Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seeding

Background: Neuroblastoma is the most frequent extracranial solid tumour in children, accounting for ∼15% of deaths due to cancer in childhood. The most common clinical presentation are abdominal tumours. An altered gut microbiome composition has been linked to multiple cancer types, and reported in...

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Autores: Vallès Colomer, Mireia, Manghi, Paolo, Cumbo, Fabio, Masetti, Giulia, Armanini, Federica, Asnicar, Francesco, Blanco-Míguez, Aitor, Pinto, Federica, Punčochář, Michal, Garaventa, Alberto, Amoroso, Loredana, Ponzoni, Mirco, Corrias, Maria Valeria, Segata, Nicola
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2024
País:España
Institución:Universitat Pompeu Fabra
Repositorio:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/70038
Acceso en línea:http://hdl.handle.net/10230/70038
http://dx.doi.org/10.1016/j.ebiom.2023.104917
Access Level:acceso abierto
Palabra clave:Gut microbiome
Metagenomics
Mother-infant transmission
Neuroblastoma
Paediatric cancer
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spelling Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seedingVallès Colomer, MireiaManghi, PaoloCumbo, FabioMasetti, GiuliaArmanini, FedericaAsnicar, FrancescoBlanco-Míguez, AitorPinto, FedericaPunčochář, MichalGaraventa, AlbertoAmoroso, LoredanaPonzoni, MircoCorrias, Maria ValeriaSegata, NicolaGut microbiomeMetagenomicsMother-infant transmissionNeuroblastomaPaediatric cancerBackground: Neuroblastoma is the most frequent extracranial solid tumour in children, accounting for ∼15% of deaths due to cancer in childhood. The most common clinical presentation are abdominal tumours. An altered gut microbiome composition has been linked to multiple cancer types, and reported in murine models of neuroblastoma. Whether children with neuroblastoma display alterations in gut microbiome composition remains unexplored. Methods: We assessed gut microbiome composition by shotgun metagenomic profiling in an observational cross-sectional study on 288 individuals, consisting of patients with a diagnosis of neuroblastoma at disease onset (N = 63), healthy controls matching the patients on the main covariates of microbiome composition (N = 94), healthy siblings of the patients (N = 13), mothers of patients (N = 59), and mothers of the controls (N = 59). We examined taxonomic and functional microbiome composition and mother-infant strain transmission patterns. Findings: Patients with neuroblastoma displayed alterations in gut microbiome composition characterised by reduced microbiome richness, decreased relative abundances of 18 species (including Phocaeicola dorei and Bifidobacterium bifidum), enriched protein fermentation and reduced carbohydrate fermentation potential. Using machine learning, we could successfully discriminate patients from controls (AUC = 82%). Healthy siblings did not display such alterations but resembled the healthy control group. No significant differences in maternal microbiome composition nor mother-to-offspring transmission were detected. Interpretation: Patients with neuroblastoma display alterations in taxonomic and functional gut microbiome composition, which cannot be traced to differential maternal seeding. Follow-up research should include investigating potential causal links.This study was funded by the Italian Ministry of Health Ricerca Corrente and Ricerca Finalizzata 5 per mille (to MPonzoni); Fondazione Italiana Neuroblastoma (to MPonzoni); European Research Council (ERC-StG project MetaPG-716575 and ERC-CoG microTOUCH-101045015 to NS); the European H2020 program ONCOBIOME-825410 project (to NS); the National Cancer Institute of the National Institutes of Health 1U01CA230551 (to NS); the Premio Internazionale Lombardia e Ricerca 2019 (to NS); the MIUR Progetti di Ricerca di Rilevante Interesse Nazionale (PRIN) Bando 2017 Grant 2017J3E2W2 (to NS); EMBO ALTF 593-2020 and Knowledge Generation Project from the Spanish Ministry of Science and Innovation (PID2022-139328OA-I00) (to MV-C).Elsevier202520252024info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/70038http://dx.doi.org/10.1016/j.ebiom.2023.104917reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésEBioMedicine. 2024 Jan;99:104917info:eu-repo/grantAgreement/EC/H2020/716575info:eu-repo/grantAgreement/EC/HE/101045015info:eu-repo/grantAgreement/EC/H2020/825410info:eu-repo/grantAgreement/ES/3PE/PID2022-139328OA-I00© 2023 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/700382026-06-12T07:21:37Z
