Diagnostic yield and clinical impact of germline sequencing in children with CNS and extracranial solid tumors-a nationwide, prospective Swedish study.

Childhood cancer predisposition Germline variants Somatic mutations Whole-genome sequencing

Journal

The Lancet regional health. Europe
ISSN: 2666-7762
Titre abrégé: Lancet Reg Health Eur
Pays: England
ID NLM: 101777707

Informations de publication

Date de publication:
Apr 2024
Historique:
received: 20 11 2023
revised: 04 02 2024
accepted: 23 02 2024
medline: 28 5 2024
pubmed: 28 5 2024
entrez: 28 5 2024
Statut: epublish

Résumé

Childhood cancer predisposition (ChiCaP) syndromes are increasingly recognized as contributing factors to childhood cancer development. Yet, due to variable availability of germline testing, many children with ChiCaP might go undetected today. We report results from the nationwide and prospective ChiCaP study that investigated diagnostic yield and clinical impact of integrating germline whole-genome sequencing (gWGS) with tumor sequencing and systematic phenotyping in children with solid tumors. gWGS was performed in 309 children at diagnosis of CNS (n = 123, 40%) or extracranial (n = 186, 60%) solid tumors and analyzed for disease-causing variants in 189 known cancer predisposing genes. Tumor sequencing data were available for 74% (227/309) of patients. In addition, a standardized clinical assessment for underlying predisposition was performed in 95% (293/309) of patients. The prevalence of ChiCaP diagnoses was 11% (35/309), of which 69% (24/35) were unknown at inclusion (diagnostic yield 8%, 24/298). A second-hit and/or relevant mutational signature was observed in 19/21 (90%) tumors with informative data. ChiCaP diagnoses were more prevalent among patients with retinoblastomas (50%, 6/12) and high-grade astrocytomas (37%, 6/16), and in those with non-cancer related features (23%, 20/88), and ≥2 positive ChiCaP criteria (28%, 22/79). ChiCaP diagnoses were autosomal dominant in 80% (28/35) of patients, yet confirmed Overall, our results demonstrate that systematic phenotyping, combined with genomics-based diagnostics of ChiCaP in children with solid tumors is feasible in large-scale clinical practice and critically guides personalized care in a sizable proportion of patients. The study was supported by the Swedish Childhood Cancer Fund and the Ministry of Health and Social Affairs.

Sections du résumé

Background UNASSIGNED
Childhood cancer predisposition (ChiCaP) syndromes are increasingly recognized as contributing factors to childhood cancer development. Yet, due to variable availability of germline testing, many children with ChiCaP might go undetected today. We report results from the nationwide and prospective ChiCaP study that investigated diagnostic yield and clinical impact of integrating germline whole-genome sequencing (gWGS) with tumor sequencing and systematic phenotyping in children with solid tumors.
Methods UNASSIGNED
gWGS was performed in 309 children at diagnosis of CNS (n = 123, 40%) or extracranial (n = 186, 60%) solid tumors and analyzed for disease-causing variants in 189 known cancer predisposing genes. Tumor sequencing data were available for 74% (227/309) of patients. In addition, a standardized clinical assessment for underlying predisposition was performed in 95% (293/309) of patients.
Findings UNASSIGNED
The prevalence of ChiCaP diagnoses was 11% (35/309), of which 69% (24/35) were unknown at inclusion (diagnostic yield 8%, 24/298). A second-hit and/or relevant mutational signature was observed in 19/21 (90%) tumors with informative data. ChiCaP diagnoses were more prevalent among patients with retinoblastomas (50%, 6/12) and high-grade astrocytomas (37%, 6/16), and in those with non-cancer related features (23%, 20/88), and ≥2 positive ChiCaP criteria (28%, 22/79). ChiCaP diagnoses were autosomal dominant in 80% (28/35) of patients, yet confirmed
Interpretation UNASSIGNED
Overall, our results demonstrate that systematic phenotyping, combined with genomics-based diagnostics of ChiCaP in children with solid tumors is feasible in large-scale clinical practice and critically guides personalized care in a sizable proportion of patients.
Funding UNASSIGNED
The study was supported by the Swedish Childhood Cancer Fund and the Ministry of Health and Social Affairs.

Identifiants

pubmed: 38803632
doi: 10.1016/j.lanepe.2024.100881
pii: S2666-7762(24)00047-4
pmc: PMC11129334
doi:

Types de publication

Journal Article

Langues

eng

Pagination

100881

Informations de copyright

© 2024 The Author(s).

