Tracking tumour evolution in glioma through liquid biopsies of cerebrospinal fluid

Diffuse gliomas are the most common malignant brain tumours in adults and include glioblastomas and World Health Organization (WHO) grade II and grade III tumours (sometimes referred to as lower-grade gliomas). Genetic tumour profiling is used to classify disease and guide therapy 1 , 2 , but involv...

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Published in:Nature (London) Vol. 565; no. 7741; pp. 654 - 658
Main Authors: Miller, Alexandra M., Shah, Ronak H., Pentsova, Elena I., Pourmaleki, Maryam, Briggs, Samuel, Distefano, Natalie, Zheng, Youyun, Skakodub, Anna, Mehta, Smrutiben A., Campos, Carl, Hsieh, Wan-Ying, Selcuklu, S. Duygu, Ling, Lilan, Meng, Fanli, Jing, Xiaohong, Samoila, Aliaksandra, Bale, Tejus A., Tsui, Dana W. Y., Grommes, Christian, Viale, Agnes, Souweidane, Mark M., Tabar, Viviane, Brennan, Cameron W., Reiner, Anne S., Rosenblum, Marc, Panageas, Katherine S., DeAngelis, Lisa M., Young, Robert J., Berger, Michael F., Mellinghoff, Ingo K.
Format: Journal Article
Language:English
Published: London Nature Publishing Group UK 01.01.2019
Nature Publishing Group
Subjects:
631/1647/2217
631/67/1922
Adults
Analysis
Biopsy
Blood circulation
Brain
Brain cancer
Brain tumors
Cancer therapies
Cerebrospinal fluid
Chemotherapy
Chromosome deletion
Consortia
Deoxyribonucleic acid
Development and progression
Diagnosis
DNA
Evolution
Evolution, Molecular
Gene deletion
Genes, Neoplasm - genetics
Genome, Human - genetics
Genomes
Genomics
Genotypes
Genotyping
Glioblastoma - cerebrospinal fluid
Glioblastoma - genetics
Glioblastoma - pathology
Glioma
Glioma - cerebrospinal fluid
Glioma - genetics
Glioma - pathology
Gliomas
Growth factors
Humanities and Social Sciences
Humans
Isocitrate dehydrogenase
Letter
Liquid Biopsy
Methods
Morbidity
multidisciplinary
Mutation
Neoplasm Grading
Oncology
Patients
Science
Science (multidisciplinary)
Signal transduction
Signs and symptoms
Surgery
Telomerase
Tumorigenesis
Tumors
United States
ISSN:0028-0836, 1476-4687, 1476-4687
Online Access:Get full text
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Abstract Diffuse gliomas are the most common malignant brain tumours in adults and include glioblastomas and World Health Organization (WHO) grade II and grade III tumours (sometimes referred to as lower-grade gliomas). Genetic tumour profiling is used to classify disease and guide therapy 1 , 2 , but involves brain surgery for tissue collection; repeated tumour biopsies may be necessary for accurate genotyping over the course of the disease 3 – 10 . While the detection of circulating tumour DNA (ctDNA) in the blood of patients with primary brain tumours remains challenging 11 , 12 , sequencing of ctDNA from the cerebrospinal fluid (CSF) may provide an alternative way to genotype gliomas with lower morbidity and cost 13 , 14 . We therefore evaluated the representation of the glioma genome in CSF from 85 patients with gliomas who underwent a lumbar puncture because they showed neurological signs or symptoms. Here we show that tumour-derived DNA was detected in CSF from 42 out of 85 patients (49.4%) and was associated with disease burden and adverse outcome. The genomic landscape of glioma in the CSF included a broad spectrum of genetic alterations and closely resembled the genomes of tumour biopsies. Alterations that occur early during tumorigenesis, such as co-deletion of chromosome arms 1p and 19q (1p/19q codeletion) and mutations in the metabolic genes isocitrate dehydrogenase 1 ( IDH1 ) or IDH2 1 , 2 , were shared in all matched ctDNA-positive CSF–tumour pairs, whereas growth factor receptor signalling pathways showed considerable evolution. The ability to monitor the evolution of the glioma genome through a minimally invasive technique could advance the clinical development and use of genotype-directed therapies for glioma, one of the most aggressive human cancers. Identification and sequencing of circulating tumour DNA in the cerebrospinal fluid of patients with glioma.
