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Urinary Protein Markers for the Detection and Prognostication of Urothelial Carcinoma

  • Tibor Szarvas
  • Péter Nyirády
  • Osamu Ogawa
  • Hideki Furuya
  • Charles J. Rosser
  • Takashi Kobayashi
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1655)

Abstract

Bladder cancer diagnosis and surveillance is mainly based on cystoscopy and urine cytology. However, both methods have significant limitations; urine cytology has a low sensitivity for low-grade tumors, while cystoscopy is uncomfortable for the patients. Therefore, in the last decade urine analysis was the subject of intensive research resulting in the identification of many potential biomarkers for the detection, surveillance, or prognostic stratification of bladder cancer. Current trends move toward the development of multiparametric models to improve the diagnostic accuracy compared with single molecular markers. Recent technical advances for high-throughput and more sensitive measurements have led to the development of multiplex assays showing potential for more efficient tools toward future clinical application. In this review, we focus on the findings of urinary protein research in the context of detection and prognostication of bladder cancer. Furthermore, we provide an up-to-date overview on the recommendations for the quality evaluation of published studies as well as for the conduction of future urinary biomarker studies.

Key words

Urine Bladder cancer Biomarker Diagnosis Prognosis 

Notes

Acknowledgements

This study was supported by National Research, Development and Innovation Office; Grant number: NKFIH/PD 115616 and by János Bolyai Research Scholarship of the Hungarian Academy of Sciences.

