Cited by 294Cancer Genomics and DiagnosticsLung Cancer Treatments and MutationsBRCA gene mutations in cancer

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Molecular Landscape and Actionable Alterations in a Genomically Guided Cancer Clinical Trial: National Cancer Institute Molecular Analysis for Therapy Choice (NCI-MATCH)

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Flaherty, Keith T., Gray, Robert J., Chen, Alice P., Li, Shuli, McShane, Lisa M., Patton, David, Hamilton, Stanley R., Williams, P. Mickey, Iafrate, A. John, Sklar, Jeffrey, Mitchell, Edith P., Harris, Lyndsay N., Takebe, Naoko, Sims, David J., Coffey, Brent, Fu, Tony, Routbort, Mark, Zwiebel, James A., Rubinstein, Larry V., Little, Richard F., Arteaga, Carlos L., Comis, Robert, Abrams, Jeffrey S., O’Dwyer, Peter J., Conley, Barbara A., for the NCI-MATCH team·2020·Journal of Clinical Oncology

DOI 10.1200/jco.19.03010PMC PMC7676882

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Abstract

PURPOSE: Therapeutically actionable molecular alterations are widely distributed across cancer types. The National Cancer Institute Molecular Analysis for Therapy Choice (NCI-MATCH) trial was designed to evaluate targeted therapy antitumor activity in underexplored cancer types. Tumor biopsy specimens were analyzed centrally with next-generation sequencing (NGS) in a master screening protocol. Patients with a tumor molecular alteration addressed by a targeted treatment lacking established efficacy in that tumor type were assigned to 1 of 30 treatments in parallel, single-arm, phase II subprotocols. PATIENTS AND METHODS: Tumor biopsy specimens from 5,954 patients with refractory malignancies at 1,117 accrual sites were analyzed centrally with NGS and selected immunohistochemistry in a master screening protocol. The treatment-assignment rate to treatment arms was assessed. Molecular alterations in seven tumors profiled in both NCI-MATCH trial and The Cancer Genome Atlas (TCGA) of primary tumors were compared. RESULTS: Molecular profiling was successful in 93.0% of specimens. An actionable alteration was found in 37.6%. After applying clinical and molecular exclusion criteria, 17.8% were assigned (26.4% could have been assigned if all subprotocols were available simultaneously). Eleven subprotocols reached their accrual goal as of this report. Actionability rates differed among histologies (eg, > 35% for urothelial cancers and < 6% for pancreatic and small-cell lung cancer). Multiple actionable or resistance-conferring tumor mutations were seen in 11.9% and 71.3% of specimens, respectively. Known resistance mutations to targeted therapies were numerically more frequent in NCI-MATCH than TCGA tumors, but not markedly so. CONCLUSION: We demonstrated feasibility of screening large numbers of patients at numerous accruing sites in a complex trial to test investigational therapies for moderately frequent molecular targets. Co-occurring resistance mutations were common and endorse investigation of combination targeted-therapy regimens.

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Self-citation

Authors: Flaherty, K. T., Gray, R. J., Chen, A. P., Li, S., McShane, L. M., Patton, D., Hamilton, S. R., Williams, P. M., Iafrate, A. J., Sklar, J., Mitchell, E. P., Harris, L. N., Takebe, N., Sims, D. J., Coffey, B., Fu, T., Routbort, M., Zwiebel, J. A., Rubinstein, L. V., Little, R. F., Arteaga, C. L., Comis, R., Abrams, J. S., O’Dwyer, P. J., Conley, B. A., & for the NCI-MATCH team
Affiliations: Massachusetts General Hospital (US)
Dana-Farber Cancer Institute (US)
National Institutes of Health (US)
The University of Texas MD Anderson Cancer Center (US)
Frederick National Laboratory for Cancer Research (US)
Harvard University (US)
Yale University (US)
Thomas Jefferson University Hospital (US)
Harold C. Simmons Comprehensive Cancer Center (US)
ECOG-ACRIN Cancer Research Group (US)
Division of Cancer Treatment and Diagnosis, National Cancer Institute (NCI), National Institutes of Health (NIH), Bethesda, MD
Corresponding author: Flaherty, Keith T.
ORCID: Flaherty, Keith T.
Gray, Robert J.
Chen, Alice P.
Li, Shuli
McShane, Lisa M.
Patton, David
Hamilton, Stanley R.
Williams, P. Mickey
Iafrate, A. John
Sklar, Jeffrey
Mitchell, Edith P.
Harris, Lyndsay N.
Takebe, Naoko
Coffey, Brent
Routbort, Mark
Zwiebel, James A.
Rubinstein, Larry V.
Little, Richard F.
Arteaga, Carlos L.
Abrams, Jeffrey S.
Conley, Barbara A.
Venue: Journal of Clinical Oncology
Publisher: American Society of Clinical Oncology (ASCO)
Published: 2020-11-20
Volume: 38
Issue: 33
Pages: 3883-3894
ISSN: 0732-183X (ISSN-L)
1527-7755
DOI: 10.1200/jco.19.03010
PMC: PMC7676882
OpenAlex: W3092241364
Cited by: 294
References: 27
Citations by year: 2026: 35 · 2025: 41 · 2024: 51 · 2023: 68 · 2022: 55 · 2021: 41 · 2020: 3
FWCI: 14.31
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
Locations: Journal of Clinical Oncology (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
The Medicine Forum (submittedVersion, cc-by)
Funders: National Cancer Institute (U10CA180820, UG1CA233337, UG1CA233329, UG1CA233180, UG1CA233341, U10CA180794, UG1CA233302, U24CA196172)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Lung Cancer Treatments and Mutations
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › BRCA gene mutations in cancer
Keywords: NCI-MATCH trial, actionable molecular alterations, targeted therapy, molecular profiling, next-generation sequencing, resistance mutations, combination targeted therapy, refractory cancer, urothelial carcinoma, pancreatic cancer, small cell lung cancer
MeSH terms: Adolescent, Adult, Aged, Antineoplastic Agents, Antineoplastic Combined Chemotherapy Protocols, Biopsy, Female, Humans, Male, Middle Aged, Neoplasms, Disease Progression, Young Adult, High-Throughput Nucleotide Sequencing

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Molecular Landscape and Actionable Alterations in a Genomically Guided Cancer Clinical Trial: National Cancer Institute Molecular Analysis for Therapy Choice (NCI-MATCH)

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