AbstractList Diffuse gliomas comprise the most common malignant brain tumors in adults and include glioblastomas (GBM) and World Health Organization (WHO) grade II and grade III tumors, sometimes referred to as lower-grade gliomas (LGGs). Genetic tumor profiling is used for disease classification and to guide therapy1,2, but involves brain surgery for tissue collection and repeated tumor biopsies may be necessary for accurate genotyping over the course of the disease 3–10. While detection of circulating tumor DNA (ctDNA) in blood remains challenging for patients with primary brain tumors 11,12, sequencing of cerebrospinal fluid (CSF) ctDNA may provide an alternative to genotype glioma at lower morbidity and cost 13,14. We therefore evaluated the representation of the glioma genome in CSF from 85 glioma patients who underwent a lumbar puncture for evaluation of neurological signs or symptoms. Tumor-derived DNA was detected in CSF from 42/85 (49.4 %) patients and was associated with disease burden and adverse outcome. The genomic landscape of glioma in CSF contained a broad spectrum of genetic alterations and closely resembled the genome in tumor biopsies. Alterations that occur early during tumorigenesis, such as co-deletion of chromosome arms 1p and 19q (1p/19q codeletion) and mutations in the metabolic genes isocitrate dehydrogenase 1 (IDH1) or IDH2 1,2, were shared in all matched ctDNA-positive CSF/tumor pairs, whereas we observed considerable evolution in growth factor receptor signaling pathways. The ability to monitor evolution of the glioma genome through a minimally invasive technique could advance the clinical development and use of genotype-directed therapies for glioma, one of the most aggressive human cancers.
Diffuse gliomas are the most common malignant brain tumours in adults and include glioblastomas and World Health Organization (WHO) grade II and grade III tumours (sometimes referred to as lower-grade gliomas). Genetic tumour profiling is used to classify disease and guide therapy.sup.1,2, but involves brain surgery for tissue collection; repeated tumour biopsies may be necessary for accurate genotyping over the course of the disease.sup.3-10. While the detection of circulating tumour DNA (ctDNA) in the blood of patients with primary brain tumours remains challenging.sup.11,12, sequencing of ctDNA from the cerebrospinal fluid (CSF) may provide an alternative way to genotype gliomas with lower morbidity and cost.sup.13,14. We therefore evaluated the representation of the glioma genome in CSF from 85 patients with gliomas who underwent a lumbar puncture because they showed neurological signs or symptoms. Here we show that tumour-derived DNA was detected in CSF from 42 out of 85 patients (49.4%) and was associated with disease burden and adverse outcome. The genomic landscape of glioma in the CSF included a broad spectrum of genetic alterations and closely resembled the genomes of tumour biopsies. Alterations that occur early during tumorigenesis, such as co-deletion of chromosome arms 1p and 19q (1p/19q codeletion) and mutations in the metabolic genes isocitrate dehydrogenase 1 (IDH1) or IDH2.sup.1,2, were shared in all matched ctDNA-positive CSF-tumour pairs, whereas growth factor receptor signalling pathways showed considerable evolution. The ability to monitor the evolution of the glioma genome through a minimally invasive technique could advance the clinical development and use of genotype-directed therapies for glioma, one of the most aggressive human cancers.
Diffuse gliomas are the most common malignant brain tumours in adults and include glioblastomas and World Health Organization (WHO) grade II and grade III tumours (sometimes referred to as lower-grade gliomas). Genetic tumour profiling is used to classify disease and guide therapy 1 , 2 , but involves brain surgery for tissue collection; repeated tumour biopsies may be necessary for accurate genotyping over the course of the disease 3 – 10 . While the detection of circulating tumour DNA (ctDNA) in the blood of patients with primary brain tumours remains challenging 11 , 12 , sequencing of ctDNA from the cerebrospinal fluid (CSF) may provide an alternative way to genotype gliomas with lower morbidity and cost 13 , 14 . We therefore evaluated the representation of the glioma genome in CSF from 85 patients with gliomas who underwent a lumbar puncture because they showed neurological signs or symptoms. Here we show that tumour-derived DNA was detected in CSF from 42 out of 85 patients (49.4%) and was associated with disease burden and adverse outcome. The genomic landscape of glioma in the CSF included a broad spectrum of genetic alterations and closely resembled the genomes of tumour biopsies. Alterations that occur early during tumorigenesis, such as co-deletion of chromosome arms 1p and 19q (1p/19q codeletion) and mutations in the metabolic genes isocitrate dehydrogenase 1 ( IDH1 ) or IDH2 1 , 2 , were shared in all matched ctDNA-positive CSF–tumour pairs, whereas growth factor receptor signalling pathways showed considerable evolution. The ability to monitor the evolution of the glioma genome through a minimally invasive technique could advance the clinical development and use of genotype-directed therapies for glioma, one of the most aggressive human cancers. Identification and sequencing of circulating tumour DNA in the cerebrospinal fluid of patients with glioma.