References

  1. 1.
    Pasin E, Josephson DY, Mitra AP et al (2008) Superficial bladder cancer: an update on etiology, molecular development, classification, and natural history. Rev Urol 10:31–43PubMedPubMedCentralGoogle Scholar
  2. 2.
    Castillo-Martin M, Domingo-Domenech J, Karni-Schmidt O et al (2010) Molecular pathways of urothelial development and bladder tumorigenesis. Urol Oncol 28:401–408PubMedCrossRefGoogle Scholar
  3. 3.
    Knowles MA, Hurst CD (2015) Molecular biology of bladder cancer: new insights into pathogenesis and clinical diversity. Nat Rev Cancer 15:25–41PubMedCrossRefGoogle Scholar
  4. 4.
    Cancer Genome Atlas Research Network (2014) Comprehensive molecular characterization of urothelial bladder carcinoma. Nature 507:315–322CrossRefGoogle Scholar
  5. 5.
    McConkey DJ, Lee S, Choi W et al (2010) Molecular genetics of bladder cancer: emerging mechanisms of tumor initiation and progression. Urol Oncol 28:429–440PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Chang SS, Boorjian SA, Chou R et al (2016) Diagnosis and treatment of non-muscle invasive bladder cancer: AUA/SUO guideline. J Urol 196:1021–1029PubMedCrossRefGoogle Scholar
  7. 7.
    Kaplan AL, Litwin MS, Chamie K (2014) The future of bladder cancer care in the USA. Nat Rev Urol 11:59–62PubMedCrossRefGoogle Scholar
  8. 8.
    Mossanen M, Gore JL (2014) The burden of bladder cancer care: direct and indirect costs. Curr Opin Urol 24:487–491PubMedCrossRefGoogle Scholar
  9. 9.
    Yeung C, Dinh T, Lee J (2014) The health economics of bladder cancer: an updated review of the published literature. Pharmacoeconomics 32:1093–1104PubMedCrossRefGoogle Scholar
  10. 10.
    Rosser CJ, Urquidi V, Goodison S et al (2013) Urinary biomarkers of bladder cancer: an update and future perspectives. Biomark Med 7:779–790PubMedCrossRefGoogle Scholar
  11. 11.
    Budman LI, Kassouf W, Steinberg JR et al (2008) Biomarkers for detection and surveillance of bladder cancer. Can Urol Assoc J 2:212–221PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    D'Costa JJ, Goldsmith JC, Wilson JS et al (2016) A systematic review of the diagnostic and prognostic value of urinary protein biomarkers in Urothelial bladder cancer. Bladder Cancer 2:301–317PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Chatziharalambous D, Lygirou V, Latosinska A et al (2016) Analytical performance of ELISA assays in urine: one more bottleneck towards biomarker validation and clinical implementation. PLoS One 11:e0149471PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Goebell PJ, Groshen SL, Schmitz-Dräger BJ (2008) Guidelines for development of diagnostic markers in bladder cancer. World J Urol 26:5–11PubMedCrossRefGoogle Scholar
  15. 15.
    Lotan Y, Shariat SF, Schmitz-Dräger BJ et al (2010) Considerations on implementing diagnostic markers into clinical decision making in bladder cancer. Urol Oncol 28:441–448PubMedCrossRefGoogle Scholar
  16. 16.
    Kobayashi T, Owczarek TB, McKiernan JM et al (2015) Modelling bladder cancer in mice: opportunities and challenges. Nat Rev Cancer 15:42–54PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Oxford Centre for Evidence-based Medicine Levels of Evidence (2016). Available from: http://www.cebm.net
  18. 18.
    Goebell PJ, Groshen S, Schmitz-Dräger BJ et al (2014) The International bladder cancer Bank: proposal for a new study concept. Urol Oncol 22:277–284CrossRefGoogle Scholar
  19. 19.
    Goebell PJ, Kamat AM, Sylvester RJ et al (2014) Assessing the quality of studies on the diagnostic accuracy of tumor markers. Urol Oncol 32:1051–1060PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Wells G et al (2014) Newcastle-Otawa scale. Available from: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
  21. 21.
    Whiting P, Rutjes AW, Reitsma JB et al (2003) The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodol 3:25PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Whiting PF, Rutjes AW, Westwood ME et al (2011) QUADAS-2 Group.QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536PubMedCrossRefGoogle Scholar
  23. 23.
    Bossuyt PM, Reitsma JB, Bruns DE et al (2003) Standards for reporting of diagnostic accuracy the STARD statement for reporting studies of diagnostic accuracy: explanation and elaboration. Clin Chem 49:7–18PubMedCrossRefGoogle Scholar
  24. 24.
