Urinary biomarkers for diagnosis of bladder cancer: A systematic review and meta-analysis

Annals of Internal Medicine

Volumn 163, Issue 12, 2015, Pages 922-931

  Chou, Roger ^a,b   Gore, John L ^a,c   Buckley, David ^a,b   Fu, Rongwei ^a,b   Gustafson, Katie ^a,b   Griffin, Jessica C ^a,b   Grusing, Sara ^a,b   Selph, Shelley ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLADDER TUMOR ANTIGEN; NUCLEAR MATRIX PROTEIN 22; TUMOR ANTIGEN; TUMOR MARKER; UNCLASSIFIED DRUG; BLADDER TUMOR-ASSOCIATED ANTIGEN; NUCLEAR PROTEIN;

BLADDER CANCER; CANCER DIAGNOSIS; CANCER GRADING; CANCER RECURRENCE; CANCER STAGING; CLINICAL ASSESSMENT; CLINICAL EVALUATION; COCHRANE LIBRARY; CYSTOSCOPY; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST ACCURACY STUDY; EVIDENCE BASED PRACTICE; FLUORESCENCE IN SITU HYBRIDIZATION; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; INTERMETHOD COMPARISON; MEDLINE; META ANALYSIS (TOPIC); PRIORITY JOURNAL; QUALITATIVE ANALYSIS; QUALITY CONTROL; QUANTITATIVE ANALYSIS; RECURRENT DISEASE; REVIEW; SENSITIVITY ANALYSIS; SENSITIVITY AND SPECIFICITY; SYSTEMATIC REVIEW; URINALYSIS; META ANALYSIS; TUMOR RECURRENCE; URINARY BLADDER NEOPLASMS; URINE;

ANTIGENS, NEOPLASM; BIOMARKERS, TUMOR; CYSTOSCOPY; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; NEOPLASM GRADING; NEOPLASM RECURRENCE, LOCAL; NEOPLASM STAGING; NUCLEAR PROTEINS; SENSITIVITY AND SPECIFICITY; URINARY BLADDER NEOPLASMS;

EID: 84950318200     PISSN: 00034819     EISSN: 15393704     Source Type: Journal    
DOI: 10.7326/M15-0997     Document Type: Review

References (84)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014;64:9-29. [PMID: 24399786]
2. Babjuk M, Burger M, Zigeuner R, Shariat SF, van Rhijn BW, Compérat E, et al; European Association of Urology. EAU guidelines on non-muscle-invasive urothelial carcinoma of the bladder: update 2013. Eur Urol. 2013;64:639-53. [PMID: 23827737]
3. Hall MC, Chang SS, Dalbagni G, Pruthi RS, Seigne JD, Skinner EC, et al. Guideline for the management of nonmuscle invasive bladder cancer (stages Ta, T1, and Tis): 2007 update. J Urol. 2007;178:2314-30. [PMID: 17993339]
4. Herman MP, Svatek RS, Lotan Y, Karakiewizc PI, Shariat SF. Urinebased biomarkers for the early detection and surveillance of nonmuscle invasive bladder cancer. Minerva Urol Nefrol. 2008;60:217-35. [PMID: 18923359]
5. Chou R, Buckley D, Fu R, Gore J, Gustafson K, Griffin J, et al. Emerging approaches to diagnosis and treatment of non-muscleinvasive bladder cancer. Comparative effectiveness review. (Prepared by the Pacific Northwest Evidence-based Practice Center.) Rockville, MD: Agency for Healthcare Research and Quality; 2015. [Forthcoming].
6. Agency for Healthcare Research and Quality. Methods Guide for Effectiveness and Comparative Effectiveness Reviews. AHRQ publication no. 10 (13)-EHC063-EF. Rockville, MD: Agency for Healthcare Research and Quality; 2014.
7. Chou R, Gore J, Buckley D, Selph S, Gustafson K, Griffin J, et al. Emerging approaches to diagnosis and treatment of non-muscleinvasive bladder cancer. PROSPERO International Prospective Register of Systematic Reviews. 2014.
8. Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, et al; QUADAS-2 Group. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155:529-36. [PMID: 22007046]
9. Chu H, Cole SR. Bivariate meta-analysis of sensitivity and specificity with sparse data: a generalized linear mixed model approach [Letter]. J Clin Epidemiol. 2006;59:1331-2. [PMID: 17098577]
10. Fu R, Gartlehner G, Grant M, Shamliyan T, Sedrakyan A, Wilt TJ, et al. Conducting quantitative synthesis when comparing medical interventions. In: Agency for Healthcare Research and Quality, ed. Methods Guide for Effectiveness and Comparative Effectiveness Reviews. Rockville, MD: Agency for Healthcare Research and Quality; 2013.
11. Zwinderman AH, Bossuyt PM. We should not pool diagnostic likelihood ratios in systematic reviews. Stat Med. 2008;27:687-97. [PMID: 17611957]
12. Trikalinos TA, Balion CM, Coleman CI, Griffith L, Santaguida PL, Vandermeer B, et al. Chapter 8: meta-analysis of test performance when there is a "gold standard". J Gen Intern Med. 2012;27 Suppl 1:S56-66. [PMID: 22648676]
13. Chappell FM, Raab GM, Wardlaw JM. When are summary ROC curves appropriate for diagnostic meta-analyses? Stat Med. 2009;28:2653-68. [PMID: 19591118]
14. Takwoingi Y, Leeflang MM, Deeks JJ. Empirical evidence of the importance of comparative studies of diagnostic test accuracy. Ann Intern Med. 2013;158:544-54. [PMID: 23546566]
15. Chahal R, Darshane A, Browning AJ, Sundaram SK. Evaluation of the clinical value of urinary NMP22 as a marker in the screening and surveillance of transitional cell carcinoma of the urinary bladder. Eur Urol. 2001;40:415-20. [PMID: 11713396]
16. Feil G, Zumbrägel A, Päulgen-Nelde HJ, Hennenlotter J, Maurer S, Krause S, et al. Accuracy of the ImmunoCyt assay in the diagnosis of transitional cell carcinoma of the urinary bladder. Anticancer Res. 2003;23:963-7. [PMID: 12820331]
17. 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;168:470-4. [PMID: 12131290]
18. Giannopoulos A, Manousakas T, Gounari A, Constantinides C, Choremi-Papadopoulou H, Dimopoulos C. 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. 2001;166:470-5. [PMID: 11458049]
19. Gibanel R, Ribal MJ, Filella X, Ballesta AM, Molina R, Alcaraz A, et al. BTA TRAK urine test increases the efficacy of cytology in the diagnosis of low-grade transitional cell carcinoma of the bladder. Anticancer Res. 2002;22:1157-60. [PMID: 12168917]
20. 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;293:810-6. [PMID: 15713770]
21. 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;295:299-305. [PMID: 16418465]
22. Gudjónsson S, Isfoss BL, Hansson K, Domanski AM, Warenholt J, Soller W, et al. The value of the UroVysion assay for surveillance of non-muscle-invasive bladder cancer. Eur Urol. 2008;54:402-8. [PMID: 18082934]
23. Gupta NP, Sharma N, Kumar R. Nuclear matrix protein 22 as adjunct to urine cytology and cystoscopy in follow-up of superficial TCC of urinary bladder. Urology. 2009;73:592-6. [PMID: 19168205]
24. Gutiérrez Baños JL, Rebollo Rodrigo MH, Antolín Juárez FM, Martín García B. NMP 22, BTA stat test and cytology in the diagnosis of bladder cancer: a comparative study. Urol Int. 2001;66:185-90. [PMID: 11385303]
25. 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;167:2001-6. [PMID: 11956427]
26. Ianari A, Sternberg CN, Rossetti A, Van Rijn A, Deidda A, Giannarelli D, et al. Results of Bard BTA test in monitoring patients with a history of transitional cell cancer of the bladder. Urology. 1997;49:786-9. [PMID: 9145993]
27. 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;35:89-92. [PMID: 9933800]
