cytology and quantitative BTA and UBC tests in surveillance of patients with pTapT1 bladder urothelial carcinoma. Urology. 2008;71(4):718–722
  34. Tsui KH, Chen SM, Wang TM, Juang HH, Chen CL, Sun GH, et al. Comparisons of voided urine cytology, nuclear matrix protein-22 and bladder tumor associated antigen tests for bladder cancer of geriatric male patients in Taiwan, China. Asian J Androl. 2007;9(5):711–715
  35. Fradet Y, Lockhart C. Performance characteristics of a new monoclonal antibody test for bladder cancer: ImmunoCyt trade mark. Can J Urol. 1997;4:400
  36. Greene KL, Berry A, Konety BR. Diagnostic utility of the ImmunoCyt/uCyt+ test in bladder cancer. Rev Urol. 2006;8(4):190–197
  37. Olsson H, Zackrisson B. ImmunoCyt a useful method in the follow-up protocol for patients with urinary bladder carcinoma. Scand J Urol Nephrol. 2001;35:280–282
  38. Mian C, Pycha A, Wiener H, Haitel A, Lodde M, Marberger M. Immunocyt: a new tool for detecting transitional cell cancer of the urinary tract. J Urol. 1999;161(5):1486–1489
  39. Vriesema JL, Atsma F, Kiemeney LA, Peelen WP, Witjes JA, Schalken JA. Diagnostic efficacy of the ImmunoCyt test to detect superficial bladder cancer recurrence. Urology. 2001;58(3):367–371
  40. Mian C, Lodde M, Comploj E, Negri G, Egarter-Vigl E, Lusuardi L, et al. Liquid-based cytology as a tool for the performance of uCyt+ and Urovysion Multicolour-FISH in the detection of urothelial carcinoma. Cytopathology. 2003;14(6):338–342
  41. Pfister C, Chautard D, Devonec M, Perrin P, Chopin D, Rischmann P, et al. Immunocyt test improves the diagnostic accuracy of urinary cytology: results of a French multicenter study. J Urol. 2003;169(3):921–924
  42. Sullivan PS, Nooraie F, Sanchez H, Hirschowitz S, Levin M, Rao PN, et al. Comparison of ImmunoCyt, UroVysion, and urine cytology in detection of recurrent urothelial carcinoma: a “split-sample” study. Cancer Cytopathol. 2009;117(3):167–173
  43. Gordon JN, Shu WP, Schlussel RN, Droller MJ, Liu BCS. Altered extracellular matrices influence cellular processes and nuclear matrix organisations of overlying human bladder urothelial cells. Cancer Res. 1993;53:4971–4977
  44. Berezney R, Coffey DS. Identification of a nuclear protein matrix. Biochem Biophys Res Commun. 1974;60(4):1410–1417
  45. Pardoll DM, Vogelstein B, Coffey DS. A fixed site of DNA replication in eukaryotic cells. Cell. 1980;19:527–536
  46. Compton DA, Cleveland DW. NuMA is required for the proper completion of mitosis. J Cell Biol. 1993;120:947–957
  47. Shelfo SW, Soloway MS. The role of nuclear matrix protein 22 in the detection of persistent or recurrent transitional-cell cancer of the bladder. World J Urol. 1997;15:107–111
  48. Hughes JH, Katz RL, Rodriguez-Villanueva J, Kidd L, Dinney C, Grossman HB, et al. Urinary nuclear matrix protein 22 (NMP22): a diagnostic adjunct to urine cytologic examination for the detection of recurrent transitional-cell carcinoma of the bladder. Diagn Cytopathol. 1999;20(5):285–290
  49. Miyanaga N, Akaza H, Tsukamoto T, Ishikawa S, Noguchi R, Ohtani M, et al. Urinary nuclear matrix protein 22 as a new marker for the screening of urothelial cancer in patients with microscopic hematuria. Int J Urol. 1999;6(4):173–177
  50. Stampfer D, Carpinito G, Rodriguez-Villanueva J, Willsey L, Dinney C, Grossman H, et al. Evaluation of NMP22 in the detection of transitional cell carcinoma of the bladder. J Urol. 1998;159:394–398
