Intraindividual variation in core microbiota in peri-implantitis and periodontitis

Noriko Maruyama, Fumito Maruyama, Yasuo Takeuchi, Chihiro Aikawa, Yuichi Izumi, Ichiro Nakagawa, Noriko Maruyama, Fumito Maruyama, Yasuo Takeuchi, Chihiro Aikawa, Yuichi Izumi, Ichiro Nakagawa

Abstract

The oral microbiota change dramatically with each part of the oral cavity, even within the same mouth. Nevertheless, the microbiota associated with peri-implantitis and periodontitis have been considered the same. To improve our knowledge of the different communities of complex oral microbiota, we compared the microbial features between peri-implantitis and periodontitis in 20 patients with both diseases. Although the clinical symptoms of peri-implantitis were similar to those of periodontitis, the core microbiota of the diseases differed. Correlation analysis revealed the specific microbial co-occurrence patterns and found some of the species were associated with the clinical parameters in a disease-specific manner. The proportion of Prevotella nigrescens was significantly higher in peri-implantitis than in periodontitis, while the proportions of Peptostreptococcaceae sp. and Desulfomicrobium orale were significantly higher in periodontitis than in peri-implantitis. The severity of the peri-implantitis was also species-associated, including with an uncultured Treponema sp. that correlated to 4 clinical parameters. These results indicate that peri-implantitis and periodontitis are both polymicrobial infections with different causative pathogens. Our study provides a framework for the ecologically different bacterial communities between peri-implantitis and periodontitis, and it will be useful for further studies to understand the complex microbiota and pathogenic mechanisms of oral polymicrobial diseases.

Figures

Figure 1. Circular maximum likelihood phylogenetic tree…
Figure 1. Circular maximum likelihood phylogenetic tree at the genus level.
The inner band shows the genera coloured by phylum (see key for taxa with multiple members). The outer bands show the relative abundance: red for peri-implantitis, blue for periodontitis, and green for overall relative abundance. The tree was constructed with the Interactive Tree of Life tool and the taxonomic names were based on results from the Ribosomal Database Project classifier. The statistical differences were calculated by Wilcoxon signed rank tests. *P <0.05 and q <0.1.
Figure 2. Principal coordinate analysis (PCoA) and…
Figure 2. Principal coordinate analysis (PCoA) and microbial differences at the species level.
(a) PCoA plots of the unweighted UniFrac distances for the samples by disease. (b) The most abundant species (>0.5% abundance) in the peri-implantitis and periodontitis samples. The species name or Human Oral Taxon (HOT) ID in the Human Oral Microbiome is shown. The taxonomy assignments were based on information in the Human Oral Microbiome Database, and the statistical differences were calculated by Wilcoxon signed rank tests. *P <0.05 and q <0.1.
Figure 3. The microbiota associated with peri-implantitis.
Figure 3. The microbiota associated with peri-implantitis.
(a) The core microbiota of peri-implantitis and periodontitis. The model includes the species detected at peri-implantitis (red), periodontitis (blue), and both sites (green), where the species were found in at least 50% of patients with a mean relative abundance of >1%, or were statistically different (outside of the square boxes; see Figure 2b). The species detected in at least 80% of patients in both sites are indicated in bold. The inner box labelled with 1 indicates a mean relative abundance of ≥2% in periodontitis and Peptostreptococcaceae [XI][G-4] sp. HOT369 is statistically abundant, although showed a mean relative abundance of <1% in periodontitis (see Figure 2b). The species name or Human Oral Taxon (HOT) ID in the Human Oral Microbiome Database is shown. The statistical differences were calculated by Wilcoxon signed rank tests. *P <0.05 and q <0.1. (b) Bacterial taxa associated with the progression of peri-implantitis. The model represents all bacterial taxa associated with each of the four clinical parameters of peri-implantitis (P <0.05 and q <0.1). The species name or HOT ID is shown. The taxa correlated to four parameters (red box) and three parameters (black boxes) are shown. PPD, probing pocket depth; CAL, clinical attachment loss.
Figure 4. Co-occurrence and co-exclusion analysis of…
Figure 4. Co-occurrence and co-exclusion analysis of the bacterial taxa.
Co-occurrence and co-exclusion were calculated by Spearman rank correlations between the abundant bacterial taxa. The co-occurrence of the top 30 species in the peri-implantitis and periodontitis samples is shown on the right and left, respectively. The species name or Human Oral Taxon ID in the Human Oral Microbiome Database is shown. The correlation values range from -1.00 (green) to 1.00 (red).

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