Next-generation sequencing of cerebrospinal fluid for clinical molecular diagnostics in pediatric, adolescent and young adult brain tumor patients.


Journal

Neuro-oncology
ISSN: 1523-5866
Titre abrégé: Neuro Oncol
Pays: England
ID NLM: 100887420

Informations de publication

Date de publication:
03 10 2022
Historique:
pubmed: 12 2 2022
medline: 5 10 2022
entrez: 11 2 2022
Statut: ppublish

Résumé

Safe sampling of central nervous system tumor tissue for diagnostic purposes may be difficult if not impossible, especially in pediatric patients, and an unmet need exists to develop less invasive diagnostic tests. We report our clinical experience with minimally invasive molecular diagnostics using a clinically validated assay for sequencing of cerebrospinal fluid (CSF) cell-free DNA (cfDNA). All CSF samples were collected as part of clinical care, and results reported to both clinicians and patients/families. We analyzed 64 CSF samples from 45 pediatric, adolescent and young adult (AYA) patients (pediatric = 25; AYA = 20) with primary and recurrent brain tumors across 12 histopathological subtypes including high-grade glioma (n = 10), medulloblastoma (n = 10), pineoblastoma (n = 5), low-grade glioma (n = 4), diffuse leptomeningeal glioneuronal tumor (DLGNT) (n = 4), retinoblastoma (n = 4), ependymoma (n = 3), and other (n = 5). Somatic alterations were detected in 30/64 samples (46.9%) and in at least one sample per unique patient in 21/45 patients (46.6%). CSF cfDNA positivity was strongly associated with the presence of disseminated disease at the time of collection (81.5% of samples from patients with disseminated disease were positive). No association was seen between CSF cfDNA positivity and the timing of CSF collection during the patient's disease course. We identified three general categories where CSF cfDNA testing provided additional relevant diagnostic, prognostic, and/or therapeutic information, impacting clinical assessment and decision making: (1) diagnosis and/or identification of actionable alterations; (2) monitor response to therapy; and (3) tracking tumor evolution. Our findings support broader implementation of clinical CSF cfDNA testing in this population to improve care.

Sections du résumé

BACKGROUND
Safe sampling of central nervous system tumor tissue for diagnostic purposes may be difficult if not impossible, especially in pediatric patients, and an unmet need exists to develop less invasive diagnostic tests.
METHODS
We report our clinical experience with minimally invasive molecular diagnostics using a clinically validated assay for sequencing of cerebrospinal fluid (CSF) cell-free DNA (cfDNA). All CSF samples were collected as part of clinical care, and results reported to both clinicians and patients/families.
RESULTS
We analyzed 64 CSF samples from 45 pediatric, adolescent and young adult (AYA) patients (pediatric = 25; AYA = 20) with primary and recurrent brain tumors across 12 histopathological subtypes including high-grade glioma (n = 10), medulloblastoma (n = 10), pineoblastoma (n = 5), low-grade glioma (n = 4), diffuse leptomeningeal glioneuronal tumor (DLGNT) (n = 4), retinoblastoma (n = 4), ependymoma (n = 3), and other (n = 5). Somatic alterations were detected in 30/64 samples (46.9%) and in at least one sample per unique patient in 21/45 patients (46.6%). CSF cfDNA positivity was strongly associated with the presence of disseminated disease at the time of collection (81.5% of samples from patients with disseminated disease were positive). No association was seen between CSF cfDNA positivity and the timing of CSF collection during the patient's disease course.
CONCLUSIONS
We identified three general categories where CSF cfDNA testing provided additional relevant diagnostic, prognostic, and/or therapeutic information, impacting clinical assessment and decision making: (1) diagnosis and/or identification of actionable alterations; (2) monitor response to therapy; and (3) tracking tumor evolution. Our findings support broader implementation of clinical CSF cfDNA testing in this population to improve care.

Identifiants

pubmed: 35148412
pii: 6527231
doi: 10.1093/neuonc/noac035
pmc: PMC9527510
doi:

Substances chimiques

Cell-Free Nucleic Acids 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

1763-1772

Subventions

Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

© The Author(s) 2022. Published by Oxford University Press on behalf of the Society for Neuro-Oncology. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

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Auteurs

Alexandra M Miller (AM)

Department of Neurology, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Luca Szalontay (L)

Department of Pediatrics, Columbia University Irving Medical Center, New York, New York, USA.

Nancy Bouvier (N)

Pediatric Translational Medicine Program, Department of Pediatrics, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Katherine Hill (K)

Pediatric Translational Medicine Program, Department of Pediatrics, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Hamza Ahmad (H)

Pediatric Translational Medicine Program, Department of Pediatrics, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Johnathan Rafailov (J)

Center for Molecular Oncology, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Alex J Lee (AJ)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

M Irene Rodriguez-Sanchez (MI)

Pediatric Translational Medicine Program, Department of Pediatrics, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Onur Yildirim (O)

Department of Radiology, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Arti Patel (A)

Center for Molecular Oncology, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Tejus A Bale (TA)

Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Jamal K Benhamida (JK)

Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Ryma Benayed (R)

Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Maria E Arcila (ME)

Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Maria Donzelli (M)

Department of Pediatrics, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Ira J Dunkel (IJ)

Department of Pediatrics, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Stephen W Gilheeney (SW)

Department of Pediatrics, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Yasmin Khakoo (Y)

Department of Pediatrics, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Kim Kramer (K)

Department of Pediatrics, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Sameer F Sait (SF)

Department of Pediatrics, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Jeffrey P Greenfield (JP)

Department of Pediatrics, Weill Cornell Medical College, New York, New York, USA.
Department of Neurosurgery, Memorial Sloan Kettering Cancer Center, New York, New York, USA.
Department of Neurological Surgery, Weill Cornell Medical College, New York, New York, USA.
Department of Neurological Surgery, Columbia University Irving Medical Center, New York, New York, USA.

Mark M Souweidane (MM)

Department of Pediatrics, Weill Cornell Medical College, New York, New York, USA.
Department of Neurosurgery, Memorial Sloan Kettering Cancer Center, New York, New York, USA.
Department of Neurological Surgery, Weill Cornell Medical College, New York, New York, USA.
Department of Neurological Surgery, Columbia University Irving Medical Center, New York, New York, USA.

Sofia Haque (S)

Department of Radiology, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Audrey Mauguen (A)

Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Michael F Berger (MF)

Center for Molecular Oncology, Memorial Sloan Kettering Cancer Center, New York, New York, USA.
Department of Pathology, Memorial Sloan Kettering Cancer Center, New York, New York, USA.
Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Ingo K Mellinghoff (IK)

Human Oncology and Pathogenesis Program, Memorial Sloan Kettering Cancer Center, New York, New York, USA.
Department of Pharmacology, Weill Cornell Medical College, New York, New York, USA.

Matthias A Karajannis (MA)

Department of Pediatrics, Memorial Sloan Kettering Cancer Center, New York, New York, USA.
Department of Pediatrics, Weill Cornell Medical College, New York, New York, USA.

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Classifications MeSH