Ultra-low-input cell-free DNA sequencing for tumor detection and characterization in a real-world pediatric brain tumor cohort

Abstract Molecular profiling of pediatric central nervous system (CNS) tumors has important clinical utility for guiding diagnostic and therapeutic strategies. Cell-free DNA (cfDNA) from liquid biopsies has been used for minimally invasive tumor profiling and longitudinal disease assessment in adult...

Full description

Saved in:
Bibliographic Details
Main Authors: Tom T. Fischer, Kendra K. Maaß, Pitithat Puranachot, Markus Mieskolainen, Martin Sill, Paulina S. Schad, Stefanie Volz, Fabian Rosing, Tatjana Wedig, Nathalie Schwarz, Agnes M. E. Finster, Florian Iser, Jochen Meyer, Felix Sahm, Olli Lohi, Ahmed El Damaty, Benedikt Brors, Hannu Haapasalo, Stefan M. Pfister, Joonas Haapasalo, Kristian W. Pajtler, Kristiina Nordfors
Format: Article
Language:English
Published: BMC 2025-06-01
Series:Acta Neuropathologica Communications
Subjects:
Online Access:https://doi.org/10.1186/s40478-025-02024-w
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850119248251191296
author Tom T. Fischer
Kendra K. Maaß
Pitithat Puranachot
Markus Mieskolainen
Martin Sill
Paulina S. Schad
Stefanie Volz
Fabian Rosing
Tatjana Wedig
Nathalie Schwarz
Agnes M. E. Finster
Florian Iser
Jochen Meyer
Felix Sahm
Olli Lohi
Ahmed El Damaty
Benedikt Brors
Hannu Haapasalo
Stefan M. Pfister
Joonas Haapasalo
Kristian W. Pajtler
Kristiina Nordfors
author_facet Tom T. Fischer
Kendra K. Maaß
Pitithat Puranachot
Markus Mieskolainen
Martin Sill
Paulina S. Schad
Stefanie Volz
Fabian Rosing
Tatjana Wedig
Nathalie Schwarz
Agnes M. E. Finster
Florian Iser
Jochen Meyer
Felix Sahm
Olli Lohi
Ahmed El Damaty
Benedikt Brors
Hannu Haapasalo
Stefan M. Pfister
Joonas Haapasalo
Kristian W. Pajtler
Kristiina Nordfors
author_sort Tom T. Fischer
collection DOAJ
description Abstract Molecular profiling of pediatric central nervous system (CNS) tumors has important clinical utility for guiding diagnostic and therapeutic strategies. Cell-free DNA (cfDNA) from liquid biopsies has been used for minimally invasive tumor profiling and longitudinal disease assessment in adult oncology and pediatric hematology. However, in pediatric neuro-oncology, low cfDNA yields pose a major barrier to translating these assays from bench to bedside. Here, we implemented a low-coverage whole genome sequencing (lcWGS) assay for picogram-level cfDNA inputs and applied it to liquid biopsies from a sizeable, population-based, cross-entity pediatric CNS tumor cohort (n = 56 patients). Applying this protocol, cfDNA whole genome profiles were successfully acquired from all liquid biopsy samples (n = 61/61 serum, n = 56/56 CSF, 100%). Based on copy number variations (CNVs), circulating-tumor DNA (ctDNA) was detected in 2/61 serum (3%) and in 25/56 CSF (45%) samples across various brain tumor entities. The integration of cfDNA results with clinical data demonstrated the utility of CSF lcWGS as a biomarker assay at diagnosis to distinguish cancerous from non-cancerous pineal region lesions (n = 6 patients). Additionally, serial CSF assessment in n = 9 patients (n = 29 CSF samples) enabled minimally invasive disease monitoring, with the added value of molecular profile availability in n = 4/6 (67%) patients at relapse. Proof-of-concept data show the feasibility of serial CSF lcWGS to reveal tumor evolution, tumor heterogeneity and potential therapeutic vulnerabilities in a case of medulloblastoma and germ cell tumor. Our study underscores the clinical utility of a robust lcWGS-based liquid biopsy assay optimized for low-input samples. We identify use-cases for implementing liquid biopsies in the clinical management of pediatric CNS tumor patients and provide a strong rationale for integration into future trials.
