Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seedingResearch in context
Summary: 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 r...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2024-01-01
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| Series: | EBioMedicine |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2352396423004838 |
| _version_ | 1827581168964337664 |
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| author | Mireia Valles-Colomer Paolo Manghi Fabio Cumbo Giulia Masetti Federica Armanini Francesco Asnicar Aitor Blanco-Miguez Federica Pinto Michal Punčochář Alberto Garaventa Loredana Amoroso Mirco Ponzoni Maria Valeria Corrias Nicola Segata |
| author_facet | Mireia Valles-Colomer Paolo Manghi Fabio Cumbo Giulia Masetti Federica Armanini Francesco Asnicar Aitor Blanco-Miguez Federica Pinto Michal Punčochář Alberto Garaventa Loredana Amoroso Mirco Ponzoni Maria Valeria Corrias Nicola Segata |
| author_sort | Mireia Valles-Colomer |
| collection | DOAJ |
| description | Summary: 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. Funding: 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). |
| first_indexed | 2024-03-08T22:31:32Z |
| format | Article |
| id | doaj.art-95f96e5e99c2418982e3fa0c8a1dbe95 |
| institution | Directory Open Access Journal |
| issn | 2352-3964 |
| language | English |
| last_indexed | 2024-03-08T22:31:32Z |
| publishDate | 2024-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | EBioMedicine |
| spelling | doaj.art-95f96e5e99c2418982e3fa0c8a1dbe952023-12-18T04:24:18ZengElsevierEBioMedicine2352-39642024-01-0199104917Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seedingResearch in contextMireia Valles-Colomer0Paolo Manghi1Fabio Cumbo2Giulia Masetti3Federica Armanini4Francesco Asnicar5Aitor Blanco-Miguez6Federica Pinto7Michal Punčochář8Alberto Garaventa9Loredana Amoroso10Mirco Ponzoni11Maria Valeria Corrias12Nicola Segata13Department CIBIO, University of Trento, Trento, Italy; MELIS Department, Pompeu Fabra University, Barcelona, Spain; Corresponding author. Department CIBIO, University of Trento, Trento, Italy.Department CIBIO, University of Trento, Trento, ItalyDepartment CIBIO, University of Trento, Trento, ItalyDepartment CIBIO, University of Trento, Trento, ItalyDepartment CIBIO, University of Trento, Trento, ItalyDepartment CIBIO, University of Trento, Trento, ItalyDepartment CIBIO, University of Trento, Trento, ItalyDepartment CIBIO, University of Trento, Trento, ItalyDepartment CIBIO, University of Trento, Trento, ItalyOncology Unit, IRCCS Istituto Giannina Gaslini, Genoa, ItalyOncology Unit, IRCCS Istituto Giannina Gaslini, Genoa, ItalyLaboratory of Experimental Therapies in Oncology, IRCCS Istituto Giannina Gaslini, Genoa, ItalyLaboratory of Experimental Therapies in Oncology, IRCCS Istituto Giannina Gaslini, Genoa, ItalyDepartment CIBIO, University of Trento, Trento, Italy; Department of Experimental Oncology, IEO European Institute of Oncology IRCCS, Milan, Italy; Corresponding author. Department CIBIO, University of Trento, Trento, Italy.Summary: 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. Funding: 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).http://www.sciencedirect.com/science/article/pii/S2352396423004838NeuroblastomaPaediatric cancerGut microbiomeMetagenomicsMother-infant transmission |
| spellingShingle | Mireia Valles-Colomer Paolo Manghi Fabio Cumbo Giulia Masetti Federica Armanini Francesco Asnicar Aitor Blanco-Miguez Federica Pinto Michal Punčochář Alberto Garaventa Loredana Amoroso Mirco Ponzoni Maria Valeria Corrias Nicola Segata Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seedingResearch in context EBioMedicine Neuroblastoma Paediatric cancer Gut microbiome Metagenomics Mother-infant transmission |
| title | Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seedingResearch in context |
| title_full | Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seedingResearch in context |
| title_fullStr | Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seedingResearch in context |
| title_full_unstemmed | Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seedingResearch in context |
| title_short | Neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seedingResearch in context |
| title_sort | neuroblastoma is associated with alterations in gut microbiome composition subsequent to maternal microbial seedingresearch in context |
| topic | Neuroblastoma Paediatric cancer Gut microbiome Metagenomics Mother-infant transmission |
| url | http://www.sciencedirect.com/science/article/pii/S2352396423004838 |
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