    Bossuyt PM, Reitsma JB, Bruns DE et al (2004) Towards complete and accurate reporting of studies of diagnostic accuracy: the STARD initiative. Fam Pract 21:4–10PubMedCrossRefGoogle Scholar
  25. 25.
    McShane LM, Altman DG, Sauerbrei W et al (2005) Statistics subcommittee of the NCI-EORTC working group on cancer diagnostics. REporting recommendations for tumour MARKer prognostic studies (REMARK). Br J Cancer 93:387–391PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Moore HM, Kelly A, McShane LM et al (2013) Biospecimen reporting for improved study quality (BRISQ). Transfusion 53:e1PubMedCrossRefGoogle Scholar
  27. 27.
    Simeon-Dubach D, Moore HM (2014) BIO comes into the cold to adopt BRISQ. Biopreserv Biobank 12:223–224PubMedCrossRefGoogle Scholar
  28. 28.
    Dreier M, Borutta B, Stahmeyer J et al (2010) Comparison of tools for assessing the methodological quality of primary and secondary studies in health technology assessment reports in Germany. GMS Health Technol 6:Doc07Google Scholar
  29. 29.
    Qi D, Li J, Jiang M et al (2015) The relationship between promoter methylation of p16 gene and bladder cancer risk: a meta-analysis. Int J Clin Exp Med 8:20701–20711PubMedPubMedCentralGoogle Scholar
  30. 30.
    Lopez LM, Chen M, Mullins Long S et al (2015) Steroidal contraceptives and bone fractures in women: evidence from observational studies. Cochrane Database Syst Rev 21(7):CD009849Google Scholar
  31. 31.
    Thelma Beatriz GC, Isela JR, Alma G et al (2014) Association between HTR2C gene variants and suicidal behaviour: a protocol for the systematic review and meta-analysis of genetic studies. BMJ Open 4:e005423PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Hartling L, Milne A, Hamm MP et al (2013) Testing the Newcastle Ottawa scale showed low reliability between individual reviewers. J Clin Epidemiol 66:982–993PubMedCrossRefGoogle Scholar
  33. 33.
    Oremus M, Oremus C, Hall GB et al (2012) ECT & Cognition Systematic Review Team. Inter-rater and test-retest reliability of quality assessments by novice student raters using the Jadad and Newcastle-Ottawa scales. BMJ Open 2:e001368PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25:603–605PubMedCrossRefGoogle Scholar
  35. 35.
    Xia Y, Liu YL, Yang KH (2010) The diagnostic value of urine-based survivin mRNA test using reverse transcription-polymerase chain reaction for bladder cancer: a systematic review. Chin J Cancer 29:441–446PubMedCrossRefGoogle Scholar
  36. 36.
    Yang X, Huang H, Zeng Z et al (2013) Diagnostic value of bladder tumor fibronectin in patients with bladder tumor: a systematic review with meta-analysis. Clin Biochem 46:1377–1382PubMedCrossRefGoogle Scholar
  37. 37.
    Hollingworth W, Medina LS, Lenkinski RE et al (2006) Interrater reliability in assessing quality of diagnostic accuracy studies using the QUADAS tool. A preliminary assessment. Acad Radiol 13:803–810PubMedCrossRefGoogle Scholar
  38. 38.
    Whiting PF, Weswood ME, Rutjes AW et al (2006) Evaluation of QUADAS, a tool for the quality assessment of diagnostic accuracy studies. BMC Med Res Methodol 6:9PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Cai Q, Wu Y, Guo Z et al (2015) Urine BLCA-4 exerts potential role in detecting patients with bladder cancers: a pooled analysis of individual studies. Oncotarget 6:37500–37510PubMedPubMedCentralGoogle Scholar
  40. 40.
    Huang YL, Chen J, Yan W et al (2015) Diagnostic accuracy of cytokeratin-19 fragment (CYFRA 21-1) for bladder cancer: a systematic review and meta-analysis. Tumour Biol 36:3137–3145PubMedCrossRefGoogle Scholar
  41. 41.
    Smidt N, Rutjes AW, van der Windt DA et al (2006) Reproducibility of the STARD checklist: an instrument to assess the quality of reporting of diagnostic accuracy studies. BMC Med Res Methodol 6:12PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Yang N, Feng S, Shedden K et al (2011) Urinary glycoprotein biomarker discovery for bladder cancer detection using LC/MS-MS and label-free quantification. Clin Cancer Res 17:3349–3359PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Miyake M, Ross S, Lawton A et al (2013) Investigation of CCL18 and A1AT as potential urinary biomarkers for bladder cancer detection. BMC Urol 13:42PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Shabayek MI, Sayed OM, Attaia HA et al (2014) Diagnostic evaluation of urinary angiogenin (ANG) and clusterin (CLU) as biomarker for bladder cancer. Pathol Oncol Res 20:859–866PubMedCrossRefGoogle Scholar