28. Karnwal A, Venegas R, Shuch B, Bassett J, Rajfer J, Reznichek R. The role of fluorescence in situ hybridization assay for surveillance of non-muscle invasive bladder cancer. Can J Urol. 2010;17:5077-81. [PMID: 20398445]
29. Leyh H, Hall R, Mazeman E, Blumenstein BA. Comparison of the Bard BTA test with voided urine and bladder wash cytology in the diagnosis and management of cancer of the bladder. Urology. 1997;50:49-53. [PMID: 9218018]
30. Leyh H, Mazeman E. Bard BTA test compared with voided urine cytology in the diagnosis of recurrent bladder cancer. Eur Urol. 1997;32:425-8. [PMID: 9412800]
31. Lodde M, Mian C, Negri G, Berner L, Maffei N, Lusuardi L, et al. Role of uCyt+ in the detection and surveillance of urothelial carcinoma. Urology. 2003;61:243-7. [PMID: 12559316]
32. 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;103:1368-74. [PMID: 19338566]
33. Messing EM, Teot L, Korman H, Underhill E, Barker E, Stork B, et al. Performance of urine test in patients monitored for recurrence of bladder cancer: a multicenter study in the United States. J Urol. 2005;174:1238-41. [PMID: 16145377]
34. 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;56:228-31. [PMID: 10925083]
35. 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;161:1486-9. [PMID: 10210378]
36. Nasuti JF, Gomella LG, Ismial M, Bibbo M. Utility of the BTA stat test kit for bladder cancer screening. Diagn Cytopathol. 1999;21:27-9. [PMID: 10405804]
37. O'Sullivan P, Sharples K, Dalphin M, Davidson P, Gilling P, Cambridge L, et al. A multigene urine test for the detection and stratification of bladder cancer in patients presenting with hematuria. J Urol. 2012;188:741-7. [PMID: 22818138]
38. Paoluzzi M, Cuttano MG, Mugnaini P, Salsano F, Giannotti P. Urinary dosage of nuclear matrix protein 22 (NMP22) like biologic marker of transitional cell carcinoma (TCC): a study on patients with hematuria. Arch Ital Urol Androl. 1999;71:13-8. [PMID: 10193018]
39. 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;169:921-4. [PMID: 12576813]
40. Placer J, Espinet B, Salido M, Solé F, Gelabert-Mas A. Clinical utility of a multiprobe FISH assay in voided urine specimens for the detection of bladder cancer and its recurrences, compared with urinary cytology. Eur Urol. 2002;42:547-52. [PMID: 12477649]
41. Pode D, Shapiro A, Wald M, Nativ O, Laufer M, Kaver I. Noninvasive detection of bladder cancer with the BTA stat test. J Urol. 1999;161:443-6. [PMID: 9915422]
42. 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;166:75-8. [PMID: 11435827]
43. Quek P, Chin CM, Lim PH. The role of BTA stat in clinical practice. Ann Acad Med Singapore. 2002;31:212-6. [PMID: 11957560]
44. Raitanen MP, Leppilahti M, Tuhkanen K, Forssel T, Nylund P, Tammela T; FinnBladder Group. Routine follow-up cystoscopy in detection of recurrence in patients being monitored for bladder cancer. Ann Chir Gynaecol. 2001;90:261-5. [PMID: 11820414]
45. Saad A, Hanbury DC, McNicholas TA, Boustead GB, Morgan S, Woodman AC. A study comparing various noninvasive methods of detecting bladder cancer in urine. BJU Int. 2002;89:369-73. [PMID: 11872026]
46. Sánchez-Carbayo M, Urrutia M, Silva JM, Romaní R, De Buitrago JM, Navajo JA. Comparative predictive values of urinary cytology, urinary bladder cancer antigen, CYFRA 21-1 and NMP22 for evaluating symptomatic patients at risk for bladder cancer. J Urol. 2001;165:1462-7. [PMID: 11342897]
47. Sarosdy MF, Schellhammer P, Bokinsky G, Kahn P, Chao R, Yore L, et al. Clinical evaluation of a multi-target fluorescent in situ hybridization assay for detection of bladder cancer. J Urol. 2002;168:1950-4. [PMID: 12394683]
