Genomic Heterogeneity as a Barrier to Precision Medicine in Gastroesophageal Adenocarcinoma
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Abstract
Gastroesophageal adenocarcinoma (GEA) is a lethal disease where targeted therapies, even when guided by genomic biomarkers, have had limited efficacy. A potential reason for the failure of such therapies is that genomic profiling results could commonly differ between the primary and metastatic tumors. To evaluate genomic heterogeneity, we sequenced paired primary GEA and synchronous metastatic lesions across multiple cohorts, finding extensive differences in genomic alterations, including discrepancies in potentially clinically relevant alterations. Multiregion sequencing showed significant discrepancy within the primary tumor (PT) and between the PT and disseminated disease, with oncogene amplification profiles commonly discordant. In addition, a pilot analysis of cell-free DNA (cfDNA) sequencing demonstrated the feasibility of detecting genomic amplifications not detected in PT sampling. Lastly, we profiled paired primary tumors, metastatic tumors, and cfDNA from patients enrolled in the personalized antibodies for GEA (PANGEA) trial of targeted therapies in GEA and found that genomic biomarkers were recurrently discrepant between the PT and untreated metastases. Divergent primary and metastatic tissue profiling led to treatment reassignment in 32% (9/28) of patients. In discordant primary and metastatic lesions, we found 87.5% concordance for targetable alterations in metastatic tissue and cfDNA, suggesting the potential for cfDNA profiling to enhance selection of therapy. Significance: We demonstrate frequent baseline heterogeneity in targetable genomic alterations in GEA, indicating that current tissue sampling practices for biomarker testing do not effectively guide precision medicine in this disease and that routine profiling of metastatic lesions and/or cfDNA should be systematically evaluated. Cancer Discov; 8(1); 37–48. ©2017 AACR. See related commentary by Sundar and Tan, p. 14. See related article by Janjigian et al., p. 49. This article is highlighted in the In This Issue feature, p. 1
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Heterogeneity, or diverse cell populations within diseased tissue, is the leading cause of treatment failure for many complex diseases and a major obstacle to precision medicine.
“Heterogeneity, or more specifically, the diverse cell populations within the diseased tissue, is the leading cause of treatment failure for many complex diseases, such as cancers1, Alzheimer’s disease2, stroke3, and coronavirus disease 2019 (COVID-19)4, etc., as well as a major obstacle to successful precision medicine5–7.”
From ASGARD is a single-cell guided pipeline to aid repurposing of drugs (2023) · cites this paper as [5]
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- Authors
- Pectasides, E., Stachler, M. D., Derks, S., Liu, Y., Maron, S., Islam, M., Alpert, L., Kwak, H., Kindler, H., Polite, B., Sharma, M. R., Allen, K., O'Day, E., Lomnicki, S., Maranto, M., Kanteti, R., Fitzpatrick, C., Weber, C., Setia, N., Xiao, S.-Y., Hart, J., Nagy, R. J., Kim, K.-M., Choi, M.-G., Min, B.-H., Nason, K. S., O'Keefe, L., Watanabe, M., Baba, H., Lanman, R., Agoston, A. T., Oh, D. J., Dunford, A., Thorner, A. R., Ducar, M. D., Wollison, B. M., Coleman, H. A., Ji, Y., Posner, M. C., Roggin, K., Turaga, K., Chang, P., Hogarth, K., Siddiqui, U., Gelrud, A., Ha, G., Freeman, S. S., Rhoades, J., Reed, S., Gydush, G., Rotem, D., Davison, J., Imamura, Y., Adalsteinsson, V., Lee, J., Bass, A. J., & Catenacci, D. V.
- Affiliations
- Beth Israel Deaconess Medical Center (US)
- Brigham and Women's Hospital (US)
- 1Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts.
- Broad Institute (US)
- University of Chicago Medical Center (US)
- 6Department of Medicine, Section of Hematology/Oncology, University of Chicago Medical Center and Biological Sciences, Chicago, Illinois.
- Guardant (United States) (US)
- Samsung Medical Center (KR)
- University of Pittsburgh (US)
- The Cancer Institute Hospital (JP)
- Kumamoto University (JP)
- University of New England (US)
- Dana-Farber Cancer Institute (US)
- 21Department of Medicine, Section of Gastroenterology, University of Chicago Medical Center and Biological Sciences, Chicago, Illinois.
- Corresponding author
- Bass, Adam J.
- Catenacci, Daniel V.
- ORCID
- Stachler, Matthew D.
- Maron, Steven
- Islam, Mirazul
- Alpert, Lindsay
- Kindler, Hedy
- Sharma, Manish R.
- Fitzpatrick, Carrie
- Weber, Christopher
- Setia, Namrata
- Xiao, Shu-Yuan
- Hart, John
- Nagy, Rebecca J.
- Kim, Kyoung-Mee
- Choi, Min-Gew
- Min, Byung-Hoon
- Watanabe, Masayuki
- Baba, Hideo
- Agoston, Agoston T.
- Oh, David J.
- Dunford, Andrew
- Thorner, Aaron R.
- Ducar, Matthew D.
- Wollison, Bruce M.
- Ji, Yuan
- Posner, Mitchell C.
- Roggin, Kevin
- Turaga, Kiran
- Chang, Paul
- Siddiqui, Uzma
- Ha, Gavin
- Freeman, Samuel S.
- Rhoades, Justin
- Reed, Sarah
- Rotem, Denisse
- Davison, Jon
- Imamura, Yu
- Adalsteinsson, Viktor
- Lee, Jeeyun
- Bass, Adam J.
- Catenacci, Daniel V.
- Venue
- Cancer Discovery
- Published
- 2018-01-01
- Volume
- 8
- Issue
- 1
- Pages
- 37-48
- ISSN
- 2159-8274 (ISSN-L)
- 2159-8290
- PMC
- PMC5894850
- OpenAlex
- W2763498516
- Cited by
- 307
- References
- 56
- Citations by year
- 2026: 18 · 2025: 19 · 2024: 19 · 2023: 40 · 2022: 51 · 2021: 44 · 2020: 48 · 2019: 41 · 2018: 27
- FWCI
- 10.63
- Type
- journal article
- Language
- en
- Open access
- green
- pure.amsterdamumc.nl
- Licence
- other-oa
- Locations
- Cancer Discovery (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, other-oa)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion, other-oa)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Funders
- National Institutes of Health (KL2TR001100)
- Japan Society for the Promotion of Science (17K19619)
- National Cancer Institute (P50CA127003, P01CA098101, K23CA178203, R01CA196932, P30CA014599)
- National Institute of General Medical Sciences (T32GM007748)
- National Institute of Diabetes and Digestive and Kidney Diseases (K08DK109209)
- National Center for Advancing Translational Sciences
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Health Sciences › Medicine › Surgery › Esophageal Cancer Research and Treatment
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Lung Cancer Treatments and Mutations
- Keywords
- gastroesophageal adenocarcinoma, tumor genomic heterogeneity, cell-free DNA, oncogene amplification, targeted therapy selection, precision medicine, biomarker testing, tissue sampling
- MeSH terms
- Exome Sequencing, Adenocarcinoma, Esophageal Neoplasms, Humans, Stomach Neoplasms, Cohort Studies, Genomics, Precision Medicine
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