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Clinical Cancer Research
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Precision Medicine and Imaging

Noninvasive Detection of Urothelial Carcinoma by Cost-effective Low-coverage Whole-genome Sequencing from Urine-Exfoliated Cell DNA

Shuxiong Zeng, Yidie Ying, Naidong Xing, Baiyun Wang, Ziliang Qian, Zunlin Zhou, Zhensheng Zhang, Weidong Xu, Huiqing Wang, Lihe Dai, Li Gao, Tie Zhou, Jiatao Ji and Chuanliang Xu
Shuxiong Zeng
1Department of Urology, Changhai Hospital, Naval Medical University, Shanghai, China.
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Yidie Ying
1Department of Urology, Changhai Hospital, Naval Medical University, Shanghai, China.
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  • ORCID record for Yidie Ying
Naidong Xing
2Department of Urology, Qilu Hospital of Shandong University, Jinan, Shandong, China.
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Baiyun Wang
3Suzhou Hongyuan Biotech Inc., Biobay, Suzhou, China.
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Ziliang Qian
3Suzhou Hongyuan Biotech Inc., Biobay, Suzhou, China.
4Prophet Genomics Inc., San Jose, California.
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Zunlin Zhou
2Department of Urology, Qilu Hospital of Shandong University, Jinan, Shandong, China.
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Zhensheng Zhang
1Department of Urology, Changhai Hospital, Naval Medical University, Shanghai, China.
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Weidong Xu
1Department of Urology, Changhai Hospital, Naval Medical University, Shanghai, China.
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Huiqing Wang
1Department of Urology, Changhai Hospital, Naval Medical University, Shanghai, China.
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Lihe Dai
1Department of Urology, Changhai Hospital, Naval Medical University, Shanghai, China.
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Li Gao
5Department of Pathology, Changhai Hospital, Naval Medical University, Shanghai, China.
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Tie Zhou
1Department of Urology, Changhai Hospital, Naval Medical University, Shanghai, China.
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Jiatao Ji
6Department of Urology, Shanghai Hudong Hospital, Pudong New Area, Shanghai, China.
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  • For correspondence: drxuchuanliang@126.com jijiatao22@163.com
Chuanliang Xu
1Department of Urology, Changhai Hospital, Naval Medical University, Shanghai, China.
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  • For correspondence: drxuchuanliang@126.com jijiatao22@163.com
DOI: 10.1158/1078-0432.CCR-20-0401 Published November 2020
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Abstract

Purpose: Urothelial carcinoma is a malignant cancer with frequent chromosomal aberrations. Here, we investigated the application of a cost-effective, low-coverage whole-genome sequencing technology in detecting all chromosomal aberrations.

Experimental Design: Patients with urothelial carcinomas and nontumor controls were prospectively recruited in clinical trial NCT03998371. Urine-exfoliated cell DNA was analyzed by Illumina HiSeq XTen, followed by genotyping with a customized bioinformatics workflow named Urine Exfoliated Cells Copy Number Aberration Detector (UroCAD).

Results: In the discovery phase, urine samples from 126 patients with urothelial carcinomas and 64 nontumor disease samples were analyzed. Frequent chromosome copy-number changes were found in patients with tumor as compared with nontumor controls. A novel diagnosis model, UroCAD, was built by incorporating all the autosomal chromosomal changes. The model reached performance of AUC = 0.92 (95% confidence interval, 89.4%–97.3%). At the optimal cutoff, |Z| ≥ 3.21, the sensitivity, specificity, and accuracy were 82.5%, 96.9%, and 89.0%, respectively. The prediction positivity was found correlated with tumor grade (P = 0.01). In the external validation cohort of 95 participants, the UroCAD assay identified urothelial carcinomas with an overall sensitivity of 80.4%, specificity of 94.9%, and AUC of 0.91. Meanwhile, UroCAD assay outperformed cytology tests with significantly improved sensitivity (80.4% vs. 33.9%; P < 0.001) and comparable specificity (94.9% vs. 100%; P = 0.49).

Conclusions: UroCAD could be a robust urothelial carcinoma diagnostic method with improved sensitivity and similar specificity as compared with cytology tests. It may be used as a noninvasive approach for diagnosis and recurrence surveillance in urothelial carcinoma prior to the use of cystoscopy, which would largely reduce the burden on patients.

Footnotes

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

  • Clin Cancer Res 2020;26:5646–54

  • Received January 31, 2020.
  • Revision received May 28, 2020.
  • Accepted August 12, 2020.
  • Published first October 9, 2020.
  • ©2020 American Association for Cancer Research.
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Clinical Cancer Research: 26 (21)
November 2020
Volume 26, Issue 21
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Noninvasive Detection of Urothelial Carcinoma by Cost-effective Low-coverage Whole-genome Sequencing from Urine-Exfoliated Cell DNA
Shuxiong Zeng, Yidie Ying, Naidong Xing, Baiyun Wang, Ziliang Qian, Zunlin Zhou, Zhensheng Zhang, Weidong Xu, Huiqing Wang, Lihe Dai, Li Gao, Tie Zhou, Jiatao Ji and Chuanliang Xu
Clin Cancer Res November 1 2020 (26) (21) 5646-5654; DOI: 10.1158/1078-0432.CCR-20-0401

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Noninvasive Detection of Urothelial Carcinoma by Cost-effective Low-coverage Whole-genome Sequencing from Urine-Exfoliated Cell DNA
Shuxiong Zeng, Yidie Ying, Naidong Xing, Baiyun Wang, Ziliang Qian, Zunlin Zhou, Zhensheng Zhang, Weidong Xu, Huiqing Wang, Lihe Dai, Li Gao, Tie Zhou, Jiatao Ji and Chuanliang Xu
Clin Cancer Res November 1 2020 (26) (21) 5646-5654; DOI: 10.1158/1078-0432.CCR-20-0401
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