Diffuse gliomas are the most common malignant brain tumours in adults and include glioblastomas and World Health Organization (WHO) grade II and grade III tumours (sometimes referred to as lower-grade gliomas). Genetic tumour profiling is used to classify disease and guide therapy.sup.1,2, but involves brain surgery for tissue collection; repeated tumour biopsies may be necessary for accurate genotyping over the course of the disease.sup.3-10. While the detection of circulating tumour DNA (ctDNA) in the blood of patients with primary brain tumours remains challenging.sup.11,12, sequencing of ctDNA from the cerebrospinal fluid (CSF) may provide an alternative way to genotype gliomas with lower morbidity and cost.sup.13,14. We therefore evaluated the representation of the glioma genome in CSF from 85 patients with gliomas who underwent a lumbar puncture because they showed neurological signs or symptoms. Here we show that tumour-derived DNA was detected in CSF from 42 out of 85 patients (49.4%) and was associated with disease burden and adverse outcome. The genomic landscape of glioma in the CSF included a broad spectrum of genetic alterations and closely resembled the genomes of tumour biopsies. Alterations that occur early during tumorigenesis, such as co-deletion of chromosome arms 1p and 19q (1p/19q codeletion) and mutations in the metabolic genes isocitrate dehydrogenase 1 (IDH1) or IDH2.sup.1,2, were shared in all matched ctDNA-positive CSF-tumour pairs, whereas growth factor receptor signalling pathways showed considerable evolution. The ability to monitor the evolution of the glioma genome through a minimally invasive technique could advance the clinical development and use of genotype-directed therapies for glioma, one of the most aggressive human cancers. Identification and sequencing of circulating tumour DNA in the cerebrospinal fluid of patients with glioma.
Diffuse gliomas are the most common malignant brain tumours in adults and include glioblastomas and World Health Organization (WHO) grade II and grade III tumours (sometimes referred to as lower-grade gliomas). Genetic tumour profiling is used to classify disease and guide therapy1,2, but involves brain surgery for tissue collection; repeated tumour biopsies may be necessary for accurate genotyping over the course of the disease3-10. While the detection of circulating tumour DNA (ctDNA) in the blood of patients with primary brain tumours remains challenging11,12, sequencing of ctDNA from the cerebrospinal fluid (CSF) may provide an alternative way to genotype gliomas with lower morbidity and cost13,14. We therefore evaluated the representation of the glioma genome in CSF from 85 patients with gliomas who underwent a lumbar puncture because they showed neurological signs or symptoms. Here we show that tumour-derived DNA was detected in CSF from 42 out of 85 patients (49.4%) and was associated with disease burden and adverse outcome. The genomic landscape of glioma in the CSF included a broad spectrum of genetic alterations and closely resembled the genomes of tumour biopsies. Alterations that occur early during tumorigenesis, such as co-deletion of chromosome arms 1p and 19q (1p/19q codeletion) and mutations in the metabolic genes isocitrate dehydrogenase 1 (IDH1) or IDH21,2, were shared in all matched ctDNA-positive CSF-tumour pairs, whereas growth factor receptor signalling pathways showed considerable evolution. The ability to monitor the evolution of the glioma genome through a minimally invasive technique could advance the clinical development and use of genotype-directed therapies for glioma, one of the most aggressive human cancers.Diffuse gliomas are the most common malignant brain tumours in adults and include glioblastomas and World Health Organization (WHO) grade II and grade III tumours (sometimes referred to as lower-grade gliomas). Genetic tumour profiling is used to classify disease and guide therapy1,2, but involves brain surgery for tissue collection; repeated tumour biopsies may be necessary for accurate genotyping over the course of the disease3-10. While the detection of circulating tumour DNA (ctDNA) in the blood of patients with primary brain tumours remains challenging11,12, sequencing of ctDNA from the cerebrospinal fluid (CSF) may provide an alternative way to genotype gliomas with lower morbidity and cost13,14. We therefore evaluated the representation of the glioma genome in CSF from 85 patients with gliomas who underwent a lumbar puncture because they showed neurological signs or symptoms. Here we show that tumour-derived DNA was detected in CSF from 42 out of 85 patients (49.4%) and was associated with disease burden and adverse outcome. The genomic landscape of glioma in the CSF included a broad spectrum of genetic alterations and closely resembled the genomes of tumour biopsies. Alterations that occur early during tumorigenesis, such as co-deletion of chromosome arms 1p and 19q (1p/19q codeletion) and mutations in the metabolic genes isocitrate dehydrogenase 1 (IDH1) or IDH21,2, were shared in all matched ctDNA-positive CSF-tumour pairs, whereas growth factor receptor signalling pathways showed considerable evolution. The ability to monitor the evolution of the glioma genome through a minimally invasive technique could advance the clinical development and use of genotype-directed therapies for glioma, one of the most aggressive human cancers.