  45. 45.
    Chen YT, Chen CL, Chen HW et al (2010) Discovery of novel bladder cancer biomarkers by comparative urine proteomics using iTRAQ technology. J Proteome Res 9:5803–5815PubMedCrossRefGoogle Scholar
  46. 46.
    Kumar P, Nandi S, Tan TZ et al (2015) Highly sensitive and specific novel biomarkers for the diagnosis of transitional bladder carcinoma. Oncotarget 6:13539–13549PubMedPubMedCentralGoogle Scholar
  47. 47.
    Korman HJ, Peabody JO, Cerny JC et al (1996) Autocrine motility factor receptor as a possible urine marker for transitional cell carcinoma of the bladder. J Urol 155:347–349PubMedCrossRefGoogle Scholar
  48. 48.
    Bhagirath D, Abrol N, Khan R et al (2012) Expression of CD147, BIGH3 and Stathmin and their potential role as diagnostic marker in patients with urothelial carcinoma of the bladder. Clin Chim Acta 413:1641–1646PubMedCrossRefGoogle Scholar
  49. 49.
    Ebbing J, Mathia S, Seibert FS et al (2014) Urinary calprotectin: a new diagnostic marker in urothelial carcinoma of the bladder. World J Urol 32:1485–1492PubMedCrossRefGoogle Scholar
  50. 50.
    Svatek RS, Karam J, Karakiewicz PI et al (2008) Role of urinary cathepsin B and L in the detection of bladder urothelial cell carcinoma. J Urol 179:478–484PubMedCrossRefGoogle Scholar
  51. 51.
    Tilki D, Singer BB, Shariat SF et al (2010) CEACAM1: a novel urinary marker for bladder cancer detection. Eur Urol 5:648–654CrossRefGoogle Scholar
  52. 52.
    Hazzaa SM, Elashry OM, Afifi IK (2010) Clusterin as a diagnostic and prognostic marker for transitional cell carcinoma of the bladder. Pathol Oncol Res 16:101–109PubMedCrossRefGoogle Scholar
  53. 53.
    Nakashima M, Matsui Y, Kobayashi T et al (2015) Urine CXCL1 as a biomarker for tumor detection and outcome prediction in bladder cancer. Cancer Biomark 15:357–364PubMedCrossRefGoogle Scholar
  54. 54.
    Burnier A, Shimizu Y, Dai Y et al (2015) CXCL1 is elevated in the urine of bladder cancer patients. Springerplus 4:610PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Nisman B, Barak V, Shapiro A et al (2002) Evaluation of urine CYFRA 21-1 for the detection of primary and recurrent bladder carcinoma. Cancer 94:2914–2922PubMedCrossRefGoogle Scholar
  56. 56.
    Sánchez-Carbayo M, Espasa A, Chinchilla V et al (1999) New electrochemiluminescent immunoassay for the determination of CYFRA 21-1: analytical evaluation and clinical diagnostic performance in urine samples of patients with bladder cancer. Clin Chem 45:1944–1953PubMedGoogle Scholar
  57. 57.
    Fernandez-Gomez J, Rodríguez-Martínez JJ, Barmadah SE et al (2007) Urinary CYFRA 21.1 is not a useful marker for the detection of recurrences in the follow-up of superficial bladder cancer. Eur Urol 51:1267–1274PubMedCrossRefGoogle Scholar
  58. 58.
    Pariente JL, Bordenave L, Michel P et al (1997) Initial evaluation of CYFRA 21-1 diagnostic performances as a urinary marker in bladder transitional cell carcinoma. J Urol 158:338–341PubMedCrossRefGoogle Scholar
  59. 59.
    Morgan R, Bryan RT, Javed S et al (2013) Expression of engrailed-2 (EN2) protein in bladder cancer and its potential utility as a urinary diagnostic biomarker. Eur J Cancer 49:2214–2222PubMedCrossRefGoogle Scholar
  60. 60.
    Ramakumar S, Bhuiyan J, Besse JA et al (1999) Comparison of screening methods in the detection of bladder cancer. J Urol 161:388–394PubMedCrossRefGoogle Scholar
  61. 61.
    Mutlu N, Turkeri L, Emerk K (2003) Analytical and clinical evaluation of a new urinary tumor marker: bladder tumor fibronectin in diagnosis and follow-up of bladder cancer. Clin Chem Lab Med 41:1069–1074PubMedCrossRefGoogle Scholar
  62. 62.
    Li LY, Yang M, Zhang HB et al (2008) Urinary fibronectin as a predictor of a residual tumour load after transurethral resection of bladder transitional cell carcinoma. BJU Int 102:566–571PubMedCrossRefGoogle Scholar
  63. 63.
    Chen YT, Chen HW, Domanski D et al (2012) Multiplexed quantification of 63 proteins in human urine by multiple reaction monitoring-based mass spectrometry for discovery of potential bladder cancer biomarkers. J Proteomics 75:3529–3545PubMedCrossRefGoogle Scholar
  64. 64.
