Oral-to-rectum microbial transmission in orthopedic patients without a history of intestinal disorders

Abstract

The enrichment of oral taxa in the gut has recently been reported as a notable alteration in the microbial balance in patients with intestinal disorders. However, translocation in populations without such diseases remains controversial. In this study, we examined 49 pairs of tongue and rectal samples collected from orthopedic patients without a history of intestinal disorders to verify the presence of oral taxa in the rectal microbiota. The bacterial composition of each sample was determined using 16S rRNA gene sequencing and amplicon sequence variant (ASV) analysis. Although the bacterial compositions of the tongue and rectal microbiota were distinctly different, tongue ASVs were detected in 67.3% of the participants and accounted for 0.0%-9.37% of the rectal microbiota. Particularly, Streptococcus salivarius, Fusobacterium nucleatum, and Streptococcus parasanguinis were abundant in the rectal microbiota. According to the network analysis, tongue taxa, such as S. salivarius and S. parasanguinis, formed a cohabiting group with Klebsiella pneumoniae and Alistipes finegoldii in the rectal microbiota. The total abundance of tongue ASVs in the rectal microbiota was significantly higher in participants with older age, hypertension, and proton pump inhibitor (PPI) use. Our study presents an extensive translocation of oral taxa to the rectum of a population without intestinal disorders and suggests that aging, hypertension, and PPI use are associated with an increased abundance of oral taxa and potential pathogenic bacteria in the rectal microbiota.

Keywords: 16S rRNA; aging; gut; hypertension; microbiota; proton pump inhibitor; tongue; translocation.

Figure 1

Bacterial compositions of tongue and rectal microbiota. (A) Principal coordinate analysis plot based on the Bray–Curtis distance at the ASV level. The bacterial composition of tongue and rectal samples is depicted using different colors. The ellipse covers 67% of the samples belonging to each group. (B) Compositional difference between tongue and rectal microbiota. Twenty-nine genera with ≥1% of mean relative abundance in either tongue or rectal microbiota are displayed. (C) Compositional similarity between the tongue and rectal microbiota, the total relative abundance of tongue ASVs in the rectal microbiota, and the percentage of tongue ASVs over the total number of ASVs observed in the rectal microbiota within an individual (intra-pair) and across different individuals (inter-pair). ***P <0.001.

Figure 2

Tongue bacteria in the rectal microbiota. The total relative abundance of tongue amplicon sequence variants (ASVs) in rectal microbiota in each participant is demonstrated in ascending order. The composition is displayed at the species level. Bacterial species with ≥0.5% of mean relative abundance in the rectal microbiota are depicted by different colors. Human microbial taxon numbers in the expanded Human Oral Microbiome Database (eHOMD) are provided in parentheses following bacterial names.

Figure 3

Co-occurrence network in rectal bacterial species. Co-occurrence network analysis is performed for 71 species with ≥0.1% of mean relative abundance in the rectal microbiota. Co-occurrence relationships with the SparCC R values of ≥0.4 are visualized as edges. Bacterial species with ≥0.1% of mean relative abundance in the tongue microbiota are indicated by blue color. Human microbial taxon (HMT) numbers in the expanded Human Oral Microbiome Database (eHOMD) are provided in parentheses following bacterial names. Bacterial names without HMT numbers are assigned based on the SILVA database.

Figure 4

Factors influencing the increased abundance of tongue bacteria in the rectal microbiota. (A) Effects of clinical factors on the total relative abundance of tongue amplicon sequence variants (ASVs) in rectal microbiota. The effect size (η²) and the significance are respectively calculated using the Kruskal–Wallis test. **P <0.01, *P <0.05. (B) Boxplot of the total abundance of tongue ASVs in rectal microbiota according to the factors with significance in the Kruskal–Wallis test. The significance is calculated using the Steel–Dwass test or the exact Wilcoxon rank sum test. **P <0.01; *P <0.05. BMI, body mass index; NSAID, nonsteroidal anti-inflammatory drugs.