Metagenomic characterization of the tracheobronchial microbiome in lung cancer

BackgroundThe tracheobronchial and oral microbiome may be associated with lung cancer, potentially acting as predictive biomarkers. Therefore, we studied the lung and oral bacteriome and virome in non-small cell lung cancer (NSCLC) patients compared to melanoma controls to discover distinguishable f...

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Main Authors: Alexis Bailey, Stephanie Hogue, Christine M. Pierce, Shirlene Paul, Natalie La Fuente, Ram Thapa, Youngchul Kim, Lary A. Robinson
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-11-01
Series:Frontiers in Microbiomes
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Online Access:https://www.frontiersin.org/articles/10.3389/frmbi.2024.1457537/full
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author Alexis Bailey
Stephanie Hogue
Christine M. Pierce
Shirlene Paul
Natalie La Fuente
Ram Thapa
Youngchul Kim
Lary A. Robinson
author_facet Alexis Bailey
Stephanie Hogue
Christine M. Pierce
Shirlene Paul
Natalie La Fuente
Ram Thapa
Youngchul Kim
Lary A. Robinson
author_sort Alexis Bailey
collection DOAJ
description BackgroundThe tracheobronchial and oral microbiome may be associated with lung cancer, potentially acting as predictive biomarkers. Therefore, we studied the lung and oral bacteriome and virome in non-small cell lung cancer (NSCLC) patients compared to melanoma controls to discover distinguishable features that may suggest lung cancer microbial biomarkers.MethodsIn this pilot case-control study, we recruited ten patients with early-stage NSCLC (cases) and ten age-matched melanoma patients (controls) who both underwent tumor resection. Preoperative oral gargles were collected from both groups, who then underwent transbronchoscopic tracheal lavage after intubation. Lung tumor and adjacent non-neoplastic lung were sterilely collected after resection. Microbial DNA from all lung specimens underwent 16S rRNA gene sequencing. Lavage and gargle specimens underwent whole-genome shotgun sequencing. Microbiome metrics were calculated to compare both cohorts. T-tests and Wilcoxon rank sum tests were used to test for significant differences in alpha diversity between cohorts. PERMANOVA was used to compare beta diversity.ResultsNo clear differences were found in the microbial community structure of case and control gargles, but beta diversity of case and control lavages significantly differed. Two species, Granulicatella adiacens and Neisseria subflava, which are both common oral commensal organisms, appeared in much higher abundance in case versus control lavages. Case lavages also maintained higher relative abundances of other oral commensals compared to controls.ConclusionsLung lavages demonstrated oral microbiota enrichment in cases compared to controls, suggesting microaspiration and resultant inflammation. The oral commensals Granulicatella adiacens and Neisseria subflava were more abundant in the tracheobronchial lavages of lung cancer versus melanoma patients, implicating these microorganisms as potential lung cancer biomarkers, warranting further validation studies.
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spelling doaj-art-1e6f20424e564f73adcc83876adb0b792024-11-21T06:23:37ZengFrontiers Media S.A.Frontiers in Microbiomes2813-43382024-11-01310.3389/frmbi.2024.14575371457537Metagenomic characterization of the tracheobronchial microbiome in lung cancerAlexis Bailey0Stephanie Hogue1Christine M. Pierce2Shirlene Paul3Natalie La Fuente4Ram Thapa5Youngchul Kim6Lary A. Robinson7Division of Thoracic Oncology, Moffitt Cancer Center, Tampa, FL, United StatesDepartment of Cancer Epidemiology, Moffitt Cancer Center, Tampa, FL, United StatesDepartment of Cancer Epidemiology, Moffitt Cancer Center, Tampa, FL, United StatesDepartment of Cancer Epidemiology, Moffitt Cancer Center, Tampa, FL, United StatesDepartment of Cancer Epidemiology, Moffitt Cancer Center, Tampa, FL, United StatesDepartment of Biostatistics and Bioinformatics, Moffitt Cancer Center, Tampa, FL, United StatesDepartment of Biostatistics and Bioinformatics, Moffitt Cancer Center, Tampa, FL, United StatesDivision of Thoracic Oncology, Moffitt Cancer Center, Tampa, FL, United StatesBackgroundThe tracheobronchial and oral microbiome may be associated with lung cancer, potentially acting as predictive biomarkers. Therefore, we studied the lung and oral bacteriome and virome in non-small cell lung cancer (NSCLC) patients compared to melanoma controls to discover distinguishable features that may suggest lung cancer microbial biomarkers.MethodsIn this pilot case-control study, we recruited ten patients with early-stage NSCLC (cases) and ten age-matched melanoma patients (controls) who both underwent tumor resection. Preoperative oral gargles were collected from both groups, who then underwent transbronchoscopic tracheal lavage after intubation. Lung tumor and adjacent non-neoplastic lung were sterilely collected after resection. Microbial DNA from all lung specimens underwent 16S rRNA gene sequencing. Lavage and gargle specimens underwent whole-genome shotgun sequencing. Microbiome metrics were calculated to compare both cohorts. T-tests and Wilcoxon rank sum tests were used to test for significant differences in alpha diversity between cohorts. PERMANOVA was used to compare beta diversity.ResultsNo clear differences were found in the microbial community structure of case and control gargles, but beta diversity of case and control lavages significantly differed. Two species, Granulicatella adiacens and Neisseria subflava, which are both common oral commensal organisms, appeared in much higher abundance in case versus control lavages. Case lavages also maintained higher relative abundances of other oral commensals compared to controls.ConclusionsLung lavages demonstrated oral microbiota enrichment in cases compared to controls, suggesting microaspiration and resultant inflammation. The oral commensals Granulicatella adiacens and Neisseria subflava were more abundant in the tracheobronchial lavages of lung cancer versus melanoma patients, implicating these microorganisms as potential lung cancer biomarkers, warranting further validation studies.https://www.frontiersin.org/articles/10.3389/frmbi.2024.1457537/fulllung cancer microbiomenon-small cell lung cancertracheal microbiotaoral microbiotalung microbiomemicroaspiration
spellingShingle Alexis Bailey
Stephanie Hogue
Christine M. Pierce
Shirlene Paul
Natalie La Fuente
Ram Thapa
Youngchul Kim
Lary A. Robinson
Metagenomic characterization of the tracheobronchial microbiome in lung cancer
Frontiers in Microbiomes
lung cancer microbiome
non-small cell lung cancer
tracheal microbiota
oral microbiota
lung microbiome
microaspiration
title Metagenomic characterization of the tracheobronchial microbiome in lung cancer
title_full Metagenomic characterization of the tracheobronchial microbiome in lung cancer
title_fullStr Metagenomic characterization of the tracheobronchial microbiome in lung cancer
title_full_unstemmed Metagenomic characterization of the tracheobronchial microbiome in lung cancer
title_short Metagenomic characterization of the tracheobronchial microbiome in lung cancer
title_sort metagenomic characterization of the tracheobronchial microbiome in lung cancer
topic lung cancer microbiome
non-small cell lung cancer
tracheal microbiota
oral microbiota
lung microbiome
microaspiration
url https://www.frontiersin.org/articles/10.3389/frmbi.2024.1457537/full
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