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

Marcos Pérez-Losada; Eduardo Castro-Nallar; José Laerte Boechat; Luís Delgado; Tiago Azenha Rama; Valentín Berrios-Farías; Manuela Oliveira

doi:10.3389/fmicb.2023.1197135

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

Front Microbiol. 2023 Jun 7:14:1197135. doi: 10.3389/fmicb.2023.1197135. eCollection 2023.

Authors

Marcos Pérez-Losada^{1

2}, Eduardo Castro-Nallar^{3

4}, José Laerte Boechat^{5

6}, Luís Delgado^{5

6

7}, Tiago Azenha Rama^{5

7}, Valentín Berrios-Farías^{3

4}, Manuela Oliveira^{8

9}

Affiliations

¹ Department of Biostatistics and Bioinformatics, Computational Biology Institute, Milken Institute School of Public Health, The George Washington University, Washington, DC, United States.
² CIBIO-InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus Agrário de Vairão, Vairão, Portugal.
³ Departamento de Microbiología, Facultad de Ciencias de la Salud, Universidad de Talca, Campus Talca, Talca, Chile.
⁴ Centro de Ecología Integrativa, Universidad de Talca, Campus Talca, Talca, Chile.
⁵ Serviço de Imunologia Básica e Clínica, Departamento de Patologia, Faculdade de Medicina da Universidade do Porto, Porto, Portugal.
⁶ Centro de Investigação em Tecnologias e Serviços de Saúde (CINTESIS@RISE), Faculdade de Medicina da Universidade do Porto, Porto, Portugal.
⁷ Serviço de Imunoalergologia, Centro Hospitalar Universitário São João (CHUSJ), Porto, Portugal.
⁸ i3S-Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal.
⁹ Ipatimup-Instituto de Patologia e Imunologia Molecular da Universidade do Porto, Porto, Portugal.

Abstract

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.

Keywords: 16S rRNA; Portugal; allergy; asthma; bacteriome; oral cavity; rhinitis.