Intratumoral microbiome is driven by metastatic site and associated with immune histopathological parameters: An ancillary study of the SHIVA clinical trial.

Ancillary study Immunity Metastases Microbiota Targeted sequencing

Journal

European journal of cancer (Oxford, England : 1990)
ISSN: 1879-0852
Titre abrégé: Eur J Cancer
Pays: England
ID NLM: 9005373

Informations de publication

Date de publication:
04 2023
Historique:
received: 29 10 2022
revised: 14 01 2023
accepted: 25 01 2023
pubmed: 4 3 2023
medline: 21 3 2023
entrez: 3 3 2023
Statut: ppublish

Résumé

Data on the role of the microbiota in cancer have accumulated in recent years, with particular interest in intratumoral bacteria. Previous results have shown that the composition of intratumoral microbiome is different depending on the type of primary tumour and that bacteria from the primary tumour could migrate to metastatic sites. Seventy-nine patients with breast, lung, or colorectal cancer and available biopsy samples from lymph node, lung, or liver site, treated in the SHIVA01 trial were analysed. We performed bacterial 16S rRNA gene sequencing on these samples to characterise the intratumoral microbiome. We assessed the association between microbiome composition, clinicopathological characteristics, and outcomes. Microbial richness (Chao1 index), evenness (Shannon index) and beta-diversity (Bray Curtis distance) were associated with biopsy site (p = 0.0001, p = 0.03 and p < 0.0001, respectively) but not with primary tumour type (p = 0.52, p = 0.54 and p = 0.82, respectively). Furthermore, microbial richness was inversely associated with tumour-infiltrating lymphocytes (TILs, p = 0.02), and PD-L1 expression on immune cells (p = 0.03), or assessed by Tumor Proportion Score (TPS, p = 0.02) or Combined Positive Score (CPS, p = 0.04). Beta-diversity was also associated with these parameters (p < 0.05). Patients with lower intratumoral microbiome richness had shorter overall survival (p = 0.03) and progression-free survival (p = 0.02) in multivariate analysis. Biopsy site, rather than primary tumour type, was strongly associated with microbiome diversity. Immune histopathological parameters such as PD-L1 expression and TILs were significantly associated with alpha and beta-diversity supporting the cancer-microbiome-immune axis hypothesis.

Sections du résumé

BACKGROUND
Data on the role of the microbiota in cancer have accumulated in recent years, with particular interest in intratumoral bacteria. Previous results have shown that the composition of intratumoral microbiome is different depending on the type of primary tumour and that bacteria from the primary tumour could migrate to metastatic sites.
METHODS
Seventy-nine patients with breast, lung, or colorectal cancer and available biopsy samples from lymph node, lung, or liver site, treated in the SHIVA01 trial were analysed. We performed bacterial 16S rRNA gene sequencing on these samples to characterise the intratumoral microbiome. We assessed the association between microbiome composition, clinicopathological characteristics, and outcomes.
RESULTS
Microbial richness (Chao1 index), evenness (Shannon index) and beta-diversity (Bray Curtis distance) were associated with biopsy site (p = 0.0001, p = 0.03 and p < 0.0001, respectively) but not with primary tumour type (p = 0.52, p = 0.54 and p = 0.82, respectively). Furthermore, microbial richness was inversely associated with tumour-infiltrating lymphocytes (TILs, p = 0.02), and PD-L1 expression on immune cells (p = 0.03), or assessed by Tumor Proportion Score (TPS, p = 0.02) or Combined Positive Score (CPS, p = 0.04). Beta-diversity was also associated with these parameters (p < 0.05). Patients with lower intratumoral microbiome richness had shorter overall survival (p = 0.03) and progression-free survival (p = 0.02) in multivariate analysis.
CONCLUSION
Biopsy site, rather than primary tumour type, was strongly associated with microbiome diversity. Immune histopathological parameters such as PD-L1 expression and TILs were significantly associated with alpha and beta-diversity supporting the cancer-microbiome-immune axis hypothesis.

Identifiants

pubmed: 36868056
pii: S0959-8049(23)00048-5
doi: 10.1016/j.ejca.2023.01.024
pii:
doi:

Substances chimiques

B7-H1 Antigen 0
RNA, Ribosomal, 16S 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

152-161

Informations de copyright

Copyright © 2023 Elsevier Ltd. All rights reserved.

Auteurs

Marc Hilmi (M)

Molecular Oncology, PSL Research University, CNRS, UMR 144, Institut Curie, Paris 75005, France; Paris Center for Microbiome Medicine, Fédération Hospitalo-Universitaire, Paris, France; Medical Oncology Department, Institut Curie, Saint-Cloud 92210, France. Electronic address: marc.hilmi@curie.fr.

Maud Kamal (M)

Department of Drug Development and Innovation (D3i), Institut Curie, Paris-Saclay University, Paris, France.

Sophie Vacher (S)

Department of Genetics, Institut Curie, PSL Research University, Paris 75005, France.

Célia Dupain (C)

Department of Drug Development and Innovation (D3i), Institut Curie, Paris-Saclay University, Paris, France.

Sabrina Ibadioune (S)

Department of Genetics, Institut Curie, PSL Research University, Paris 75005, France.

Maral Halladjian (M)

Department of Drug Development and Innovation (D3i), Institut Curie, Paris-Saclay University, Paris, France.

Marie Paule Sablin (MP)

Department of Drug Development and Innovation (D3i), Institut Curie, Paris-Saclay University, Paris, France.

Grégoire Marret (G)

Department of Drug Development and Innovation (D3i), Institut Curie, Paris-Saclay University, Paris, France.

Zahra Castel Ajgal (ZC)

Department of Drug Development and Innovation (D3i), Institut Curie, Paris-Saclay University, Paris, France.

Michèle Nijnikoff (M)

Institut Curie, PSL Research University, Biological Resource Center, Paris 75248, France.

Anne Salomon (A)

Pathology Department, Institut Curie, 75005 Paris, France.

Zakhia El Beaino (Z)

Pathology Department, Hopital Tenon, 75020 Paris, France.

Nicolas Servant (N)

INSERM U900, Mines Paris Tech, Institut Curie, Paris 75000, France.

Sylvain Dureau (S)

Statistics Department, Institut Curie, Saint-Cloud 92210, France.

Harry Sokol (H)

Paris Center for Microbiome Medicine, Fédération Hospitalo-Universitaire, Paris, France; Sorbonne University, INSERM, Centre de Recherche Saint-Antoine, CRSA, AP-HP, Saint Antoine Hospital, Gastroenterology Department, Paris 75012, France; INRA, UMR1319 Micalis & AgroParisTech, Jouy en Josas, France.

Remy Nicolle (R)

Université Paris Cité, Centre de Recherche sur L'Inflammation (CRI), INSERM, U1149, CNRS, ERL 8252, Paris F-75018, France.

Christophe Le Tourneau (C)

Department of Drug Development and Innovation (D3i), Institut Curie, Paris-Saclay University, Paris, France.

Ivan Bieche (I)

Department of Genetics, Institut Curie, PSL Research University, Paris 75005, France; INSERM U1016, Faculty of Pharmaceutical and Biological Sciences, Paris Cité University, Paris, France.

Cindy Neuzillet (C)

Molecular Oncology, PSL Research University, CNRS, UMR 144, Institut Curie, Paris 75005, France; Paris Center for Microbiome Medicine, Fédération Hospitalo-Universitaire, Paris, France; Medical Oncology Department, Institut Curie, Saint-Cloud 92210, France.

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