Ultrasensitive plasma-based monitoring of tumor burden using machine-learning-guided signal enrichment

Adam J. Widman(Memorial Sloan Kettering Cancer Center), Minita Shah(New York Genome Center), Amanda Frydendahl(Aarhus University), Daniel Halmos(Cornell University), Cole C. Khamnei(Cornell University), Nadia Øgaard(Aarhus University), Srinivas Rajagopalan(Cornell University), Anushri Arora(Cornell University), Aditya Deshpande(Cornell University), William F. Hooper(New York Genome Center), Jean Quentin(Cornell University), Jake Bass(Cornell University), Mingxuan Zhang(Cornell University), Theophile Langanay(Cornell University), Laura Andersen(Aarhus University), Zoe Steinsnyder(New York Genome Center), Will Liao(New York Genome Center), Mads H. Rasmussen(Aarhus University), Tenna Vesterman Henriksen(Aarhus University), Sarah Østrup Jensen(Aarhus University), Jesper Nors(Aarhus University), Christina Therkildsen(Hvidovre Hospital), Jesús Alfonso López Sotélo(Cornell University), Ryan Brand(Cornell University), Joshua S. Schiffman(Cornell University), Ronak Shah(Memorial Sloan Kettering Cancer Center), Alexandre Pellan Cheng(Cornell University), Colleen Maher(Memorial Sloan Kettering Cancer Center), Lavinia Spain(Royal Marsden NHS Foundation Trust), Kate Krause(Massachusetts General Hospital), Dennie T. Frederick(Massachusetts General Hospital), Wendie Den Brok(BC Cancer Agency), Caroline Lohrisch(BC Cancer Agency), Tamara Shenkier(BC Cancer Agency), Christine Simmons(BC Cancer Agency), Diego Villa(BC Cancer Agency), Andrew J. Mungall(Canada's Michael Smith Genome Sciences Centre), Richard A. Moore(Canada's Michael Smith Genome Sciences Centre), Elena Zaikova(BC Cancer Agency), Viviana Cerda(BC Cancer Agency), Esther Kong(BC Cancer Agency), Daniel Lai(BC Cancer Agency), Murtaza Malbari(Cornell University), Melissa Marton(New York Genome Center), Dina Manaa(New York Genome Center), Lara Winterkorn(New York Genome Center), Karen A. Gelmon(BC Cancer Agency), Margaret K. Callahan(Memorial Sloan Kettering Cancer Center), Genevieve M. Boland(Massachusetts General Hospital), Catherine Potenski(Cornell University), Jedd D. Wolchok(Memorial Sloan Kettering Cancer Center), Ashish Saxena(Cornell University), Samra Turajlic(Royal Marsden NHS Foundation Trust), Marcin Imieliński(New York Genome Center), Michael F. Berger(Memorial Sloan Kettering Cancer Center), Samuel Aparício(BC Cancer Agency), Nasser K. Altorki(Cornell University), Michael A. Postow(Memorial Sloan Kettering Cancer Center), Nicolas Robine(New York Genome Center), Claus L. Andersen(Aarhus University), Dan A. Landau(Cornell University)
Nature Medicine
June 1, 2024
Cited by 93Open Access
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Abstract

In solid tumor oncology, circulating tumor DNA (ctDNA) is poised to transform care through accurate assessment of minimal residual disease (MRD) and therapeutic response monitoring. To overcome the sparsity of ctDNA fragments in low tumor fraction (TF) settings and increase MRD sensitivity, we previously leveraged genome-wide mutational integration through plasma whole-genome sequencing (WGS). Here we now introduce MRD-EDGE, a machine-learning-guided WGS ctDNA single-nucleotide variant (SNV) and copy-number variant (CNV) detection platform designed to increase signal enrichment. MRD-EDGESNV uses deep learning and a ctDNA-specific feature space to increase SNV signal-to-noise enrichment in WGS by ~300× compared to previous WGS error suppression. MRD-EDGECNV also reduces the degree of aneuploidy needed for ultrasensitive CNV detection through WGS from 1 Gb to 200 Mb, vastly expanding its applicability within solid tumors. We harness the improved performance to identify MRD following surgery in multiple cancer types, track changes in TF in response to neoadjuvant immunotherapy in lung cancer and demonstrate ctDNA shedding in precancerous colorectal adenomas. Finally, the radical signal-to-noise enrichment in MRD-EDGESNV enables plasma-only (non-tumor-informed) disease monitoring in advanced melanoma and lung cancer, yielding clinically informative TF monitoring for patients on immune-checkpoint inhibition. Detection of circulating tumor DNA using MRD-EDGE, a machine-learning-guided single-nucleotide variant and copy-number variant detection platform for signal enrichment, enables monitoring of minimal residual disease and immunotherapy response in settings of low tumor burden.


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