  51. Soloway MS, Briggman JV, Carpinito GA, Chodak GW, Church PA, Lamm DL, et al. Use of new tumor marker, urinary NMP22, in detection of occult or rapidly recurring transitional cell carcinoma of the urinary tract following surgical treatment. J Urol. 1996;156(2 Pt 1):363–367
  52. Ramakumar S, Bhuiyan J, Besse JA, Roberts SG, Wollan PC, Blute ML, et al. Comparison of screening methods in the detection of bladder cancer. J Urol. 1999;161(2):388–394
  53. Ponsky LE, Sharma S, Pandrangi L, Kedia S, Nelson D, Agarwal A, et al. Screening and monitoring for bladder cancer: refining the use of NMP22. J Urol. 2001;166:75–78
  54. Mansoor I, Calam RR, Al-Khafaji B. Role of urinary NMP-22 combined with urine cytology in follow-up surveillance of recurring superficial bladder urothelial carcinoma. Anal Quant Cytol Histol. 2008;30(1):25–32
  55. Shariat SF, Marberger MJ, Lotan Y, Sanchez-Carbayo M, Zippe C, Ludecke G, et al. Variability in the performance of nuclear matrix protein 22 for the detection of bladder cancer. J Urol. 2006;176(3):919–926
  56. Shariat SF, Casella R, Wians FH, Ashfaq R, Balko J, Sulser T, et al. Risk stratification for bladder tumor recurrence, stage and grade by urinary nuclear matrix protein 22 and cytology. Eur Urol. 2004;45(3):304–313author reply 313
  57. Shariat SF, Zippe C, Ludecke G, Boman H, Sanchez-Carbayo M, Casella R, et al. Nomograms including nuclear matrix protein 22 for prediction of disease recurrence and progression in patients with Ta, T1 or CIS transitional cell carcinoma of the bladder. J Urol. 2005;173(5):1518–1525
  58. Grossman HB, Messing E, Soloway M, Tomera K, Katz G, Berger Y, et al. Detection of bladder cancer using a point-of-care proteomic assay. JAMA. 2005;293(7):810–816
  59. Grossman HB, Soloway M, Messing E, Katz G, Stein B, Kassabian V, et al. Surveillance for recurrent bladder cancer using a point-of-care proteomic assay. JAMA. 2006;295(3):299–305
  60. Lotan Y, Shariat SF. Impact of risk factors on the performance of the nuclear matrix protein 22 point-of-care test for bladder cancer detection. BJU Int. 2008;101(11):1362–1367
  61. Lotan Y, Capitanio U, Shariat SF, Hutterer GC, Karakiewicz PI. Impact of clinical factors, including a point-of-care nuclear matrix protein-22 assay and cytology, on bladder cancer detection. BJU Int. 2009;103(10):1368–1374
  62. Junker K, Boerner D, Schulze W, Utting M, Schubert J, Werner W. Analysis of genetic alterations in normal bladder urothelium. Urology. 2003;62(6):1134–1138
  63. Halling KC. Vysis UroVysion for the detection of urothelial carcinoma. Expert Rev Mol Diagn. 2003;3(4):507–519
  64. Skacel M, Fahmy M, Brainard JA, Pettay JD, Biscotti CV, Liou LS, et al. Multitarget fluorescence in situ hybridization assay detects transitional cell carcinoma in the majority of patients with bladder cancer and atypical or negative urine cytology. J Urol. 2003;169(6):2101–2105
  65. Friedrich MG, Hellstern A, Toma MI, Hammerer P, Huland H. Are false-positive urine markers for the detection of bladder carcinoma really wrong or do they predict tumor recurrence?. Eur Urol. 2003;43(2):146–150discussion 150-1
  66. Halling KC, King W, Sokolova IA, Karnes RJ, Meyer RG, Powell EL, et al. A comparison of BTA stat, hemoglobin dipstick, telomerase and Vysis UroVysion assays for the detection of urothelial carcinoma in urine. J Urol. 2002;167(5):2001–2006
  67. Hajdinjak T. UroVysion FISH test for detecting urothelial cancers: meta-analysis of diagnostic accuracy and comparison with urinary cytology testing. Urol Oncol. 2008;26(6):646–651