    Orenes-Piñero E, Cortón M, González-Peramato P et al (2007) Searching urinary tumor markers for bladder cancer using a two-dimensional differential gel electrophoresis (2D-DIGE) approach. J Proteome Res 6:4440–4448PubMedCrossRefGoogle Scholar
  65. 65.
    Eissa S, Labib RA, Mourad MS et al (2003) Comparison of telomerase activity and matrix metalloproteinase-9 in voided urine and bladder wash samples as a useful diagnostic tool for bladder cancer. Eur Urol 44:687–694PubMedCrossRefGoogle Scholar
  66. 66.
    Hakenberg OW, Fuessel S, Richter K et al (2004) Qualitative and quantitative assessment of urinary cytokeratin 8 and 18 fragments compared with voided urine cytology in diagnosis of bladder carcinoma. Urology 64:1121–1126PubMedCrossRefGoogle Scholar
  67. 67.
    Mian C, Lodde M, Haitel A (2000) 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 56:228–231PubMedCrossRefGoogle Scholar
  68. 68.
    Sánchez-Carbayo M, Herrero E, Megías J et al (1999) Initial evaluation of the new urinary bladder cancer rapid test in the detection of transitional cell carcinoma of the bladder. Urology 54:656–661PubMedCrossRefGoogle Scholar
  69. 69.
    Ecke TH, Arndt C, Stephan C et al (2015) Preliminary results of a multicentre study of the UBC rapid test for detection of urinary bladder cancer. Anticancer Res 35:2651–2655PubMedGoogle Scholar
  70. 70.
    Babjuk M, Kostírová M, Mudra K et al (2002) 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 41:34–39PubMedCrossRefGoogle Scholar
  71. 71.
    Giannopoulos A, Manousakas T, Gounari A et al (2001) Comparative evaluation of the diagnostic performance of the BTA stat test, NMP22 and urinary bladder cancer antigen for primary and recurrent bladder tumors. J Urol 166:470–475PubMedCrossRefGoogle Scholar
  72. 72.
    May M, Hakenberg OW, Gunia S, Pohling P, Helke C, Lübbe L, Nowack R, Siegsmund M, Hoschke B (2007) Comparative diagnostic value of urine cytology, UBC-ELISA, and fluorescence in situ hybridization for detection of transitional cell carcinoma of urinary bladder in routine clinical practice. Urology 70(3):449–453PubMedCrossRefGoogle Scholar
  73. 73.
    Mian C, Lodde M, Haitel A et al (2000) Comparison of the monoclonal UBC-ELISA test and the NMP22 ELISA test for the detection of urothelial cell carcinoma of the bladder. Urology 55:223–226PubMedCrossRefGoogle Scholar
  74. 74.
    Boman H, Hedelin H, Holmäng S (2002) Four bladder tumor markers have a disappointingly low sensitivity for small size and low grade recurrence. J Urol 167:80–83PubMedCrossRefGoogle Scholar
  75. 75.
    Boman H, Hedelin H, Jacobsson S et al (2002) Newly diagnosed bladder cancer: the relationship of initial symptoms, degree of microhematuria and tumor marker status. J Urol 168:1955–1959PubMedCrossRefGoogle Scholar
  76. 76.
    Mungan NA, Vriesema JL, Thomas CM et al (2002) Urinary bladder cancer test: a new urinary tumor marker in the follow-up of superficial bladder cancer. Urology 56:787–792CrossRefGoogle Scholar
  77. 77.
    Kawanishi H, Matsui Y, Ito M et al (2008) Secreted CXCL1 is a potential mediator and marker of the tumor invasion of bladder cancer. Clin Cancer Res 14:2579–2587PubMedCrossRefGoogle Scholar
  78. 78.
    Su L, Cao L, Zhou R et al (2013) Identification of novel biomarkers for sepsis prognosis via urinary proteomic analysis using iTRAQ labeling and 2D-LC-MS/MS. PLoS One 8:e54237PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Bakun M, Niemczyk M, Domanski D et al (2012) Urine proteome of autosomal dominant polycystic kidney disease patients. Clin Proteomics 9:13PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Lei T, Zhao X, Jin S et al (2013) Discovery of potential bladder cancer biomarkers by comparative urine proteomics and analysis. Clin Genitourin Cancer 11:56–62PubMedCrossRefGoogle Scholar
  81. 81.
    Lindén M, Lind SB, Mayrhofer C et al (2012) Proteomic analysis of urinary biomarker candidates for nonmuscle invasive bladder cancer. Proteomics 12:135–144PubMedCrossRefGoogle Scholar
  82. 82.
