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Salivary microbiota and metabolome associated with celiac disease
Ruggiero Francavilla1, Danilo Ercolini, Maria Piccolo
1Department of Interdisciplinary Medicine, University of Bari Aldo Moro, Bari, Italy.
Insights
Children with celiac disease (CD) on a gluten-free diet exhibit oral dysbiosis, altering salivary microbiota and metabolome. This study found distinct bacterial and volatile organic compound profiles in treated celiac disease (T-CD) children compared to healthy controls.
Area of Science:
- Microbiology
- Metabolomics
- Gastroenterology
Background:
- Celiac disease (CD) is an autoimmune disorder triggered by gluten ingestion.
- Dietary management with a gluten-free diet (GFD) is the primary treatment for CD.
- The impact of treated celiac disease (T-CD) on the oral microbiome and metabolome remains incompletely understood.
Purpose of the Study:
- To investigate the salivary microbiota composition in children with T-CD compared to healthy children (HC).
- To analyze the salivary metabolome, specifically volatile organic compounds (VOCs), in children with T-CD versus HC.
- To explore potential correlations between salivary bacterial profiles and VOCs in T-CD.
Main Methods:
- Integrated analysis of salivary microbiota using culture-dependent and -independent (pyrosequencing) methods.
- Metabolome analysis of saliva using gas chromatography-mass spectrometry-solid-phase microextraction.
- Multivariate statistical analyses to differentiate T-CD children based on VOC profiles and identify correlations.
Main Results:
- Significant differences in cultivable bacterial groups and overall microbial diversity (Shannon's index, richness) between T-CD and HC groups.
- Distinct bacterial abundances in T-CD, including higher Lachnospiraceae, Gemellaceae, Streptococcus sanguinis, and Bacteroidetes, with lower Streptococcus thermophilus and Actinobacteria.
- Specific VOCs (ethyl-acetate, nonanal, 2-hexanone) were associated with T-CD, and correlations were found between bacterial abundances and VOCs.
Conclusions:
- Celiac disease, even when treated with a gluten-free diet, is associated with oral dysbiosis.
- The salivary metabolome, characterized by specific volatile organic compounds, is altered in children with treated celiac disease.
- These oral microbiome and metabolome alterations may have implications for understanding celiac disease pathogenesis and progression.
Abstract:
This study aimed to investigate the salivary microbiota and metabolome of 13 children with celiac disease (CD) under a gluten-free diet (treated celiac disease [T-CD]). The same number of healthy children (HC) was used as controls. The salivary microbiota was analyzed by an integrated approach using culture-dependent and -independent methods. Metabolome analysis was carried out by gas chromatography-mass spectrometry-solid-phase microextraction. Compared to HC, the number of some cultivable bacterial groups (e.g., total anaerobes) significantly (P < 0.05) differed in the saliva samples of the T-CD children. As shown by community-level catabolic profiles, the highest Shannon's diversity and substrate richness were found in HC. Pyrosequencing data showed the highest richness estimator and diversity index values for HC. Levels of Lachnospiraceae, Gemellaceae, and Streptococcus sanguinis were highest for the T-CD children. Streptococcus thermophilus levels were markedly decreased in T-CD children. The saliva of T-CD children showed the largest amount of Bacteroidetes (e.g., Porphyromonas sp., Porphyromonas endodontalis, and Prevotella nanceiensis), together with the smallest amount of Actinobacteria. T-CD children were also characterized by decreased levels of some Actinomyces species, Atopobium species, and Corynebacterium durum. Rothia mucilaginosa was the only Actinobacteria species found at the highest level in T-CD children. As shown by multivariate statistical analyses, the levels of organic volatile compounds markedly differentiated T-CD children. Some compounds (e.g., ethyl-acetate, nonanal, and 2-hexanone) were found to be associated with T-CD children. Correlations (false discovery rate [FDR], <0.05) were found between the relative abundances of bacteria and some volatile organic compounds (VOCs). The findings of this study indicated that CD is associated with oral dysbiosis that could affect the oral metabolome.
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