  68. Daniely M, Rona R, Kaplan T, Olsfanger S, Elboim L, Freiberger A, et al. Combined morphologic and fluorescence in situ hybridization analysis of voided urine samples for the detection and follow-up of bladder cancer in patients with benign urine cytology. Cancer. 2007;111(6):517–524
  69. Daniely M, Rona R, Kaplan T, Olsfanger S, Elboim L, Zilberstien Y, et al. Combined analysis of morphology and fluorescence in situ hybridization significantly increases accuracy of bladder cancer detection in voided urine samples. Urology. 2005;66(6):1354–1359
  70. Lotan Y, Bensalah K, Ruddell T, Shariat SF, Sagalowsky AI, Ashfaq R. Prospective evaluation of the clinical usefulness of reflex fluorescence in situ hybridization assay in patients with atypical cytology for the detection of urothelial carcinoma of the bladder. J Urol. 2008;179(6):2164–2169
  71. Bergman J, Reznichek RC, Rajfer J. Surveillance of patients with bladder carcinoma using fluorescent in-situ hybridization on bladder washings. BJU Int. 2008;101(1):26–29
  72. Gofrit ON, Zorn KC, Silvestre J, Shalhav AL, Zagaja GP, Msezane LP, et al. The predictive value of multi-targeted fluorescent in-situ hybridization in patients with history of bladder cancer. Urol Oncol. 2008;26(3):246–249
  73. Yoder BJ, Skacel M, Hedgepeth R, Babineau D, Ulchaker JC, Liou LS, et al. Reflex UroVysion testing of bladder cancer surveillance patients with equivocal or negative urine cytology: a prospective study with focus on the natural history of anticipatory positive findings. Am J Clin Pathol. 2007;127(2):295–301
  74. Heicappell R, Schostack M, Müller M, Miller K. Evaluation of urinary bladder cancer antigen as a marker for diagnosis of transitional cell carcinoma of the urinary bladder. Scand J Clin Lab Invest. 2000;60(4):275–282
  75. Mian C, Lodde M, Haitel A, Egarter Vigl E, Marberger M, Pycha A. Comparison of two qualitative assays, the UBC rapid test and the BTA stat test, in the diagnosis of urothelial cell carcinoma of the bladder. Urology. 2000;56(2):228–231
  76. Saad A, Hanbury DC, McNicholas TA, Boustead GB, Woodman AC. The early detection and diagnosis of bladder cancer: a critical review of the options. Eur Urol. 2001;39:619–633
  77. Babjuk M, Kostirova M, Mudra K, Pecher S, Smolova H, Pecen L, et al. Qualitative and quantitative detection of urinary human complement factor H-related protein (BTA stat and BTA TRAK) and fragments of cytokeratins 8, 18 (UBC rapid and UBC IRMA) as markers for transitional cell carcinoma of the bladder. Eur Urol. 2002;41(1):34–39
  78. Hakenberg OW, Fuessel S, Richter K, Froehner M, Oehlschlaeger S, Rathert P, et al. Qualitative and quantitative assessment of urinary cytokeratin 8 and 18 fragments compared with voided urine cytology in diagnosis of bladder carcinoma. Urology. 2004;64(6):1121–1126
  79. Myers-Irvin JM, Landsittel D, Getzenberg RH. Use of the novel marker BLCA-1 for the detection of bladder cancer. J Urol. 2005;174(1):64–68
  80. Konety BR, Nguyen TS, Dhir R, Day RS, Becich MJ, Stadler WM, et al. Detection of bladder cancer using a novel nuclear matrix protein, BLCA-4. Clin Cancer Res. 2000;6(7):2618–2625
  81. Van Le TS, Myers J, Konety BR, Barder T, Getzenberg RH. Functional characterization of the bladder cancer marker, BLCA-4. Clin Cancer Res. 2004;10(4):1384–1391
  82. Van Le TS, Miller R, Barder T, Babjuk M, Potter DM, Getzenberg RH. Highly specific urine-based marker of bladder cancer. Urology. 2005;66(6):1256–1260
  83. Konety BR, Nguyen TS, Brenes G, Sholder A, Lewis N, Bastacky S, et al. Clinical usefulness of the novel marker BLCA-4 for the detection of bladder cancer. J Urol. 2000;164(3 Pt 1):634–639
