Dietary pattern and the corresponding gut microbiome in response to immunotherapy in Thai patients with advanced non-small cell lung cancer (NSCLC)

Abstract Gut microbiota is considered a key player modulating the response to immune checkpoint inhibitors (ICI) in cancer. The effects of dietary pattern on this interaction is not well-studied. A prospective multicenter cohort of 95 patients with advanced non-small cell lung cancer (NSCLC) undergo...

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Main Authors: Piyada Sitthideatphaiboon, Nicha Somlaw, Nicha Zungsontiporn, Pongsakorn Ouwongprayoon, Narittee Sukswai, Krittiya Korphaisarn, Naravat Poungvarin, Chatchawit Aporntewan, Nattiya Hirankarn, Chanida Vinayanuwattikun, Vinayanuwattikun Chanida
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Language:English
Published: Nature Portfolio 2024-11-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-024-79339-6
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author Piyada Sitthideatphaiboon
Nicha Somlaw
Nicha Zungsontiporn
Pongsakorn Ouwongprayoon
Narittee Sukswai
Krittiya Korphaisarn
Naravat Poungvarin
Chatchawit Aporntewan
Nattiya Hirankarn
Chanida Vinayanuwattikun
Vinayanuwattikun Chanida
author_facet Piyada Sitthideatphaiboon
Nicha Somlaw
Nicha Zungsontiporn
Pongsakorn Ouwongprayoon
Narittee Sukswai
Krittiya Korphaisarn
Naravat Poungvarin
Chatchawit Aporntewan
Nattiya Hirankarn
Chanida Vinayanuwattikun
Vinayanuwattikun Chanida
author_sort Piyada Sitthideatphaiboon
collection DOAJ
description Abstract Gut microbiota is considered a key player modulating the response to immune checkpoint inhibitors (ICI) in cancer. The effects of dietary pattern on this interaction is not well-studied. A prospective multicenter cohort of 95 patients with advanced non-small cell lung cancer (NSCLC) undergoing ICI therapy were enrolled. Stool shotgun metagenomic sequencing was performed. Three-day dietary patterns before ICI were assessed. Patients were categorized as hyperprogressive disease (HPD) if they exhibited a time to treatment failure of less than 2 months. All others were categorized as non-hyperprogressive disease (non-HPD). The correlation between dietary patterns, gut microbiome, and response to ICI therapy was analyzed. In the multivariate analysis, a high abundance of Firmicutes unclassified and the Ruminococcaceae family correlated with a significantly diminished progression-free survival (PFS) with an HR of 2.40 [P = 0.006] and 4.30 [P = 0.005], respectively. More specifically, within the subset of NSCLC patients treated solely with ICI therapy, a high abundance of Intestinimonas and the Enterobacteriaceae family were associated with substantially reduced PFS with an HR of 2.61 [P = 0.02] and HR 3.34 [P = 0.005], respectively. In our comprehensive dietary pattern analysis, the HPD group showed increased consumption of cholesterol, sodium, and fats beyond recommended levels compared to the non-HPD group. This group also displayed a tendency towards higher food pattern scores characterized by a high intake of fat and dairy products. Our study revealed a distinct association between the gut microbiome composition and treatment outcomes. The overall composition of diet might be related to ICI therapeutic outcomes.
