The Oral Microbiome across Oral Sites in Cats with Chronic Gingivostomatitis, Periodontal Disease, and Tooth Resorption Compared with Healthy Cats

Abstract

Feline chronic gingivostomatitis (FCGS) is a chronic mucosal and gingival inflammatory disease in which pathogenesis remains unclear. Interactions between the host inflammatory process, the host immune response, and the oral microbiome are implicated in this pathogenesis. To begin to understand this disease and the impact of the microbiome to host inflammatory disease states, we collected sterile noninvasive plaque biofilm samples from ten distinct sites within the oral cavity in cats with stomatitis (n = 12), healthy cats (n = 9), and cats with tooth resorption or periodontitis (n = 11). Analysis of full-length 16S rRNA gene sequences indicated that the microbiomes of cats with FCGS presented marked dysbiosis at multiple oral sites. Additionally, microbiome beta diversity varied with oral condition, indicating that stomatitis, periodontitis, and/or tooth resorption influence the microbiome differently. Lastly, we found that the microbiomes of swabs taken from the oral cavity were comparable to those taken from plaque using endodontic paper points, validating this as another sampling method. Collectively, our work furthers our understanding of the dysbiosis and composition of bacteria in the oral microbiome in FCGS, with hopes of contributing to the prevention, diagnosis, and treatment of this challenging condition in felines.

Keywords: cats; dysbiosis; gingivostomatitis; oral microbiome; periodontal disease; stomatitis; tooth resorption.

Figure 1

Biogeography of the oral microbiomes in healthy cats (left) and cats with FCGS (right). Note that microbiome composition from the deep periodontal pocket and external tooth resorption site are excluded. Plots showing the relative abundances of bacterial genera are on top (A,B) and of bacterial species at the bottom (C,D). Bacterial genera with mean relative abundances <1.28% are encapsulated by the “Other” category.

Figure 2

The oral microbiomes of cats with FCGS are distinct from those of healthy cats. (A) Boxplots of microbiome ASV richness and (B) Pielou’s evenness in plaque samples from eight oral sites, in healthy cats and cats with FCGS. Asterisks *** indicate statistical significance (p = 0.05), ns denotes where difference was not statistically significant. (C) PCA ordinations based on Aitchison distances calculated from bacterial species abundances. PERMANOVA p-values are shown.

Figure 3

The microbiomes of the dorsal tongue and gingival sulcus cluster separately from the microbiomes at other oral sites. (A) PCA ordinations based on Aitchison distances calculated from species-level bacterial abundances, color-coded by oral site. Healthy cats are on the left and cats diagnosed with FCGS are on the right. (B) The same ordination but meant to highlight the separation of two sites (dorsal tongue; gingival sulcus) from the rest.

Figure 4

The oral microbiomes of cats with FCGS have an underrepresentation of 21 bacterial species compared with the oral microbiomes of healthy cats. Results from LinDA differential abundance analyses performed at the (A) bacterial species or (B) bacterial genus level. Bacterial taxa enriched in healthy cats are in pink while those enriched in FCGS cats are in blue.

Figure 5

Microbiome varies with oral condition in felines. (A) Microbiome ASV richness and (B) Pielou’s evenness for plaque samples from cats diagnosed with stomatitis (FCGS), tooth resorption (TR), periodontitis (SPD), or a combination of these conditions. Samples were pooled across oral sites for analysis with GLMMs (Table S9). Asterisks *** indicate statistical significance (p = 0.05), ns denotes where difference was not statistically significant. (C) PCoA ordination based on Bray–Curtis distances showing the clustering of oral microbiome samples by condition. PERMANOVA output is shown.

Figure 6

Oral swab microbiomes are comparable to plaque microbiomes. (A) Relative abundances of bacterial genera in swab samples taken from the oral cavity and in plaque samples taken from the gingival sulcus using endodontic paper points. Bacteria genera with mean relative abundances < 1.27% are represented by the “Other” category. (B) PCoA ordinations based on Bray–Curtis distances. Samples are color-coded by host identity to showcase the similarity between the two sample types. (C) Microbiome similarity (1-Bray–Curtis dissimilarity) between pairs of samples from the same cat or different cats.