    Majewski T, Spiess PE, Bondaruk J et al (2012) Detection of bladder cancer using proteomic profiling of urine sediments. PLoS One 7:e42452PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Urquidi V, Goodison S, Cai Y et al (2012) A candidate molecular biomarker panel for the detection of bladder cancer. Cancer Epidemiol Biomarkers Prev 21:2149–2158PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Kreunin P, Zhao J, Rosser C et al (2007) Bladder cancer associated glycoprotein signatures revealed by urinary proteomic profiling. J Proteome Res 6:2631–2639PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Goodison S, Chang M, Dai Y et al (2012) A multi-analyte assay for the non-invasive detection of bladder cancer. PLoS One 7:e47469PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Rosser CJ, Ross S, Chang M et al (2013) Multiplex protein signature for the detection of bladder cancer in voided urine samples. J Urol 190:2257–2262PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Chen LM, Chang M, Dai Y et al (2014) External validation of a multiplex urinary protein panel for the detection of bladder cancer in a multicenter cohort. Cancer Epidemiol Biomarkers Prev 23:1804–1812PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Rosser CJ, Chang M, Dai Y et al (2014) Urinary protein biomarker panel for the detection of recurrent bladder cancer. Cancer Epidemiol Biomarkers Prev 23:1340–1345PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Huang S, Kou L, Furuya H et al (2016) A Nomogram derived by combination of demographic and biomarker data improves the noninvasive evaluation of patients at risk for bladder cancer. Cancer Epidemiol Biomarkers Prev 25:1361–1366PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Shimizu Y, Furuya H, Bryant Greenwood P et al (2016) A multiplex immunoassay for the non-invasive detection of bladder cancer. J Transl Med 14:31PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Frantzi M, van Kessel KE, Zwarthoff EC et al (2016) Development and validation of urine-based peptide biomarker panels for detecting bladder cancer in a multi-center study. Clin Cancer Res 22:4077–4086PubMedCrossRefGoogle Scholar
  92. 92.
    Goodison S, Ogawa O, Matsui Y et al (2016) A multiplex urinary immunoassay for bladder cancer detection: analysis of a Japanese cohort. J Transl Med 14:287PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Stein JP, Skinner DG (2006) Radical cystectomy for invasive bladder cancer: long-term results of a standard procedure. World J Urol 24:296–304PubMedCrossRefGoogle Scholar
  94. 94.
    Poulakis V, Witzsch U, De Vries R (2001) A comparison of urinary nuclear matrix protein-22 and bladder tumour antigen tests with voided urinary cytology in detecting and following bladder cancer: the prognostic value of false-positive results. BJU Int 88:692–701PubMedCrossRefGoogle Scholar
  95. 95.
    Raitanen MP, Kaasinen E, Rintala E et al (2001) Prognostic utility of human complement factor H related protein test (the BTA stat test). Br J Cancer 85:552–556PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Bryan RT, Regan HL, Pirrie SJ et al (2015) Protein shedding in urothelial bladder cancer: prognostic implications of soluble urinary EGFR and EpCAM. Br J Cancer 112:1052–1058PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Feng J, He W, Song Y et al (2014) Platelet-derived growth factor receptor beta: a novel urinary biomarker for recurrence of non-muscle-invasive bladder cancer. PLoS One 9:e96671PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Svatek RS, Herman MP, Lotan Y et al (2006) Soluble Fas–a promising novel urinary marker for the detection of recurrent superficial bladder cancer. Cancer 106:1701–1707PubMedCrossRefGoogle Scholar
  99. 99.
    Yang H, Li H, Wang Z et al (2013) Is urinary soluble Fas an independent predictor of non-muscle-invasive bladder cancer? A prospective chart study. Urol Int 91:456–461PubMedCrossRefGoogle Scholar
  100. 100.
    Bryan RT, Shimwell NJ, Wei W et al (2014) Urinary EpCAM in urothelial bladder cancer patients: characterisation and evaluation of biomarker potential. Br J Cancer 110:679–685PubMedCrossRefGoogle Scholar
  101. 101.
    Guan Z, Zeng J, Wang Z et al (2014) Urine tenascin-C is an independent risk factor for bladder cancer patients. Mol Med Rep 9:961–966PubMedCrossRefGoogle Scholar
  102. 102.
    Durkan GC, Nutt JE, Rajjayabun PH et al (2001) Prognostic significance of matrix metalloproteinase-1 and tissue inhibitor of metalloproteinase-1 in voided urine samples from patients with transitional cell carcinoma of the bladder. Clin Cancer Res 7:3450–3456PubMedGoogle Scholar
  103. 103.
    Offersen BV, Knap MM, Horsman MR et al (2010) Matrix metalloproteinase-9 measured in urine from bladder cancer patients is an independent prognostic marker of poor survival. Acta Oncol 49:1283–1287PubMedCrossRefGoogle Scholar
