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Predictive Biomarkers and Personalized Medicine

A Panel of Three Markers Hyper- and Hypomethylated in Urine Sediments Accurately Predicts Bladder Cancer Recurrence

Sheng-Fang Su, André Luís de Castro Abreu, Yoshitomo Chihara, Yvonne Tsai, Claudia Andreu-Vieyra, Siamak Daneshmand, Eila C. Skinner, Peter A. Jones, Kimberly D. Siegmund and Gangning Liang
Sheng-Fang Su
Departments of 1Urology and 2Preventive Medicine; 3Program in Genetic, Molecular, and Cellular Biology, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles; and 4Department of Urology, School of Medicine, University of Stanford, Stanford, California
Departments of 1Urology and 2Preventive Medicine; 3Program in Genetic, Molecular, and Cellular Biology, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles; and 4Department of Urology, School of Medicine, University of Stanford, Stanford, California
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André Luís de Castro Abreu
Departments of 1Urology and 2Preventive Medicine; 3Program in Genetic, Molecular, and Cellular Biology, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles; and 4Department of Urology, School of Medicine, University of Stanford, Stanford, California
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Yoshitomo Chihara
Departments of 1Urology and 2Preventive Medicine; 3Program in Genetic, Molecular, and Cellular Biology, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles; and 4Department of Urology, School of Medicine, University of Stanford, Stanford, California
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Yvonne Tsai
Departments of 1Urology and 2Preventive Medicine; 3Program in Genetic, Molecular, and Cellular Biology, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles; and 4Department of Urology, School of Medicine, University of Stanford, Stanford, California
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Claudia Andreu-Vieyra
Departments of 1Urology and 2Preventive Medicine; 3Program in Genetic, Molecular, and Cellular Biology, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles; and 4Department of Urology, School of Medicine, University of Stanford, Stanford, California
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Siamak Daneshmand
Departments of 1Urology and 2Preventive Medicine; 3Program in Genetic, Molecular, and Cellular Biology, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles; and 4Department of Urology, School of Medicine, University of Stanford, Stanford, California
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Eila C. Skinner
Departments of 1Urology and 2Preventive Medicine; 3Program in Genetic, Molecular, and Cellular Biology, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles; and 4Department of Urology, School of Medicine, University of Stanford, Stanford, California
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Peter A. Jones
Departments of 1Urology and 2Preventive Medicine; 3Program in Genetic, Molecular, and Cellular Biology, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles; and 4Department of Urology, School of Medicine, University of Stanford, Stanford, California
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Kimberly D. Siegmund
Departments of 1Urology and 2Preventive Medicine; 3Program in Genetic, Molecular, and Cellular Biology, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles; and 4Department of Urology, School of Medicine, University of Stanford, Stanford, California
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Gangning Liang
Departments of 1Urology and 2Preventive Medicine; 3Program in Genetic, Molecular, and Cellular Biology, USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles; and 4Department of Urology, School of Medicine, University of Stanford, Stanford, California
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DOI: 10.1158/1078-0432.CCR-13-2637 Published April 2014
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Abstract

Purpose: The high risk of recurrence after transurethral resection of bladder tumor of nonmuscle invasive disease requires lifelong treatment and surveillance. Changes in DNA methylation are chemically stable, occur early during tumorigenesis, and can be quantified in bladder tumors and in cells shed into the urine. Some urine markers have been used to help detect bladder tumors; however, their use in longitudinal tumor recurrence surveillance has yet to be established.

Experimental Design: We analyzed the DNA methylation levels of six markers in 368 urine sediment samples serially collected from 90 patients with noninvasive urothelial carcinoma (Tis, Ta, T1; grade low-high). The optimum marker combination was identified using logistic regression with 5-fold cross-validation, and validated in separate samples.

Results: A panel of three markers discriminated between patients with and without recurrence with the area under the curve of 0.90 [95% confidence interval (CI), 0.86–0.92] and 0.95 (95% CI, 0.90–1.00), sensitivity and specificity of 86%/89% (95% CI, 74%–99% and 81%–97%) and 80%/97% (95% CI, 60%–96% and 91%–100%) in the testing and validation sets, respectively. The three-marker DNA methylation test reliably predicted tumor recurrence in 80% of patients superior to cytology (35%) and cystoscopy (15%) while accurately forecasting no recurrence in 74% of patients that scored negative in the test.

Conclusions: Given their superior sensitivity and specificity in urine sediments, a combination of hyper- and hypomethylated markers may help avoid unnecessary invasive exams and reveal the importance of DNA methylation in bladder tumorigenesis. Clin Cancer Res; 20(7); 1978–89. ©2014 AACR.

This article is featured in Highlights of This Issue, p. 1707

Footnotes

  • Note: Supplementary data for this article are available at Clinical Cancer Research online (http://clincancerres.aacrjournals.org/).

  • Received September 27, 2013.
  • Revision received December 19, 2013.
  • Accepted January 9, 2014.
  • ©2014 American Association for Cancer Research.
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Clinical Cancer Research: 20 (7)
April 2014
Volume 20, Issue 7
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A Panel of Three Markers Hyper- and Hypomethylated in Urine Sediments Accurately Predicts Bladder Cancer Recurrence
Sheng-Fang Su, André Luís de Castro Abreu, Yoshitomo Chihara, Yvonne Tsai, Claudia Andreu-Vieyra, Siamak Daneshmand, Eila C. Skinner, Peter A. Jones, Kimberly D. Siegmund and Gangning Liang
Clin Cancer Res April 1 2014 (20) (7) 1978-1989; DOI: 10.1158/1078-0432.CCR-13-2637

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A Panel of Three Markers Hyper- and Hypomethylated in Urine Sediments Accurately Predicts Bladder Cancer Recurrence
Sheng-Fang Su, André Luís de Castro Abreu, Yoshitomo Chihara, Yvonne Tsai, Claudia Andreu-Vieyra, Siamak Daneshmand, Eila C. Skinner, Peter A. Jones, Kimberly D. Siegmund and Gangning Liang
Clin Cancer Res April 1 2014 (20) (7) 1978-1989; DOI: 10.1158/1078-0432.CCR-13-2637
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