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. 2023 Aug 28;15(1):2250650.
doi: 10.1080/20002297.2023.2250650. eCollection 2023.

Parkinson's disease alters the composition of subgingival microbiome

Ekin Yay  1   2 , Melis Yilmaz  1   2 , Hilal Toygar  2 , Nur Balci  2 , Carla Alvarez Rivas  1   3 , Basak Bolluk Kilic  2 , Ali Zirh  4 , Bruce Paster  1   3 , Alpdogan Kantarci  1   3
Affiliations

Parkinson's disease alters the composition of subgingival microbiome

Ekin Yay et al. J Oral Microbiol. .

Abstract

Aim: The current study aimed to test the hypothesis that Parkinson's disease exacerbates periodontitis by altering its microbiome.

Materials and methods: Clinical periodontal parameters were recorded. Subgingival samples from healthy controls, periodontitis patients (PD), and Parkinson's patients with periodontitis (PA+PD) were analyzed using the checkerboard DNA-DNA hybridization technique for targeting 40 bacterial species typically associated with periodontal disease and health. Next-generation sequencing (NGS) of the 16S ribosomal RNA gene (V1-V3 regions) was performed to analyze the microbiome comprehensively.

Results: Parkinson's patients had mild-to-moderate motor dysfunctions. Bleeding on probing was significantly increased in the PA+PD group compared to PD (p < 0.05). With checkerboard analysis, PA was associated with increased Treponema socranskii (p = 0.0062), Peptostreptococcaceae_[G-6] [Eubacterium]_nodatum (p = 0.0439), Parvimona micra (p < 0.0001), Prevotella melaninogenica (p = 0.0002), Lachnoanaerobaculum saburreum (p < 0.0001), and Streptococcus anginosus (p = 0.0020). Streptococcus intermedia (p = 0.0042), P.nodatum (p = 0.0022), P. micra (p = 0.0002), Treponema denticola (p = 0.0045), L.saburreum (p = 0.0267), P.melaninogenica (p = 0.0017), Campylobacter rectus (p = 0.0020), and T.socranskii (p = 0.0002) were higher; Aggregatibacter actinomycetemcomitans (p = 0.0072) was lower in deep pockets in the PA+PD compared to PD. Schaalia odontolytica (p = 0.0351) and A.actinomycetemcomitans (p = 0.002) were lower; C.rectus (p = 0.0002), P. micra (p = 0065), Streptococcus constellatus (p = 0.0151), T.denticola (p = 0.0141), P.melaninogenica (p = 0.0057), and T.socranskii (p = 0.0316) were higher in shallow pockets in the PA+PD. Diversity decreased in PD (p = 0.001) and PA+PD (p = 0.026) compared to control, with minimal differences in alpha and beta diversities among PD and PA+PD based on NGS results.

Conclusion: These data demonstrated that Parkinson's disease modifies PD-associated subgingival microbiome.

Keywords: Checkerboard; Parkinson’s disease; microbiome; microbiota; pathogenesis; periodontitis.

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Conflict of interest statement

No potential conflict of interest was reported by the author(s).

Figures

Figure 1.
Figure 1.
Mean DNA probe counts of 40 bacterial species in all sites from subgingival plaque samples of HC, PD, and PA+PD groups (x10) [5]. Values present results of 40, 39, and 35 samples from control, periodontitis, and periodontitis-Parkinson’s disease groups, respectively, analyzed with the checkerboard DNA-DNA hybridization technique. Normality was tested with the Kolmogorov-Smirnov test. The Kruskal-Wallis test was used for data not distributed normally, and one-way ANOVA was used for normally distributed data. Bacterial species were arranged by the microbial complexes described by Socransky et al. [10] *Statistically significant difference between HC and PD (p < 0.05), #Statistically significant difference between HC and PA+PD (p < 0.05), †Statistically significant difference between PD and PA+PD (p < 0.05).
Figure 2.
Figure 2.
Group comparisons of subgingival samples from all sites. Mean values of DNA probe counts (x10) [5] of subgingival samples from HC (n = 40), PD (n = 39), and PA+PD (n = 35) patients are represented. Normality was tested with the Kolmogorov-Smirnov test. Kruskal-Wallis test was used for data not distributed normally, and one-way ANOVA was used for normally distributed data. p < 0.05 values are shown on the graphs.
Figure 3.
Figure 3.
Mean DNA probe counts of 40 bacterial species in deep pockets from subgingival plaque samples of HC, PD, and PA+PD groups (x10) [5]. Values present results of 20, 20, and 18 samples from control, periodontitis, and periodontitis-Parkinson’s disease groups, respectively, analyzed with the checkerboard DNA-DNA hybridization technique. Normality was tested with the Kolmogorov-Smirnov test. The Kruskal-Wallis test was used for data not distributed normally, and one-way ANOVA was used for normally distributed data. Bacterial species were arranged in accordance with the microbial complexes described by Socransky et al. [10], *Statistically significant difference between HC and PD (p < 0.05), #Statistically significant difference between HC and PA+PD (p < 0.05), †Statistically significant difference between PD and PA+PD (p < 0.05).
Figure 4.
Figure 4.
Group comparisons of subgingival samples from the deep pockets. Mean values of DNA probe counts (x10) [5] of subgingival samples from HC (n = 20), PD (n = 20), and PA+PD (n = 18) patients are represented. Normality was tested with the Kolmogorov-Smirnov test. Kruskal-Wallis test was used for data not distributed normally, and one-way ANOVA was used for normally distributed data. p < 0.05 values are shown on the graphs.
Figure 5.
Figure 5.
Mean DNA probe counts of 40 bacterial species in shallow pockets from subgingival plaque samples of C, P, and PA+PD groups (x10) [5]. Values present results of 20, 19, and 17 samples from control, periodontitis, and periodontitis-Parkinson’s disease groups, respectively, analyzed with the checkerboard DNA-DNA hybridization technique. Normality was tested with the Kolmogorov-Smirnov test. The Kruskal-Wallis test was used for data not distributed normally, and one-way ANOVA was used for normally distributed data. Bacterial species were arranged in accordance with the microbial complexes described by Socransky et al. [10], *Statistically significant difference between HC and PD (p < 0.05), #Statistically significant difference between HC and PA+PD (p < 0.05), †Statistically significant difference between PD and PA+PD (p < 0.05).
Figure 6.
Figure 6.
Group comparisons of subgingival samples from the shallow pockets. Mean values of DNA probe counts (x10) [5] of subgingival samples from HC (n = 20), PD (n = 19), and PA+PD (n = 17) patients are represented. Normality was tested with the Kolmogorov-Smirnov test. Kruskal-Wallis test was used for data not distributed normally, and one-way ANOVA was used for normally distributed data. p < 0.05 values are shown on the graphs.
Figure 7.
Figure 7.
Alpha and beta diversity indices of the subgingival samples from HC, PD, and PA+PD groups. Panel A. observed species index, Shannon index, and Simpson’s diversity index illustrate differences between three groups based on OTU counts. Panel B. PCoA plots of bacterial beta-diversity depict the statistically significant difference in PD and P.A+PD groups compared to HC.
Figure 8.
Figure 8.
LEfSe analysis representing the similarities between HC, PD, and PA+PD samples. LDA scores of (log 10) > 2 and p < 0.05 are listed.
Figure 9.
Figure 9.
LEfSe analysis results of direct comparison between PD and PA+PD groups show differential abundances among the groups.
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