format Article
id doaj-art-9587743f1f8643da8b65d568b4ac4ddc
institution OA Journals
issn 2051-5960
language English
publishDate 2025-06-01
publisher BMC
record_format Article
series Acta Neuropathologica Communications
spelling doaj-art-9587743f1f8643da8b65d568b4ac4ddc2025-08-20T02:35:40ZengBMCActa Neuropathologica Communications2051-59602025-06-0113111910.1186/s40478-025-02024-wUltra-low-input cell-free DNA sequencing for tumor detection and characterization in a real-world pediatric brain tumor cohortTom T. Fischer0Kendra K. Maaß1Pitithat Puranachot2Markus Mieskolainen3Martin Sill4Paulina S. Schad5Stefanie Volz6Fabian Rosing7Tatjana Wedig8Nathalie Schwarz9Agnes M. E. Finster10Florian Iser11Jochen Meyer12Felix Sahm13Olli Lohi14Ahmed El Damaty15Benedikt Brors16Hannu Haapasalo17Stefan M. Pfister18Joonas Haapasalo19Kristian W. Pajtler20Kristiina Nordfors21Hopp Children’s Cancer Center (KiTZ)Hopp Children’s Cancer Center (KiTZ)Princess Srisavangavadhana Faculty of Medicine, Chulabhorn Royal AcademyDepartment of Neurosurgery, Tampere University Hospital and Tampere UniversityHopp Children’s Cancer Center (KiTZ)Hopp Children’s Cancer Center (KiTZ)Hopp Children’s Cancer Center (KiTZ)Hopp Children’s Cancer Center (KiTZ)Hopp Children’s Cancer Center (KiTZ)Hopp Children’s Cancer Center (KiTZ)Hopp Children’s Cancer Center (KiTZ)Clinical Cooperation Unit Neurooncology, German Cancer Consortium (DKTK) and German Cancer Research Center (DKFZ)Clinical Cooperation Unit Neurooncology, German Cancer Consortium (DKTK) and German Cancer Research Center (DKFZ)Hopp Children’s Cancer Center (KiTZ)Tampere Center for Child, Adolescent, and Maternal Health Research, Faculty of Medicine and Health Technology, Tampere UniversityHeidelberg Faculty of Medicine, Department of Neurosurgery, Heidelberg University, Heidelberg University HospitalNational Center for Tumor Diseases (NCT), NCT Heidelberg, a partnership between DKFZ and Heidelberg University HospitalDepartment of Pathology, Fimlab Laboratories LtdHopp Children’s Cancer Center (KiTZ)Department of Neurosurgery, Tampere University Hospital and Tampere UniversityHopp Children’s Cancer Center (KiTZ)Tampere Center for Child, Adolescent, and Maternal Health Research, Faculty of Medicine and Health Technology, Tampere UniversityAbstract Molecular profiling of pediatric central nervous system (CNS) tumors has important clinical utility for guiding diagnostic and therapeutic strategies. Cell-free DNA (cfDNA) from liquid biopsies has been used for minimally invasive tumor profiling and longitudinal disease assessment in adult oncology and pediatric hematology. However, in pediatric neuro-oncology, low cfDNA yields pose a major barrier to translating these assays from bench to bedside. Here, we implemented a low-coverage whole genome sequencing (lcWGS) assay for picogram-level cfDNA inputs and applied it to liquid biopsies from a sizeable, population-based, cross-entity pediatric CNS tumor cohort (n = 56 patients). Applying this protocol, cfDNA whole genome profiles were successfully acquired from all liquid biopsy samples (n = 61/61 serum, n = 56/56 CSF, 100%). Based on copy number variations (CNVs), circulating-tumor DNA (ctDNA) was detected in 2/61 serum (3%) and in 25/56 CSF (45%) samples across various brain tumor entities. The integration of cfDNA results with clinical data demonstrated the utility of CSF lcWGS as a biomarker assay at diagnosis to distinguish cancerous from non-cancerous pineal region lesions (n = 6 patients). Additionally, serial CSF assessment in n = 9 patients (n = 29 CSF samples) enabled minimally invasive disease monitoring, with the added value of molecular profile availability in n = 4/6 (67%) patients at relapse. Proof-of-concept data show the feasibility of serial CSF lcWGS to reveal tumor evolution, tumor heterogeneity and potential therapeutic vulnerabilities in a case of medulloblastoma and germ cell tumor. Our study underscores the clinical utility of a robust lcWGS-based liquid biopsy assay optimized for low-input samples. We identify use-cases for implementing liquid biopsies in the clinical management of pediatric CNS tumor patients and provide a strong rationale for integration into future trials.https://doi.org/10.1186/s40478-025-02024-wCerebrospinal fluid liquid biopsiesCell-free DNALow-input samplesCirculating-tumor DNACopy number variation profilingLow-coverage whole genome sequencing
