Cited by 690Cancer Genomics and DiagnosticsColorectal Cancer Treatments and StudiesColorectal Cancer Surgical Treatments

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Circulating Tumor DNA Analyses as Markers of Recurrence Risk and Benefit of Adjuvant Therapy for Stage III Colon Cancer

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Tie, Jeanne, Cohen, Joshua D., Wang, Yuxuan, Christie, Michael, Simons, Koen, Lee, Margaret, Wong, Rachel, Kosmider, Suzanne, Ananda, Sumitra, McKendrick, Joseph, Lee, Belinda, Cho, Jin Hee, Faragher, Ian, Jones, Ian T., Ptak, Janine, Schaeffer, Mary J., Silliman, Natalie, Dobbyn, Lisa, Li, Lu, Tomasetti, Cristian, Papadopoulos, Nicholas, Kinzler, Kenneth W., Vogelstein, Bert, Gibbs, Peter·2019·JAMA Oncology

DOI 10.1001/jamaoncol.2019.3616PMC PMC6802034

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Abstract

Importance: Adjuvant chemotherapy in patients with stage III colon cancer prevents recurrence by eradicating minimal residual disease. However, which patients remain at high risk of recurrence after completing standard adjuvant treatment cannot currently be determined. Postsurgical circulating tumor DNA (ctDNA) analysis can detect minimal residual disease and is associated with recurrence in colorectal cancers. Objective: To determine whether serial postsurgical and postchemotherapy ctDNA analysis could provide a real-time indication of adjuvant therapy efficacy in stage III colon cancer. Design, Setting, and Participants: This multicenter, Australian, population-based cohort biomarker study recruited 100 consecutive patients with newly diagnosed stage III colon cancer planned for 24 weeks of adjuvant chemotherapy from November 1, 2014, through May 31, 2017. Patients with another malignant neoplasm diagnosed within the last 3 years were excluded. Median duration of follow-up was 28.9 months (range, 11.6-46.4 months). Physicians were blinded to ctDNA results. Data were analyzed from December 10, 2018, through June 23, 2019. Exposures: Serial plasma samples were collected after surgery and after chemotherapy. Somatic mutations in individual patients' tumors were identified via massively parallel sequencing of 15 genes commonly mutated in colorectal cancer. Personalized assays were designed to quantify ctDNA. Main Outcomes and Measures: Detection of ctDNA and recurrence-free interval (RFI). Results: After 4 exclusions, 96 eligible patients were eligible; median patient age was 64 years (range, 26-82 years); 49 (51%) were men. At least 1 somatic mutation was identified in the tumor tissue of all 96 evaluable patients. Circulating tumor DNA was detectable in 20 of 96 (21%) postsurgical samples and was associated with inferior recurrence-free survival (hazard ratio [HR], 3.8; 95% CI, 2.4-21.0; P < .001). Circulating tumor DNA was detectable in 15 of 88 (17%) postchemotherapy samples. The estimated 3-year RFI was 30% when ctDNA was detectable after chemotherapy and 77% when ctDNA was undetectable (HR, 6.8; 95% CI, 11.0-157.0; P < .001). Postsurgical ctDNA status remained independently associated with RFI after adjusting for known clinicopathologic risk factors (HR, 7.5; 95% CI, 3.5-16.1; P < .001). Conclusions and Relevance: Results suggest that ctDNA analysis after surgery is a promising prognostic marker in stage III colon cancer. Postchemotherapy ctDNA analysis may define a patient subset that remains at high risk of recurrence despite completing standard adjuvant treatment. This high-risk population presents a unique opportunity to explore additional therapeutic approaches.

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Authors: Tie, J., Cohen, J. D., Wang, Y., Christie, M., Simons, K., Lee, M., Wong, R., Kosmider, S., Ananda, S., McKendrick, J., Lee, B., Cho, J. H., Faragher, I., Jones, I. T., Ptak, J., Schaeffer, M. J., Silliman, N., Dobbyn, L., Li, L., Tomasetti, C., Papadopoulos, N., Kinzler, K. W., Vogelstein, B., & Gibbs, P.
Affiliations: The University of Melbourne (AU)
Johns Hopkins University (US)
The Royal Melbourne Hospital (AU)
Walter and Eliza Hall Institute of Medical Research (AU)
Western Health (AU)
Eastern Health (AU)
Division of Biostatistics & Bioinformatics, Department of Oncology, Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins University School of Medicine, Baltimore, Maryland
Ludwig Center for Cancer Genetics and Therapeutics, Johns Hopkins University School of Medicine, Baltimore, Maryland
Corresponding author: Tie, Jeanne
ORCID: Tie, Jeanne
Cohen, Joshua D.
Wang, Yuxuan
Christie, Michael
Simons, Koen
Wong, Rachel
Kosmider, Suzanne
Lee, Belinda
Cho, Jin Hee
Faragher, Ian
Jones, Ian T.
Ptak, Janine
Silliman, Natalie
Dobbyn, Lisa
Tomasetti, Cristian
Kinzler, Kenneth W.
Vogelstein, Bert
Gibbs, Peter
Venue: JAMA Oncology
Publisher: American Medical Association (AMA)
Published: 2019-12-01
Volume: 5
Issue: 12
Pages: 1710
ISSN: 2374-2437 (ISSN-L)
DOI: 10.1001/jamaoncol.2019.3616
PMC: PMC6802034
OpenAlex: W2980567593
Cited by: 668
References: 28
Citations by year: 2026: 76 · 2025: 91 · 2024: 104 · 2023: 124 · 2022: 107 · 2021: 102 · 2020: 57 · 2019: 6
FWCI: 21.84
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: JAMA Oncology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Cancer Institute (P50CA062924)
National Institute of General Medical Sciences (T32GM136577)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
Health Sciences › Medicine › Oncology › Colorectal Cancer Surgical Treatments
Keywords: circulating tumor DNA, stage III colon cancer, adjuvant chemotherapy, recurrence risk, minimal residual disease, recurrence-free interval, somatic mutations, liquid biopsy, predictive biomarkers, treatment response monitoring, recurrent colorectal cancer, recurrence-free survival, prognostic factors
MeSH terms: Circulating Tumor DNA, Adult, Aged, Aged, 80 and over, Australia, Colonic Neoplasms, Female, Humans, Male, Middle Aged, Mutation, Neoplasm Staging, Prognosis, Risk Factors, Biomarkers, Tumor, Treatment Outcome, Chemotherapy, Adjuvant, Neoplasm, Residual, Disease-Free Survival, Precision Medicine, High-Throughput Nucleotide Sequencing

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Circulating Tumor DNA Analyses as Markers of Recurrence Risk and Benefit of Adjuvant Therapy for Stage III Colon Cancer

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