  84. Knudson W. Tumor-associated hyaluronan. Providing an extracellular matrix that facilitates invasion. Am J Pathol. 1996;148(6):1721–1726
  85. Lokeshwar VB, Obek C, Soloway MS, Block NL. Tumor-associated hyaluronic acid: a new sensitive and specific urine marker for bladder cancer. Cancer Res. 1997;57(4):773–777
  86. Lokeshwar VB, Block NL. HA-HAase urine test. A sensitive and specific method for detecting bladder cancer and evaluating its grade. Urol Clin North Am. 2000;27(1):53–61
  87. Pham HT, Block NL, Lokeshwar VB. Tumor-derived hyaluronidase: a diagnostic urine marker for high-grade bladder cancer. Cancer Res. 1997;57(4):778–783
  88. Hautmann SH, Lokeshwar VB, Schroeder GL, Civantos F, Duncan RC, Gnann R, et al. Elevated tissue expression of hyaluronic acid and hyaluronidase validates the HA-HAase urine test for bladder cancer. J Urol. 2001;165(6 Pt 1):2068–2074
  89. Lokeshwar VB, Schroeder GL, Selzer MG, Hautmann SH, Posey JT, Duncan RC, et al. Bladder tumor markers for monitoring recurrence and screening comparison of hyaluronic acid-hyaluronidase and BTA-Stat tests. Cancer. 2002;95(1):61–72
  90. Hautmann S, Toma M, Lorenzo Gomez MF, Friedrich MG, Jaekel T, Michl U, et al. Immunocyt and the HA-HAase urine tests for the detection of bladder cancer: a side-by-side comparison. Eur Urol. 2004;46(4):466–471
  91. Decenzo JM, Howard P, Irish CE. Antigenic deletion and prognosis of patients with stage A transitional cell bladder carcinoma. J Urol. 1975;114(6):874–878
  92. Golijanin D, Sherman Y, Shapiro A, Pode D. Detection of bladder tumors by immunostaining of the Lewis X antigen in cells from voided urine. Urology. 1995;46(2):173–177
  93. Pode D, Golijanin D, Sherman Y, Lebensart P, Shapiro A. Immunostaining of Lewis X in cells from voided urine, cytopathology and ultrasound for noninvasive detection of bladder tumors. J Urol. 1998;159(2):389–392discussion 393
  94. Friedrich MG, Hellstern A, Hautmann SH, Graefen M, Conrad S, Huland E, et al. Clinical use of urinary markers for the detection and prognosis of bladder carcinoma: a comparison of immunocytology with monoclonal antibodies against Lewis X and 486p3/12 with the BTA STAT and NMP22 tests. J Urol. 2002;168(2):470–474
  95. van Rhijn BW, Lurkin I, Kirkels WJ, van der Kwast TH, Zwarthoff EC. Microsatellite analysis – DNA test in urine competes with cystoscopy in follow-up of superficial bladder carcinoma: a phase II trial. Cancer. 2001;92(4):768–775
  96. Czerniak B, Chaturvedi V, Li L, Hodges S, Johnston D, Roy JY, et al. Superimposed histologic and genetic mapping of chromosome 9 in progression of human urinary bladder neoplasia: implications for a genetic model of multistep urothelial carcinogenesis and early detection of urinary bladder cancer. Oncogene. 1999;18(5):1185–1196
  97. Knowles MA, Elder PA, Williamson M, Cairns JP, Shaw ME, Law MG. Allelotype of human bladder cancer. Cancer Res. 1994;54(2):531–538
  98. von Knobloch R, Hegele A, Brandt H, Olbert P, Heidenreich A, Hofmann R. Serum DNA and urine DNA alterations of urinary transitional cell bladder carcinoma detected by fluorescent microsatellite analysis. Int J Cancer. 2001;94(1):67–72
  99. van der Aa MN, Zwarthoff EC, Steyerberg EW, Boogaard MW, Nijsen Y, van der Keur KA, et al. Microsatellite analysis of voided-urine samples for surveillence of low-grade non-muscle-invasive urothelial carcinoma: feasibility and clinical utility in a prospective multicenter study (Cost-Effectiveness of Follow-Up of Urinary Bladder Cancer Trial [CEFUB]). Eur Urol. 2009;55(3):659–668