spellingShingle Tom T. Fischer
Kendra K. Maaß
Pitithat Puranachot
Markus Mieskolainen
Martin Sill
Paulina S. Schad
Stefanie Volz
Fabian Rosing
Tatjana Wedig
Nathalie Schwarz
Agnes M. E. Finster
Florian Iser
Jochen Meyer
Felix Sahm
Olli Lohi
Ahmed El Damaty
Benedikt Brors
Hannu Haapasalo
Stefan M. Pfister
Joonas Haapasalo
Kristian W. Pajtler
Kristiina Nordfors
Ultra-low-input cell-free DNA sequencing for tumor detection and characterization in a real-world pediatric brain tumor cohort
Acta Neuropathologica Communications
Cerebrospinal fluid liquid biopsies
Cell-free DNA
Low-input samples
Circulating-tumor DNA
Copy number variation profiling
Low-coverage whole genome sequencing
title Ultra-low-input cell-free DNA sequencing for tumor detection and characterization in a real-world pediatric brain tumor cohort
title_full Ultra-low-input cell-free DNA sequencing for tumor detection and characterization in a real-world pediatric brain tumor cohort
title_fullStr Ultra-low-input cell-free DNA sequencing for tumor detection and characterization in a real-world pediatric brain tumor cohort
title_full_unstemmed Ultra-low-input cell-free DNA sequencing for tumor detection and characterization in a real-world pediatric brain tumor cohort
title_short Ultra-low-input cell-free DNA sequencing for tumor detection and characterization in a real-world pediatric brain tumor cohort
title_sort ultra low input cell free dna sequencing for tumor detection and characterization in a real world pediatric brain tumor cohort
topic Cerebrospinal fluid liquid biopsies
Cell-free DNA
Low-input samples
Circulating-tumor DNA
Copy number variation profiling
Low-coverage whole genome sequencing
url https://doi.org/10.1186/s40478-025-02024-w
work_keys_str_mv AT tomtfischer ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT kendrakmaaß ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT pitithatpuranachot ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT markusmieskolainen ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT martinsill ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT paulinasschad ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT stefanievolz ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT fabianrosing ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT tatjanawedig ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT nathalieschwarz ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT agnesmefinster ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT florianiser ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT jochenmeyer ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT felixsahm ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT ollilohi ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT ahmedeldamaty ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT benediktbrors ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT hannuhaapasalo ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT stefanmpfister ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT joonashaapasalo ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT kristianwpajtler ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort
AT kristiinanordfors ultralowinputcellfreednasequencingfortumordetectionandcharacterizationinarealworldpediatricbraintumorcohort