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The oral bacteriomes of patients with allergic rhinitis and asthma differ from that of healthy controls

Allergic rhinitis and asthma are two of the most common chronic respiratory diseases in developed countries and have become a major public health concern. Substantial evidence has suggested a strong link between respiratory allergy and upper airway dysbacteriosis, but the role of the oral bacteriota...

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Autores principales: Pérez-Losada, Marcos, Castro-Nallar, Eduardo, Laerte Boechat, José, Delgado, Luís, Azenha Rama, Tiago, Berrios-Farías, Valentín, Oliveira, Manuela
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10335798/
https://www.ncbi.nlm.nih.gov/pubmed/37440882
http://dx.doi.org/10.3389/fmicb.2023.1197135
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author Pérez-Losada, Marcos
Castro-Nallar, Eduardo
Laerte Boechat, José
Delgado, Luís
Azenha Rama, Tiago
Berrios-Farías, Valentín
Oliveira, Manuela
author_facet Pérez-Losada, Marcos
Castro-Nallar, Eduardo
Laerte Boechat, José
Delgado, Luís
Azenha Rama, Tiago
Berrios-Farías, Valentín
Oliveira, Manuela
author_sort Pérez-Losada, Marcos
collection PubMed
description Allergic rhinitis and asthma are two of the most common chronic respiratory diseases in developed countries and have become a major public health concern. Substantial evidence has suggested a strong link between respiratory allergy and upper airway dysbacteriosis, but the role of the oral bacteriota is still poorly understood. Here we used 16S rRNA massive parallel sequencing to characterize the oral bacteriome of 344 individuals with allergic rhinitis (AR), allergic rhinitis with asthma (ARAS), asthma (AS) and healthy controls (CT). Four of the most abundant (>2%) phyla (Actinobacteriota, Firmicutes, Fusobacteriota, and Proteobacteria) and 10 of the dominant genera (Actinomyces, Fusobacterium, Gemella, Haemophilus, Leptotrichia, Neisseria, Porphyromonas, Prevotella, Streptococcus, and Veillonella) in the oral cavity differed significantly (p ≤ 0.03) between AR, ARAS or AS and CT groups. The oral bacteriome of ARAS patients showed the highest intra-group diversity, while CT showed the lowest. All alpha-diversity indices of microbial richness and evenness varied significantly (p ≤ 0.022) in ARAS vs. CT and ARAS vs. AR, but they were not significantly different in AR vs. CT. All beta-diversity indices of microbial structure (Unifrac, Bray-Curtis, and Jaccard distances) differed significantly (p ≤ 0.049) between each respiratory disease group and controls. Bacteriomes of AR and ARAS patients showed 15 and 28 upregulated metabolic pathways (PICRUSt2) mainly related to degradation and biosynthesis (p < 0.05). A network analysis (SPIEC-EASI) of AR and ARAS bacteriomes depicted simpler webs of interactions among their members than those observed in the bacteriome of CT, suggesting chronic respiratory allergic diseases may disrupt bacterial connectivity in the oral cavity. This study, therefore, expands our understanding of the relationships between the oral bacteriome and allergy-related conditions. It demonstrates for the first time that the mouth harbors distinct bacteriotas during health and allergic rhinitis (with and without comorbid asthma) and identifies potential taxonomic and functional microbial biomarkers of chronic airway disease.
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spelling pubmed-103357982023-07-12 The oral bacteriomes of patients with allergic rhinitis and asthma differ from that of healthy controls Pérez-Losada, Marcos Castro-Nallar, Eduardo Laerte Boechat, José Delgado, Luís Azenha Rama, Tiago Berrios-Farías, Valentín Oliveira, Manuela Front Microbiol Microbiology Allergic rhinitis and asthma are two of the most common chronic respiratory diseases in developed countries and have become a major public health concern. Substantial evidence has suggested a strong link between respiratory allergy and upper airway dysbacteriosis, but the role of the oral bacteriota is still poorly understood. Here we used 16S rRNA massive parallel sequencing to characterize the oral bacteriome of 344 individuals with allergic rhinitis (AR), allergic rhinitis with asthma (ARAS), asthma (AS) and healthy controls (CT). Four of the most abundant (>2%) phyla (Actinobacteriota, Firmicutes, Fusobacteriota, and Proteobacteria) and 10 of the dominant genera (Actinomyces, Fusobacterium, Gemella, Haemophilus, Leptotrichia, Neisseria, Porphyromonas, Prevotella, Streptococcus, and Veillonella) in the oral cavity differed significantly (p ≤ 0.03) between AR, ARAS or AS and CT groups. The oral bacteriome of ARAS patients showed the highest intra-group diversity, while CT showed the lowest. All alpha-diversity indices of microbial richness and evenness varied significantly (p ≤ 0.022) in ARAS vs. CT and ARAS vs. AR, but they were not significantly different in AR vs. CT. All beta-diversity indices of microbial structure (Unifrac, Bray-Curtis, and Jaccard distances) differed significantly (p ≤ 0.049) between each respiratory disease group and controls. Bacteriomes of AR and ARAS patients showed 15 and 28 upregulated metabolic pathways (PICRUSt2) mainly related to degradation and biosynthesis (p < 0.05). A network analysis (SPIEC-EASI) of AR and ARAS bacteriomes depicted simpler webs of interactions among their members than those observed in the bacteriome of CT, suggesting chronic respiratory allergic diseases may disrupt bacterial connectivity in the oral cavity. This study, therefore, expands our understanding of the relationships between the oral bacteriome and allergy-related conditions. It demonstrates for the first time that the mouth harbors distinct bacteriotas during health and allergic rhinitis (with and without comorbid asthma) and identifies potential taxonomic and functional microbial biomarkers of chronic airway disease. Frontiers Media S.A. 2023-06-07 /pmc/articles/PMC10335798/ /pubmed/37440882 http://dx.doi.org/10.3389/fmicb.2023.1197135 Text en Copyright © 2023 Pérez-Losada, Castro-Nallar, Laerte Boechat, Delgado, Azenha Rama, Berrios-Farías and Oliveira. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Pérez-Losada, Marcos
Castro-Nallar, Eduardo
Laerte Boechat, José
Delgado, Luís
Azenha Rama, Tiago
Berrios-Farías, Valentín
Oliveira, Manuela
The oral bacteriomes of patients with allergic rhinitis and asthma differ from that of healthy controls
title The oral bacteriomes of patients with allergic rhinitis and asthma differ from that of healthy controls
title_full The oral bacteriomes of patients with allergic rhinitis and asthma differ from that of healthy controls
title_fullStr The oral bacteriomes of patients with allergic rhinitis and asthma differ from that of healthy controls
title_full_unstemmed The oral bacteriomes of patients with allergic rhinitis and asthma differ from that of healthy controls
title_short The oral bacteriomes of patients with allergic rhinitis and asthma differ from that of healthy controls
title_sort oral bacteriomes of patients with allergic rhinitis and asthma differ from that of healthy controls
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10335798/
https://www.ncbi.nlm.nih.gov/pubmed/37440882
http://dx.doi.org/10.3389/fmicb.2023.1197135
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