dc.title.none.fl_str_mv Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seeding
title Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seeding
spellingShingle Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seeding
Vallès Colomer, Mireia
Gut microbiome
Metagenomics
Mother-infant transmission
Neuroblastoma
Paediatric cancer
title_short Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seeding
title_full Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seeding
title_fullStr Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seeding
title_full_unstemmed Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seeding
title_sort Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seeding
dc.creator.none.fl_str_mv Vallès Colomer, Mireia
Manghi, Paolo
Cumbo, Fabio
Masetti, Giulia
Armanini, Federica
Asnicar, Francesco
Blanco-Míguez, Aitor
Pinto, Federica
Punčochář, Michal
Garaventa, Alberto
Amoroso, Loredana
Ponzoni, Mirco
Corrias, Maria Valeria
Segata, Nicola
author Vallès Colomer, Mireia
author_facet Vallès Colomer, Mireia
Manghi, Paolo
Cumbo, Fabio
Masetti, Giulia
Armanini, Federica
Asnicar, Francesco
Blanco-Míguez, Aitor
Pinto, Federica
Punčochář, Michal
Garaventa, Alberto
Amoroso, Loredana
Ponzoni, Mirco
Corrias, Maria Valeria
Segata, Nicola
author_role author
author2 Manghi, Paolo
Cumbo, Fabio
Masetti, Giulia
Armanini, Federica
Asnicar, Francesco
Blanco-Míguez, Aitor
Pinto, Federica
Punčochář, Michal
Garaventa, Alberto
Amoroso, Loredana
Ponzoni, Mirco
Corrias, Maria Valeria
Segata, Nicola
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Gut microbiome
Metagenomics
Mother-infant transmission
Neuroblastoma
Paediatric cancer
topic Gut microbiome
Metagenomics
Mother-infant transmission
Neuroblastoma
Paediatric cancer
description Background: Neuroblastoma is the most frequent extracranial solid tumour in children, accounting for ∼15% of deaths due to cancer in childhood. The most common clinical presentation are abdominal tumours. An altered gut microbiome composition has been linked to multiple cancer types, and reported in murine models of neuroblastoma. Whether children with neuroblastoma display alterations in gut microbiome composition remains unexplored. Methods: We assessed gut microbiome composition by shotgun metagenomic profiling in an observational cross-sectional study on 288 individuals, consisting of patients with a diagnosis of neuroblastoma at disease onset (N = 63), healthy controls matching the patients on the main covariates of microbiome composition (N = 94), healthy siblings of the patients (N = 13), mothers of patients (N = 59), and mothers of the controls (N = 59). We examined taxonomic and functional microbiome composition and mother-infant strain transmission patterns. Findings: Patients with neuroblastoma displayed alterations in gut microbiome composition characterised by reduced microbiome richness, decreased relative abundances of 18 species (including Phocaeicola dorei and Bifidobacterium bifidum), enriched protein fermentation and reduced carbohydrate fermentation potential. Using machine learning, we could successfully discriminate patients from controls (AUC = 82%). Healthy siblings did not display such alterations but resembled the healthy control group. No significant differences in maternal microbiome composition nor mother-to-offspring transmission were detected. Interpretation: Patients with neuroblastoma display alterations in taxonomic and functional gut microbiome composition, which cannot be traced to differential maternal seeding. Follow-up research should include investigating potential causal links.
publishDate 2024
dc.date.none.fl_str_mv 2024
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/70038
http://dx.doi.org/10.1016/j.ebiom.2023.104917
url http://hdl.handle.net/10230/70038
http://dx.doi.org/10.1016/j.ebiom.2023.104917
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv EBioMedicine. 2024 Jan;99:104917
info:eu-repo/grantAgreement/EC/H2020/716575
info:eu-repo/grantAgreement/EC/HE/101045015
info:eu-repo/grantAgreement/EC/H2020/825410
info:eu-repo/grantAgreement/ES/3PE/PID2022-139328OA-I00
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:Repositorio Digital de la UPF
instname:Universitat Pompeu Fabra
instname_str Universitat Pompeu Fabra
reponame_str Repositorio Digital de la UPF
collection Repositorio Digital de la UPF
repository.name.fl_str_mv
repository.mail.fl_str_mv
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