Diffuse gliomas are the most common malignant brain tumours in adults and include glioblastomas and World Health Organization (WHO) grade II and grade III tumours (sometimes referred to as lower-grade gliomas). Genetic tumour profiling is used to classify disease and guide therapy , but involves brain surgery for tissue collection; repeated tumour biopsies may be necessary for accurate genotyping over the course of the disease . While the detection of circulating tumour DNA (ctDNA) in the blood of patients with primary brain tumours remains challenging , sequencing of ctDNA from the cerebrospinal fluid (CSF) may provide an alternative way to genotype gliomas with lower morbidity and cost . We therefore evaluated the representation of the glioma genome in CSF from 85 patients with gliomas who underwent a lumbar puncture because they showed neurological signs or symptoms. Here we show that tumour-derived DNA was detected in CSF from 42 out of 85 patients (49.4%) and was associated with disease burden and adverse outcome. The genomic landscape of glioma in the CSF included a broad spectrum of genetic alterations and closely resembled the genomes of tumour biopsies. Alterations that occur early during tumorigenesis, such as co-deletion of chromosome arms 1p and 19q (1p/19q codeletion) and mutations in the metabolic genes isocitrate dehydrogenase 1 (IDH1) or IDH2 , were shared in all matched ctDNA-positive CSF-tumour pairs, whereas growth factor receptor signalling pathways showed considerable evolution. The ability to monitor the evolution of the glioma genome through a minimally invasive technique could advance the clinical development and use of genotype-directed therapies for glioma, one of the most aggressive human cancers.
Diffuse gliomas are the most common malignant brain tumours in adults and include glioblastomas and World Health Organization (WHO) grade II and grade III tumours (sometimes referred to as lower-grade gliomas). Genetic tumour profiling is used to classify disease and guide therapy, but involves brain surgery for tissue collection; repeated tumour biopsies may be necessary for accurate genotyping over the course of the disease. While the detection of circulating tumour DNA (ctDNA) in the blood of patients with primary brain tumours remains challenging, sequencing of ctDNA from the cerebrospinal fluid (CSF) may provide an alternative way to genotype gliomas with lower morbidity and cost. We therefore evaluated the representation of the glioma genome in CSF from 85 patients with gliomas who underwent a lumbar puncture because they showed neurological signs or symptoms. Here we show that tumour-derived DNA was detected in CSF from 42 out of 85 patients (49.4%) and was associated with disease burden and adverse outcome. The genomic landscape of glioma in the CSF included a broad spectrum of genetic alterations and closely resembled the genomes of tumour biopsies. Alterations that occur early during tumorigenesis, such as co-deletion of chromosome arms 1p and 19q (1p/19q codeletion) and mutations in the metabolic genes isocitrate dehydrogenase 1 (IDH1) or IDH2, were shared in all matched ctDNA-positive CSF-tumour pairs, whereas growth factor receptor signalling pathways showed considerable evolution. The ability to monitor the evolution of the glioma genome through a minimally invasive technique could advance the clinical development and use of genotype-directed therapies for glioma, one of the most aggressive human cancers.
Audience Academic
Author Ling, Lilan
Jing, Xiaohong
Grommes, Christian
Selcuklu, S. Duygu
Reiner, Anne S.
Rosenblum, Marc
Young, Robert J.
Pourmaleki, Maryam
Zheng, Youyun
Skakodub, Anna
Meng, Fanli
Campos, Carl
Brennan, Cameron W.
Hsieh, Wan-Ying
Tsui, Dana W. Y.
Tabar, Viviane
Shah, Ronak H.
Panageas, Katherine S.
DeAngelis, Lisa M.
Mellinghoff, Ingo K.
Pentsova, Elena I.
Bale, Tejus A.
Viale, Agnes
Souweidane, Mark M.
Briggs, Samuel
Miller, Alexandra M.
Mehta, Smrutiben A.
Berger, Michael F.