  104. 104.
    Durkan GC, Nutt JE, Marsh C et al (2003) Alteration in urinary matrix metalloproteinase-9 to tissue inhibitor of metalloproteinase-1 ratio predicts recurrence in nonmuscle-invasive bladder cancer. Clin Cancer Res 9:2576–2582PubMedGoogle Scholar
  105. 105.
    Becker M, Szarvas T, Wittschier M et al (2010) Prognostic impact of plasminogen activator inhibitor type 1 expression in bladder cancer. Cancer 116:4502–4512PubMedCrossRefGoogle Scholar
  106. 106.
    Kelloniemi E, Rintala E, Finne P et al (2003) Tumor-associated trypsin inhibitor as a prognostic factor during follow-up of bladder cancer. Urology 62:249–253PubMedCrossRefGoogle Scholar
  107. 107.
    Feldman AS, Banyard J, Wu CL et al (2009) Cystatin B as a tissue and urinary biomarker of bladder cancer recurrence and disease progression. Clin Cancer Res 15:1024–1031PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Zimmerman R, Wahren B, Edsmyr F (1980) Assessment of serial CEA determinations in urine of patients with bladder carcinoma. Cancer 46:1802–1809PubMedCrossRefGoogle Scholar
  109. 109.
    Arnold SA, Loomans HA, Ketova T et al (2016) Urinary oncofetal ED-A fibronectin correlates with poor prognosis in patients with bladder cancer. Clin Exp Metastasis 33:29–44PubMedCrossRefGoogle Scholar
  110. 110.
    Compton DA, Cleveland DW (1993) NuMA is required for the proper completion of mitosis. J Cell Biol 120:947–957PubMedCrossRefGoogle Scholar
  111. 111.
    Mizutani Y, Yoshida O, Ukimura O et al (2002) Prognostic significance of a combination of soluble Fas and soluble Fas ligand in the serum of patients with ta bladder cancer. Cancer Biother Radiopharm 17:563–567PubMedCrossRefGoogle Scholar
  112. 112.
    Szarvas T, vom Dorp F, Ergün S et al (2011) Matrix metalloproteinases and their clinical relevance in urinary bladder cancer. Nat Rev Urol 8:241–254PubMedCrossRefGoogle Scholar
  113. 113.
    Szarvas T, Becker M, vom Dorp F et al (2010) Matrix metalloproteinase-7 as a marker of metastasis and predictor of poor survival in bladder cancer. Cancer Sci 101:1300–1308PubMedCrossRefGoogle Scholar
  114. 114.
    Szarvas T, Jäger T, Becker M et al (2011) Validation of circulating MMP-7 level as an independent prognostic marker of poor survival in urinary bladder cancer. Pathol Oncol Res 17:325–332PubMedCrossRefGoogle Scholar
  115. 115.
    Szarvas T, Singer BB, Becker M et al (2011) Urinary matrix metalloproteinase-7 level is associated with the presence of metastasis in bladder cancer. BJU Int 107:1069–1073PubMedCrossRefGoogle Scholar
  116. 116.
    Cruz-Munoz W, Khokha R (2008) The role of tissue inhibitors of metalloproteinases in tumorigenesis and metastasis. Crit Rev Clin Lab Sci 45:291–338PubMedCrossRefGoogle Scholar
  117. 117.
    Thomas P, Khokha R, Shepherd FA et al (2000) Differential expression of matrix metalloproteinases and their inhibitors in non-small cell lung cancer. J Pathol 190:150–156PubMedCrossRefGoogle Scholar
  118. 118.
    Rhee JS, Diaz R, Korets L et al (2004) TIMP-1 alters susceptibility to carcinogenesis. Cancer Res 64:952–961PubMedCrossRefGoogle Scholar
  119. 119.
    Brunner A, Prelog M, Verdorfer I et al (2008) EpCAM is predominantly expressed in high grade and advanced stage urothelial carcinoma of the bladder. J Clin Pathol 61:307–310PubMedCrossRefGoogle Scholar
  120. 120.
    Brunner A, Mayerl C, Tzankov A et al (2004) Prognostic significance of tenascin-C expression in superficial and invasive bladder cancer. J Clin Pathol 57:927–931PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Feng Z, Kagan J, Pepe M et al (2013) The early detection research Network's specimen reference sets: paving the way for rapid evaluation of potential biomarkers. Clin Chem 59:68–74PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media LLC 2018

Authors and Affiliations

  • Tibor Szarvas
    • 2
  • Péter Nyirády
    • 2
  • Osamu Ogawa
    • 1
  • Hideki Furuya
    • 3
  • Charles J. Rosser
    • 3
  • Takashi Kobayashi
    • 1
  1. 1.Department of UrologyKyoto University Graduate School of MedicineKyotoJapan
  2. 2.Department of UrologySemmelweis UniversityBudapestHungary
  3. 3.Clinical and Translational Research ProgramUniversity of Hawaii Cancer CenterHonoluluUSA

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