The oral-gut axis: Salivary and fecal microbiome dysbiosis in patients with inflammatory bowel disease

Abstract

Inflammatory bowel disease (IBD) is a group of chronic inflammatory disorders that fall into two main categories: Crohn’s disease (CD) and ulcerative colitis (UC). The gastrointestinal tract extends from the mouth to the anus and harbors diverse bacterial communities. Several sequencing-based studies have identified an intestinal enrichment of oral-associated bacteria and demonstrated their ability to induce intestinal inflammation in mice, suggesting that intestinal pathobionts originate from the oral cavity, particularly members of the genus Streptococcus. This study aimed to investigate the composition of the salivary and fecal microbiome of IBD patients (n = 14) compared to healthy controls (n = 12) and to determine the abundance of common bacterial taxa in both niches. Metagenomic DNA was extracted from saliva and fecal samples, and the 16S rRNA gene was targeted for sequencing. Our results revealed that the overall microbial composition of saliva was significantly altered in the IBD patients compared to the control subjects (p = 0.038). At the genus level, Veillonella and Prevotella were highly abundant in IBD (median: 25.4% and 22.2%, respectively) compared to the control group (17.9% and 13.4%, respectively). In contrast, Neisseria, Streptococcus, Haemophilus, and Fusobacterium were associated with a healthy gut state. Regarding the fecal microbiome, the IBD group had a significantly higher abundance of Clostridium sensu stricto 1 and Escherichia-Shigella (both comprising pathogenic bacteria) compared with the control group. Members of both bacterial groups have previously been shown to positively correlate with intestinal inflammation and high expression of pro-inflammatory cytokines that disrupt intestinal barrier integrity. In addition, we demonstrate that the increased abundance of Clostridium sensu stricto 1 and Escherichia-Shigella has also been associated with significant upregulation of certain metabolic pathways in the feces of the IBD group, including bacterial invasion of epithelial cells. Streptococcus was the only common genus detected in both the salivary and fecal microbiome and represented the oral-gut axis in our study. Using culture-based methods, we isolated 57 and 91 Streptococcus strains from saliva as well as 40 and 31 strains from fecal samples of the controls and IBD patients, respectively. The phylogenetic tree of streptococci based on sodA sequences revealed several patient-specific clusters comprising salivary and fecal streptococcal isolates from the same patient and belonging to the same species, suggesting that the oral cavity is an endogenous reservoir for intestinal strains.

Gum-gut axis: The potential role of salivary biomarkers in the diagnosis and monitoring progress of inflammatory bowel diseases

“…Although salivary microbial alterations have not been studied extensively, available evidence suggests an association between certain aberrations in salivary microorganisms and IBD especially in terms of relative microbial abundance. In a recent study, Abdelbary et al (2022) were able to show that IBD patients' saliva contained more Veillonella and Prevotella on a relative basis than did those of healthy people. Conversely, IBD-free individuals had higher levels of salivary Neisseria , Streptococcus , Haemophilus , and Fusobacterium ( Abdelbary et al, 2022 ).…”

“…In a recent study, Abdelbary et al (2022) were able to show that IBD patients' saliva contained more Veillonella and Prevotella on a relative basis than did those of healthy people. Conversely, IBD-free individuals had higher levels of salivary Neisseria , Streptococcus , Haemophilus , and Fusobacterium ( Abdelbary et al, 2022 ). Prevotella was more prevalent, and Neisseria was less prevalent in active CD compared to remission phase and healthy controls ( Zhang et al, 2020 ).…”

Effect of Periodontitis and Periodontal Therapy on Oral and Gut Microbiota

“…Although some preliminary studies have focused on comparing the oral and enteral microbiota in inflammatory bowel diseases and cirrhosis (Bajaj et al 2018; Abdelbary et al 2022), data on the gut microbial profile of patients with periodontitis are still limited. Our baseline findings are somehow consistent with the study of Lourenço et al (2022) and Bao et al (2022), which reported differences in the gut microbial composition in a smaller group of patients.…”

Two putative glutamate decarboxylases of Streptococcus pneumoniae as possible antigens for the production of anti-GAD65 antibodies leading to type 1 diabetes mellitus

“…In general, dysbiosis is characterized by low microbial diversity and prevalence of pathogenic bacteria. Most studies showing the involvement of dysbiosis in a variety of human diseases have been performed mainly with the gut and/or oral microbiomes (see Suárez et al 2020 ; Abdelbary et al 2022 ; Afzaal et al 2022 for recent reviews). Particularly, gut dysbiosis is thought to be linked to various human diseases, such as type 1 diabetes mellitus (T1DM), cardiovascular diseases, obesity, inflammatory bowel disease, or cancer, although the mechanisms over gut microbiota exerting its positive or harmful impacts remain largely unclear (Afzaal et al 2022 ; Majumdar et al 2022 ).…”