  100. van der Poel HG, van Balken MR, Schamhart DH, Peelen P, de Reijke T, Debruyne FM, et al. Bladder wash cytology, quantitative cytology, and the qualitative BTA test in patients with superficial bladder cancer. Urology. 1998;51(1):44–50
  101. Gregoire M, Fradet Y, Meyer F, Tetu B, Bois R, Bedard G, et al. Diagnostic accuracy of urinary cytology, and deoxyribonucleic acid flow cytometry and cytology on bladder washings during followup for bladder tumors. J Urol. 1997;157(5):1660–1664
  102. Cajulis RS, Haines GK, Frias-Hidvegi D, McVary K, Bacus JW. Cytology, flow cytometry, image analysis, and interphase cytogenetics by fluorescence in situ hybridization in the diagnosis of transitional cell carcinoma in bladder washes: a comparative study. Diagn Cytopathol. 1995;13(3):214–223discussion 224
  103. Witjes JA, van der Poel HG, van Balken MR, Debruyne FM, Schalken JA. Urinary NMP22 and karyometry in the diagnosis and follow-up of patients with superficial bladder cancer. Eur Urol. 1998;33(4):387–391
  104. Moonen PM, Merkx GF, Peelen P, Karthaus HF, Smeets DF, Witjes JA. UroVysion compared with cytology and quantitative cytology in the surveillance of non-muscle-invasive bladder cancer. Eur Urol. 2007;51(5):1275–1280discussion 1280
  105. Svatek RS, Herman MP, Lotan Y, Casella R, Hsieh JT, Sagalowsky AI, et al. Soluble Fas – a promising novel urinary marker for the detection of recurrent superficial bladder cancer. Cancer. 2006;106(8):1701–1707
  106. Altieri DC. Survivin, versatile modulation of cell division and apoptosis in cancer. Oncogene. 2003;22(53):8581–8589
  107. Margulis V, Lotan Y, Shariat SF. Survivin: a promising biomarker for detection and prognosis of bladder cancer. World J Urol. 2008;26(1):59–65
  108. Smith SD, Wheeler MA, Plescia J, Colberg JW, Weiss RM, Alterieri DC. Urine detection of survivin and diagnosis of bladder cancer. JAMA. 2001;285(3):324–328
  109. Shariat SF, Casella R, Khoddami SM, Hernandez G, Sulser T, Gasser TC, et al. Urine detection of survivin is a sensitive marker for the noninvasive diagnosis of bladder cancer. J Urol. 2004;171(2 Pt 1):626–630
  110. Schultz IJ, Kiemeney LA, Karthaus HF, Witjes JA, Willems JL, Swinkels DW, et al. Survivin mRNA copy number in bladder washings predicts tumor recurrence in patients with superficial urothelial cell carcinomas. Clin Chem. 2004;50(8):1425–1428
  111. Weikert S, Christoph F, Schrader M, Krause H, Miller K, Müller M. Quantitative analysis of survivin mRNA expression in urine and tumor tissue of bladder cancer patients and its potential relevance for disease detection and prognosis. Int J Cancer. 2005;116(1):100–104
  112. Smith SD, Wheeler MA, Plescia J, Colberg JW, Weiss RM, Altieri DC. Urine detection of survivin and diagnosis of bladder cancer. JAMA. 2001;285(3):324–328
  113. Greider CW. Telomere length regulation. Annu Rev Biochem. 1996;65:337–365
  114. Blackburn EH. Telomeres and their synthesis. Science. 1990;249:489–490
  115. Blackburn EH. Structure and function of telomeres. Nature. 1991;350:569–573
  116. Morin GB. The human telomere terminal transferase enzyme is a ribonucleoprotein that synthesizes TTAGGG repeats. Cell. 1989;59:521–529
  117. Ito H, Kyo S, Kanaya T, Takakura M, Inoue M, Namiki M. Expression of human telomerase subunits and correlation with telomerase activity in urothelial cancer. Clin Cancer Res. 1998;4(7):1603–1608
  118. Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, et al. Specific association of human telomerase activity with immortal cells and cancer. Science. 1994;266:2011–2015