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spelling doaj-art-482c069cc9b44a9f87daa90e16e99eb32024-11-17T12:18:55ZengNature PortfolioScientific Reports2045-23222024-11-0114111210.1038/s41598-024-79339-6Dietary pattern and the corresponding gut microbiome in response to immunotherapy in Thai patients with advanced non-small cell lung cancer (NSCLC)Piyada Sitthideatphaiboon0Nicha Somlaw1Nicha Zungsontiporn2Pongsakorn Ouwongprayoon3Narittee Sukswai4Krittiya Korphaisarn5Naravat Poungvarin6Chatchawit Aporntewan7Nattiya Hirankarn8Chanida Vinayanuwattikun9Vinayanuwattikun Chanida10Division of Medical Oncology, Department of Medicine, Faculty of Medicine, Chulalongkorn University and The King Chulalongkorn Memorial HospitalDivision of Clinical Nutrition, Department of Medicine, Faculty of Medicine, Chulalongkorn University and The King Chulalongkorn, Memorial HospitalDivision of Medical Oncology, Department of Medicine, Faculty of Medicine, Chulalongkorn University and The King Chulalongkorn Memorial HospitalDepartment of Radiology, Faculty of Medicine, Chulalongkorn University and King Chulalongkorn Memorial HospitalPrecision Pathology of Neoplasia Research Group, Department of Pathology, Faculty of Medicine, Chulalongkorn University and The King Chulalongkorn Memorial HospitalDivision of Medical Oncology, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol UniversityDepartment of Clinical Pathology, Faculty of Medicine Siriraj Hospital, Mahidol UniversityDepartment of Mathematics and Computer Science & Omics Sciences and Bioinformatics Center, Faculty of Science, Chulalongkorn UniversityCenter of Excellence in Immunology and Immune-mediated Diseases, Department of Microbiology, Faculty of Medicine, Chulalongkorn University and The King Chulalongkorn Memorial HospitalDivision of Medical Oncology, Department of Medicine, Faculty of Medicine, Chulalongkorn University and The King Chulalongkorn Memorial HospitalDivision of Medical Oncology, Department of Medicine, Faculty of Medicine, Chulalongkorn University and The King Chulalongkorn Memorial HospitalAbstract Gut microbiota is considered a key player modulating the response to immune checkpoint inhibitors (ICI) in cancer. The effects of dietary pattern on this interaction is not well-studied. A prospective multicenter cohort of 95 patients with advanced non-small cell lung cancer (NSCLC) undergoing ICI therapy were enrolled. Stool shotgun metagenomic sequencing was performed. Three-day dietary patterns before ICI were assessed. Patients were categorized as hyperprogressive disease (HPD) if they exhibited a time to treatment failure of less than 2 months. All others were categorized as non-hyperprogressive disease (non-HPD). The correlation between dietary patterns, gut microbiome, and response to ICI therapy was analyzed. In the multivariate analysis, a high abundance of Firmicutes unclassified and the Ruminococcaceae family correlated with a significantly diminished progression-free survival (PFS) with an HR of 2.40 [P = 0.006] and 4.30 [P = 0.005], respectively. More specifically, within the subset of NSCLC patients treated solely with ICI therapy, a high abundance of Intestinimonas and the Enterobacteriaceae family were associated with substantially reduced PFS with an HR of 2.61 [P = 0.02] and HR 3.34 [P = 0.005], respectively. In our comprehensive dietary pattern analysis, the HPD group showed increased consumption of cholesterol, sodium, and fats beyond recommended levels compared to the non-HPD group. This group also displayed a tendency towards higher food pattern scores characterized by a high intake of fat and dairy products. Our study revealed a distinct association between the gut microbiome composition and treatment outcomes. The overall composition of diet might be related to ICI therapeutic outcomes.https://doi.org/10.1038/s41598-024-79339-6Non-small cell lung cancerGut microbiomeImmune checkpoints inhibitorsAnti-PD-1/PD-L1 immunotherapyDietNutrition
spellingShingle Piyada Sitthideatphaiboon
Nicha Somlaw
Nicha Zungsontiporn
Pongsakorn Ouwongprayoon
Narittee Sukswai
Krittiya Korphaisarn
Naravat Poungvarin
Chatchawit Aporntewan
Nattiya Hirankarn
Chanida Vinayanuwattikun
Vinayanuwattikun Chanida
Dietary pattern and the corresponding gut microbiome in response to immunotherapy in Thai patients with advanced non-small cell lung cancer (NSCLC)
Scientific Reports
Non-small cell lung cancer
Gut microbiome
Immune checkpoints inhibitors
Anti-PD-1/PD-L1 immunotherapy
Diet
Nutrition
title Dietary pattern and the corresponding gut microbiome in response to immunotherapy in Thai patients with advanced non-small cell lung cancer (NSCLC)
title_full Dietary pattern and the corresponding gut microbiome in response to immunotherapy in Thai patients with advanced non-small cell lung cancer (NSCLC)
title_fullStr Dietary pattern and the corresponding gut microbiome in response to immunotherapy in Thai patients with advanced non-small cell lung cancer (NSCLC)
title_full_unstemmed Dietary pattern and the corresponding gut microbiome in response to immunotherapy in Thai patients with advanced non-small cell lung cancer (NSCLC)
title_short Dietary pattern and the corresponding gut microbiome in response to immunotherapy in Thai patients with advanced non-small cell lung cancer (NSCLC)
title_sort dietary pattern and the corresponding gut microbiome in response to immunotherapy in thai patients with advanced non small cell lung cancer nsclc
topic Non-small cell lung cancer
Gut microbiome
Immune checkpoints inhibitors
Anti-PD-1/PD-L1 immunotherapy
Diet
Nutrition
url https://doi.org/10.1038/s41598-024-79339-6
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