Déclaration de conflit d'intérêts

BT, FA, ET, and AN received support from the Swedish Childhood Cancer Fund (BT: TJ2018-0042; FA: KP2021-0010; ET: TJ2021-0125; AN: KP2019-0024, PR2019-0027, TJ2019-0013) and the Swedish Cancer Fund (FA: 21 1540 Fk 01 H; ET: 22 2451Fk; AN: 22 2057Pj). BT, ET and AN received support from Region Stockholm (BT: FoUI-985957; ET: FoUI-973659; AN: 5010124 ALF, 520136 ALF). AN received support from The Swedish Research Council (2021-02860). MB received honoraria for lectures by the Swedish Childhood Cancer Fund. GS served as advisor for trial design for Cyxone AB, Sweden. NH served as Chair of NOPHO Scientific Committee and Young NOPHO without retribution. RR received honoraria from AbbVie, AstraZeneca, Janssen, Illumina, and Roche. DG received grants from Swedish Ministry of Health and Social Affairs for GMS Childhood Cancer and is Vice dean for internationalization and recruitment, Faculty of Medicine, Lund University. AN received also funding from the Cancer Society of Stockholm, Stiftelsen Frimurare Barnhuset i Stockholm, Hållsten research foundation, Berth von Kantzow foundation and is board member of Sävstaholm foundation, Ågrenska foundation, Sällsyntafonden. All other authors have no conflict of interest to declare.

Auteurs

Bianca Tesi (B)

Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden.
Clinical Genetics and Genomics, Karolinska University Hospital, Solna, Sweden.
Department of Medicine, Center for Hematology and Regenerative Medicine, Karolinska Institutet, Stockholm, Sweden.

Kristina Lagerstedt Robinson (KL)

Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden.
Clinical Genetics and Genomics, Karolinska University Hospital, Solna, Sweden.

Frida Abel (F)

Department of Clinical Genetics and Genomics, Sahlgrenska University Hospital, Gothenburg, Sweden.
Department of Laboratory Medicine, Institute of Biomedicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden.

Teresita Díaz de Ståhl (T)

Department of Oncology-Pathology, Karolinska Institutet, Stockholm, Sweden.
Clinical Pathology and Cancer Diagnostics, Karolinska University Hospital, Stockholm, Sweden.

Sara Orrsjö (S)

Department of Clinical Genetics and Genomics, Sahlgrenska University Hospital, Gothenburg, Sweden.
Department of Laboratory Medicine, Institute of Biomedicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden.

Anna Poluha (A)

Clinical Genetics, Uppsala University Hospital, Uppsala, Sweden.
Department of Immunology, Genetics and Pathology, Uppsala University, Uppsala, Sweden.

Maria Hellberg (M)

Department of Clinical Genetics, Pathology and Molecular Diagnostics, Office of Medical Services, Region Skåne, Lund, Sweden.

Sandra Wessman (S)

Department of Oncology-Pathology, Karolinska Institutet, Stockholm, Sweden.
Clinical Pathology and Cancer Diagnostics, Karolinska University Hospital, Stockholm, Sweden.

Sofie Samuelsson (S)

Department of Clinical Genetics, Pathology and Molecular Diagnostics, Office of Medical Services, Region Skåne, Lund, Sweden.

Tony Frisk (T)

Department of Pediatric Hematology and Oncology, Karolinska University Hospital, Stockholm, Sweden.
Childhood Cancer Research Unit, Department of Women's and Children's Health, Karolinska Institutet, Stockholm, Sweden.

Hartmut Vogt (H)

Crown Princess Victoria Children's Hospital, and Division of Children's and Women's Health, Department of Biomedical and Clinical Sciences, Linköping University, Linköping, Sweden.

Karin Henning (K)

Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden.
Department of Pediatric Hematology and Oncology, Karolinska University Hospital, Stockholm, Sweden.

Magnus Sabel (M)

Department of Pediatrics, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg, Sweden.
Queen Silvia Children's Hospital, Sahlgrenska University Hospital, Gothenburg, Sweden.

Torben Ek (T)

Department of Pediatrics, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg, Sweden.
Queen Silvia Children's Hospital, Sahlgrenska University Hospital, Gothenburg, Sweden.

Niklas Pal (N)

Department of Pediatric Hematology and Oncology, Karolinska University Hospital, Stockholm, Sweden.

Per Nyman (P)

Department of Health, Medicine and Caring Sciences, Linköping University, Linköping, Sweden.
Centre for Medical Image Science and Visualization (CMIV), Linköping University, Linköping, Sweden.

Geraldine Giraud (G)

Department of Immunology, Genetics, and Pathology, Science for Life Laboratory, Rudbeck Laboratory, Uppsala University, Uppsala, Sweden.
Pediatric Oncology, Uppsala University Children's Hospital, Uppsala, Sweden.
Department of Women's and Children's Health, Uppsala University, Sweden.

Joakim Wille (J)

Childhood Cancer Center, Skåne University Hospital, Lund, Sweden.

Cornelis Jan Pronk (CJ)

Childhood Cancer Center, Skåne University Hospital, Lund, Sweden.
Division of Molecular Hematology/Wallenberg Center for Molecular Medicine, Lund University, Sweden.

Ulrika Norén-Nyström (U)

Department of Clinical Sciences, Pediatrics, Umeå University, Umeå, Sweden.

Magnus Borssén (M)

Department of Clinical Sciences, Pediatrics, Umeå University, Umeå, Sweden.

Maria Fili (M)

Division of Eye and Vision, Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden.
St. Erik Eye Hospital, Stockholm, Sweden.