  119. De Kok JB, Schalken JA, Aalders TW, Ruers TJ, Willems HL, Swinkels DW. Quantitative measurement of telomerase reverse transcriptase (hTERT) mRNA in urothelial cell carcinomas. Int J Cancer. 2000;87(2):217–220
  120. Melissourgos N, Kastrinakis NG, Davilas I, Foukas P, Farmakis A, Lykourinas M. Detection of human telomerase reverse transcriptase mRNA in urine of patients with bladder cancer: evaluation of an emerging tumor marker. Urology. 2003;62(2):362–367
  121. Wu X, Kakehi Y, Takahashi T, Habuchi T, Ogawa O. Telomerase activity in urine after transurethral resection of superficial bladder cancer and early recurrence. Int J Urol. 2000;7:210–217
  122. Cheng CW, Chueh SC, Chern HD. Diagnosis of bladder cancer using telomerase activity in voided urine. J Formos Med Assoc. 2000;99(12):920–925
  123. Cassel A, Rahat MA, Lahat N, Lindenfield N, Mecz Y, Stein A. Telomerase activity and cytokeratin 20 as markers for the detection and followup of transitional cell carcinoma: an unfulfilled promise. J Urol. 2001;166:841–844
  124. Kavaler E, Landman J, Chang Y, Droller MJ, Liu BC. Detecting human bladder carcinoma cells in voided urine samples by assaying for the presence of telomerase activity. Cancer. 1998;82(4):708–714
  125. Lee DH, Yang SC, Hong SJ, Chung BH, Kim IY. Telomerase: a potential marker of bladder transitional cell carcinoma in bladder washes. Clin Cancer Res. 1998;4(3):535–538
  126. Dalbagni G, Han W, Zhang ZF, Cordon-Cardo C, Saigo P, Fair WR, et al. Evaluation of the telomeric repeat amplification protocol (TRAP) assay for telomerase as a diagnostic modality in recurrent bladder cancer. Clin Cancer Res. 1997;3(9):1593–1598
  127. Yokota K, Kanda K, Inoue Y, Kanayama H, Kagawa S. Semi-quantitative analysis of telomerase activity in exfoliated human urothelial cells and bladder transitional cell carcinoma. Br J Urol. 1998;82(5):727–732
  128. Mayfield MP, Shah T, Flannigan GM, Hamilton Stewart PA, Bibby MC. Telomerase activity in malignant and benign bladder conditions. Int J Mol Med. 1998;1(5):835–840
  129. Müller M, Krause H, Heicappell R, Tischendorf J, Shay JW, Miller K. Comparison of human telomerase RNA and telomerase activity in urine for diagnosis of bladder cancer. Clin Cancer Res. 1998;4(8):1949–1954
  130. Lee MY, Tsou MH, Cheng MH, Chang DS, Yang AL, Ko JS. Clinical application of NMP22 and urinary cytology in patients with hematuria or a history of urothelial carcinoma. World J Urol. 2000;18:401–405
  131. Weikert S, Krause H, Wolff I, Christoph F, Schrader M, Emrich T, et al. Quantitative evaluation of telomerase subunits in urine as biomarkers for noninvasive detection of bladder cancer. Int J Cancer. 2005;117(2):274–280
  132. Sanchini MA, Gunelli R, Nanni O, Bravaccini S, Fabbri C, Sermasi A, et al. Relevance of urine telomerase in the diagnosis of bladder cancer. JAMA. 2005;294(16):2052–2056
  133. Guo B, Luo C, Xun C, Xie J, Wu X, Pu J. Quantitative detection of cytokeratin 20 mRNA in urine samples as diagnostic tools for bladder cancer by real-time PCR. Exp Oncol. 2009;31(1):43–47
  134. Soloway MS. Bladder tumor markers, intravesical therapy and systemic chemotherapy (Editorial). J Urol. 2001;166:488–489
  135. Yossepowitch O, Herr HW, Donat SM. Use of urinary biomarkers for bladder cancer surveillance: patient perspectives. J Urol. 2007;177(4):1277–1282discussion 1282
  136. Bensalah K, Montorsi F, Shariat SF. Challenges of cancer biomarker profiling. Eur Urol. 2007;52(6):1601–1609

PII: S1875-6867(09)00296-6

doi: 10.1016/j.jomh.2009.07.004

journal of men's health
Volume 6, Issue 4 , Pages 368-382 , December 2009