Distefano, Natalie
Samoila, Aliaksandra
AuthorAffiliation 4 Department of Radiology, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USA
7 Human Oncology and Pathogenesis Program, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USA
5 Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USA
1 Department of Neurology, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USA
10 Department of Pharmacology, Weill-Cornell School of Medicine, New York, NY 10021, USA
3 Department of Neurosurgery, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USA
8 Department of Laboratory Medicine, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USA
2 Department of Pathology, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USA
6 Center for Molecular Oncology, Memorial Sloan-Kettering Cancer Center, New York, NY 10065, USA
9 Department of Neurological Surgery, Weill-Cornell School of Medicine, New York, NY 10021, USA
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  organization: Department of Neurology, Memorial Sloan Kettering Cancer Center, Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, Department of Pharmacology, Weill Cornell Medical College
BackLink https://www.ncbi.nlm.nih.gov/pubmed/30675060$$D View this record in MEDLINE/PubMed
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COPYRIGHT 2019 Nature Publishing Group
Copyright Nature Publishing Group Jan 31, 2019
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Present address: Medical Genetics and Human Genomics, Department of Pediatrics, Northwell Health; 350 Community Dr.; Suite 2133A; Manhasset, NY 11030.
AUTHOR CONTRIBUTIONS
AUTHOR INFORMATION
Reprints and permissions information is available at www.nature.com/reprints. EIP reports advisory roles with AstraZeneca. VT is a founding investigator of Blue Rock Therapeutics. KSP reports stock ownership in Pfizer. LMD reports advisory roles for Sapience Therapeutics, Tocagen, BTG International, Roche, and Syndax. RJY reports research funding from Agios and advisory roles with Icon plc, NordicNeuroLab, and Puma Biotechnology. MFB reports advisory roles with Roche and research funding from Illumina. IKM reports research funding from General Electric, Amgen, and Lilly; advisory roles with Agios, Puma Biotechnology, and Debiopharm Group; and honoraria from Roche for a presentation. Correspondence and requests for materials should be addressed to bergerm1@mskcc.org and mellingi@mskcc.org.
AMM, RHS, and EIP contributed equally to this work.
AMM, RHS, EIP, LMD, RJY, MFB and IKM conceived and designed the study. AMM, RHS, EIP, RJY, MFB and IKM collected and assembled the data. AMM, RHS, EIP, MP, SB, ND, AS, SDS, LL, FM, XJ, CG, AV, MMS, VT, CWB, MR, RJY, MFB and IKM were responsible for provision of the study materials and the patients. AMM, RHS, EIP, YZ, AR, KP, RJY, MFB, IKM analyzed and interpreted the data. MP, CC, SAM, AS, FM processed the CSF and blood samples. AMM, RHS, EIP, W-YH, TAB, AV, LMD, KP, RJY, MFB, IKM provided administrative, material and technical support. AMM, RHS, EIP, DWT, CG, LMD, KP, RJY, MFB, IKM wrote the manuscript. All authors approved the manuscript.
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31304547 - Neurosurgery. 2019 Aug 1;85(2):E196-E197
31836074 - Int J Radiat Oncol Biol Phys. 2020 Jan 1;106(1):1-4
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Snippet Diffuse gliomas are the most common malignant brain tumours in adults and include glioblastomas and World Health Organization (WHO) grade II and grade III...
Diffuse gliomas comprise the most common malignant brain tumors in adults and include glioblastomas (GBM) and World Health Organization (WHO) grade II and...
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StartPage 654
SubjectTerms 631/1647/2217
631/67/1922
Adults
Analysis
Biopsy
Blood circulation
Brain
Brain cancer
Brain tumors
Cancer therapies
Cerebrospinal fluid
Chemotherapy
Chromosome deletion
Consortia
Deoxyribonucleic acid
Development and progression
Diagnosis
DNA
Evolution
Evolution, Molecular
Gene deletion
Genes, Neoplasm - genetics
Genome, Human - genetics
Genomes
Genomics
Genotypes
Genotyping
Glioblastoma - cerebrospinal fluid
Glioblastoma - genetics
Glioblastoma - pathology
Glioma
Glioma - cerebrospinal fluid
Glioma - genetics
Glioma - pathology
Gliomas
Growth factors
Humanities and Social Sciences
Humans
Isocitrate dehydrogenase
Letter
Liquid Biopsy
Methods
Morbidity
multidisciplinary
Mutation
Neoplasm Grading
Oncology
Patients
Science
Science (multidisciplinary)
Signal transduction
Signs and symptoms
Surgery
Telomerase
Tumorigenesis
Tumors
Title Tracking tumour evolution in glioma through liquid biopsies of cerebrospinal fluid
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https://pubmed.ncbi.nlm.nih.gov/PMC6457907
Volume 565
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