48. Sawczuk IS, Bagiella E, Sawczuk AT, Yun EJ. Clinical application of NMP22 in the management of transitional cell carcinoma of the bladder. Cancer Detect Prev. 2000;24:364-8. [PMID: 11059567]
49. Schamhart DH, de Reijke TM, van der Poel HG, Witjes JA, de Boer EC, Kurth K, et al. The Bard BTA test: its mode of action, sensitivity and specificity, compared to cytology of voided urine, in the diagnosis of superficial bladder cancer. Eur Urol. 1998;34:99-106. [PMID: 9693243]
50. Serretta V, Lo Presti D, Vasile P, Gange E, Esposito E, Menozzi I. Urinary NMP22 for the detection of recurrence after transurethral resection of transitional cell carcinoma of the bladder: experience on 137 patients. Urology. 1998;52:793-6. [PMID: 9801101]
51. Shariat SF, Marberger MJ, Lotan Y, Sanchez-Carbayo M, Zippe C, Lüdecke G, et al. Variability in the performance of nuclear matrix protein 22 for the detection of bladder cancer. J Urol. 2006;176:919-26. [PMID: 16890655]
52. 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;162:53-7. [PMID: 10379739]
53. The use of the bladder-tumour associated analyte test to determine the type of cystoscopy in the follow-up of patients with bladder cancer. The United Kingdom and Eire Bladder Tumour Antigen Study Group. Br J Urol. 1997;79:362-6. [PMID: 9117214]
54. 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;45:472-7. [PMID: 10102906]
55. 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;51:44-50. [PMID: 9457287]
56. Varella-Garcia M, Akduman B, Sunpaweravong P, Di Maria MV, Crawford ED. The UroVysion fluorescence in situ hybridization assay is an effective tool for monitoring recurrence of bladder cancer. Urol Oncol. 2004;22:16-9. [PMID: 14969798]
57. 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;33:387-91. [PMID: 9612682]
58. Zippe C, Pandrangi L, Potts JM, Kursh E, Novick A, Agarwal A. NMP22: a sensitive, cost-effective test in patients at risk for bladder cancer. Anticancer Res. 1999;19:2621-3. [PMID: 10470205]
59. Cha EK, Tirsar LA, Schwentner C, Christos PJ, Mian C, Hennenlotter J, et al. Immunocytology is a strong predictor of bladder cancer presence in patients with painless hematuria: a multicentre study. Eur Urol. 2012;61:185-92. [PMID: 21924544]
60. Horstmann M, Patschan O, Hennenlotter J, Senger E, Feil G, Stenzl A. Combinations of urine-based tumour markers in bladder cancer surveillance. Scand J Urol Nephrol. 2009;43:461-6. [PMID: 19903092]
61. Junker K, Fritsch T, Hartmann A, Schulze W, Schubert J. Multicolor fluorescence in situ hybridization (M-FISH) on cells from urine for the detection of bladder cancer. Cytogenet Genome Res. 2006;114:279-83. [PMID: 16954667]
62. 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;35:52-6. [PMID: 9933795]
63. Olsson H, Zackrisson B. ImmunoCyt a useful method in the follow-up protocol for patients with urinary bladder carcinoma. Scand J Urol Nephrol. 2001;35:280-2. [PMID: 11676352]
64. Piaton E, Daniel L, Verriele V, Dalifard I, Zimmermann U, Renaudin K, et al; French Prospective Multicenter Study. Improved detection of urothelial carcinomas with fluorescence immunocytochemistry (uCyt+ assay) and urinary cytology: results of a French Prospective Multicenter Study. Lab Invest. 2003;83:845-52. [PMID: 12808119]
65. Raitanen MP, Hellström P, Marttila T, Korhonen H, Talja M, Ervasti J, et al; FinnBladder Group. Effect of intravesical instillations on the human complement factor H related protein (BTA stat) test. Eur Urol. 2001;40:422-6. [PMID: 11713397]