Gustav Stålhammar (G)

Division of Eye and Vision, Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden.
St. Erik Eye Hospital, Stockholm, Sweden.

Nikolas Herold (N)

Department of Pediatric Hematology and Oncology, Karolinska University Hospital, Stockholm, Sweden.
Childhood Cancer Research Unit, Department of Women's and Children's Health, Karolinska Institutet, Stockholm, Sweden.

Giorgio Tettamanti (G)

Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden.
Unit of Epidemiology, Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.

Carolina Maya-Gonzalez (C)

Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden.

Linda Arvidsson (L)

Department of Clinical Genetics, Pathology and Molecular Diagnostics, Office of Medical Services, Region Skåne, Lund, Sweden.

Anna Rosén (A)

Department of Radiation Sciences, Oncology, Umeå University, Umeå, Sweden.

Katja Ekholm (K)

Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden.
Clinical Genetics and Genomics, Karolinska University Hospital, Solna, Sweden.

Ekaterina Kuchinskaya (E)

Department of Clinical Genetics, Linköping University Hospital, Linköping, Sweden.

Anna-Lotta Hallbeck (AL)

Department of Clinical Genetics, Linköping University Hospital, Linköping, Sweden.
Department of Biomedical and Clinical Sciences, Linköping University, Linköping, Sweden.

Margareta Nordling (M)

Department of Clinical Genetics, Linköping University Hospital, Linköping, Sweden.
Department of Biomedical and Clinical Sciences, Linköping University, Linköping, Sweden.

Pia Palmebäck (P)

Department of Clinical Genetics, Linköping University Hospital, Linköping, Sweden.

Per Kogner (P)

Department of Pediatric Hematology and Oncology, Karolinska University Hospital, Stockholm, Sweden.
Childhood Cancer Research Unit, Department of Women's and Children's Health, Karolinska Institutet, Stockholm, Sweden.

Gunilla Kanter Smoler (GK)

Department of Clinical Genetics and Genomics, Sahlgrenska University Hospital, Gothenburg, Sweden.

Päivi Lähteenmäki (P)

Childhood Cancer Research Unit, Department of Women's and Children's Health, Karolinska Institutet, Stockholm, Sweden.

Susanne Fransson (S)

Department of Clinical Genetics and Genomics, Sahlgrenska University Hospital, Gothenburg, Sweden.
Department of Laboratory Medicine, Institute of Biomedicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden.

Tommy Martinsson (T)

Department of Laboratory Medicine, Institute of Biomedicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden.

Alia Shamik (A)

Department of Oncology-Pathology, Karolinska Institutet, Stockholm, Sweden.
Clinical Pathology and Cancer Diagnostics, Karolinska University Hospital, Stockholm, Sweden.

Fredrik Mertens (F)

Department of Clinical Genetics, Pathology and Molecular Diagnostics, Office of Medical Services, Region Skåne, Lund, Sweden.

Richard Rosenquist (R)

Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden.
Clinical Genetics and Genomics, Karolinska University Hospital, Solna, Sweden.
Genomic Medicine Center Karolinska, Karolinska University Hospital, Stockholm, Sweden.

Valtteri Wirta (V)

Genomic Medicine Center Karolinska, Karolinska University Hospital, Stockholm, Sweden.
Science for Life Laboratory, Department of Microbiology, Tumour and Cell Biology, Karolinska Institutet, Stockholm, Sweden.
Science for Life Laboratory, School of Engineering Sciences in Chemistry, Biotechnology and Health, KTH Royal Institutet of Technology, Stockholm, Sweden.

Emma Tham (E)

Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden.
Clinical Genetics and Genomics, Karolinska University Hospital, Solna, Sweden.

Pernilla Grillner (P)

Department of Pediatric Hematology and Oncology, Karolinska University Hospital, Stockholm, Sweden.
Childhood Cancer Research Unit, Department of Women's and Children's Health, Karolinska Institutet, Stockholm, Sweden.

Johanna Sandgren (J)

Department of Oncology-Pathology, Karolinska Institutet, Stockholm, Sweden.
Clinical Pathology and Cancer Diagnostics, Karolinska University Hospital, Stockholm, Sweden.

Gustaf Ljungman (G)

Pediatric Oncology, Uppsala University Children's Hospital, Uppsala, Sweden.
Department of Women's and Children's Health, Uppsala University, Sweden.

David Gisselsson (D)

Department of Clinical Genetics, Pathology and Molecular Diagnostics, Office of Medical Services, Region Skåne, Lund, Sweden.

Fulya Taylan (F)

Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden.
Clinical Genetics and Genomics, Karolinska University Hospital, Solna, Sweden.

Ann Nordgren (A)

Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden.
Clinical Genetics and Genomics, Karolinska University Hospital, Solna, Sweden.
Department of Clinical Genetics and Genomics, Sahlgrenska University Hospital, Gothenburg, Sweden.
Department of Laboratory Medicine, Institute of Biomedicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden.
Genomic Medicine Center Karolinska, Karolinska University Hospital, Stockholm, Sweden.

Classifications MeSH