66. Schmitz-Dräger B, Tirsar LA, Schmitz-Dräger C, Dörsam J, Bismarck E, Ebert T. Immunocytology in the assessment of patients with painless gross haematuria. BJU Int. 2008;101:455-8. [PMID: 18005211]
67. Schmitz-Dräger BJ, Beiche B, Tirsar LA, Schmitz-Dräger C, Bismarck E, Ebert T. Immunocytology in the assessment of patients with asymptomatic microhaematuria. Eur Urol. 2007;51:1582-8. [PMID: 17107748]
68. Serretta V, Pomara G, Rizzo I, Esposito E. Urinary BTA-stat, BTAtrak and NMP22 in surveillance after TUR of recurrent superficial transitional cell carcinoma of the bladder. Eur Urol. 2000;38:419-25. [PMID: 11025380]
69. Song MJ, Lee HM, Kim SH. Clinical usefulness of fluorescence in situ hybridization for diagnosis and surveillance of bladder cancer. Cancer Genet Cytogenet. 2010;198:144-50. [PMID: 20362229]
70. 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. 2009;117:167-73. [PMID: 19365828]
71. Têtu B, Tiguert R, Harel F, Fradet Y. ImmunoCyt/uCyt+ improves the sensitivity of urine cytology in patients followed for urothelial carcinoma. Mod Pathol. 2005;18:83-9. [PMID: 15389253]
72. Toma MI, Friedrich MG, Hautmann SH, Jäkel KT, Erbersdobler A, Hellstern A, et al. Comparison of the ImmunoCyt test and urinary cytology with other urine tests in the detection and surveillance of bladder cancer. World J Urol. 2004;22:145-9. [PMID: 14991320]
73. 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;58:367-71. [PMID: 11549482]
74. 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;159:1876-80. [PMID: 9598479]
75. Jaeschke R, Guyatt GH, Sackett DL. Users' guides to the medical literature. III. How to use an article about a diagnostic test. B. What are the results and will they help me in caring for my patients? The Evidence-Based Medicine Working Group. JAMA. 1994;271:703-7. [PMID: 8309035]
76. 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;61:109-18. [PMID: 12559279]
77. van Rhijn BW, van der Poel HG, van der Kwast TH. Urine markers for bladder cancer surveillance: a systematic review. Eur Urol. 2005;47:736-48. [PMID: 15925067]
78. Hajdinjak T. UroVysion FISH test for detecting urothelial cancers: meta-analysis of diagnostic accuracy and comparison with urinary cytology testing. Urol Oncol. 2008;26:646-51. [PMID: 18367109]
79. Lijmer JG, Mol BW, Heisterkamp S, Bonsel GJ, Prins MH, van der Meulen JH, et al. Empirical evidence of design-related bias in studies of diagnostic tests. JAMA. 1999;282:1061-6. [PMID: 10493205]
80. Lijmer JG, Bossuyt PM, Heisterkamp SH. Exploring sources of heterogeneity in systematic reviews of diagnostic tests. Stat Med. 2002;21:1525-37. [PMID: 12111918]
81. Gatsonis C, Paliwal P. Meta-analysis of diagnostic and screening test accuracy evaluations: methodologic primer. AJR Am J Roentgenol. 2006;187:271-81. [PMID: 16861527]
82. Macaskill P, Gatsonis C, Deeks JJ, Harbord RM, Takwoingi Y. Chapter 10: Analysing and presenting results. In: Deeks JJ, Bossuyt PM, Gatsonis C, eds. Cochrane Handbook for Systematic Reviews of Diagnostic Test Accuracy Version 1.0. The Cochrane Collaboration; 2010. Accessed at http://srdta.cochrane.org on 5 October 2015.
83. Ru Y, Dancik GM, Theodorescu D. Biomarkers for prognosis and treatment selection in advanced bladder cancer patients. Curr Opin Urol. 2011;21:420-7. [PMID: 21814055]
84. Lotan Y, Shariat SF, Schmitz-Dräger BJ, Sanchez-Carbayo M, Jankevicius F, Racioppi M, et al. Considerations on implementing diagnostic markers into clinical decision making in bladder cancer. Urol Oncol. 2010;28:441-8. [PMID: 20610281] doi:10.1016/j.urolonc.2009.11.004