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, 5 (1), 34

Subgingival Microbiota Dysbiosis in Systemic Lupus Erythematosus: Association With Periodontal Status

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Subgingival Microbiota Dysbiosis in Systemic Lupus Erythematosus: Association With Periodontal Status

Jôice Dias Corrêa et al. Microbiome.

Abstract

Background: Periodontitis results from the interaction between a subgingival biofilm and host immune response. Changes in biofilm composition are thought to disrupt homeostasis between the host and subgingival bacteria resulting in periodontal damage. Chronic systemic inflammatory disorders have been shown to affect the subgingival microbiota and clinical periodontal status. However, this relationship has not been examined in subjects with systemic lupus erythematosus (SLE). The objective of our study was to investigate the influence of SLE on the subgingival microbiota and its connection with periodontal disease and SLE activity.

Methods: We evaluated 52 patients with SLE compared to 52 subjects without SLE (control group). Subjects were classified as without periodontitis and with periodontitis. Oral microbiota composition was assessed by amplifying the V4 region of 16S rRNA gene from subgingival dental plaque DNA extracts. These amplicons were examined by Illumina MiSeq sequencing.

Results: SLE patients exhibited higher prevalence of periodontitis which occurred at a younger age compared to subjects of the control group. More severe forms of periodontitis were found in SLE subjects that had higher bacterial loads and decreased microbial diversity. Bacterial species frequently detected in periodontal disease were observed in higher proportions in SLE patients, even in periodontal healthy sites such as Fretibacterium, Prevotella nigrescens, and Selenomonas. Changes in the oral microbiota were linked to increased local inflammation, as demonstrated by higher concentrations of IL-6, IL-17, and IL-33 in SLE patients with periodontitis.

Conclusions: SLE is associated with differences in the composition of the microbiota, independently of periodontal status.

Keywords: Cytokine; Illumina sequencing; Lupus; Oral microbiota; Periodontitis; Subgingival dental plaque.

Figures

Fig. 1
Fig. 1
Subgingival bacterial load of healthy subjects (control) and patients with Systemic Lupus Erythematosus (SLE) with chronic periodontitis (CP) and Non-CP (NCP), determined by real-time PCR using universal primers for 16S rRNA gene. *Statistically different compared to NCP subjects within the same group. #Statistically different compared to control subjects. p < 0.05, Kruskal-Wallis test with Dunn’s post hoc test
Fig. 2
Fig. 2
Alpha diversity index, a observed species and b Chao1 index of control subjects or Systemic Lupus Erythematosus patients (SLE) with chronic periodontitis (CP) or Non-CP (NCP). *Statistically different compared to NCP subjects within the same group. #Statistically different compared to Control group. p < 0.05, Kruskal-Wallis test with Dunn’s post hoc test. Alpha diversity metrics were calculated after subsampling to obtain equal number of sequences per library
Fig. 3
Fig. 3
Beta diversity. Microbiota separation on the principal coordinates calculated from unweighted UniFrac distances. a Control subjects, b SLE patients, c non-periodontitis subjects, and d chronic periodontitis subjects
Fig. 4
Fig. 4
The average weighted UniFrac distance values (the beta diversities) of healthy subjects (control) and patients with Systemic Lupus Erythematosus (SLE) with chronic periodontitis (CP) and Non-CP (NCP).*Statistically different compared to NCP subjects within the same group. #Statistically different compared to control group. p < 0.05, Kruskal-Wallis test with Dunn’s post hoc test
Fig. 5
Fig. 5
OTUs and taxa differing between non-periodontitis (upper panel) and periodontitis (lower anel) sites. a, c Heat map with the OTUs showing a p value of less than 0.05 when comparing relative abundances between control and SLE subjects. Subjects are shown in columns, while OTUs appear in rows. Blue asterisks indicate OTUs with decreased proportions in SLE patients, while red asterisks indicated OTUs with increased proportions in SLE in relation to respective controls. b, d The graphic representation of differences in the relative abundances of species represented in the heat maps
Fig. 6
Fig. 6
OTUs with different relative abundance in control subjects (red) and SLE samples (green) in non-periodontitis (a) and chronic periodontitis subjects (b). Graph depicts OTUs with different relative abundance based on LEfSe results. Bars represent linear discriminant analysis scores (LDA)
Fig. 7
Fig. 7
Correlations among bacteria species in control (a) and SLE subjects (b) with chronic periodontitis (CP) (green) and Non-CP (NCP) (yellow). In white area are the bacteria that are common to subjects with CP and NCP. Spearman Rank test with a cutoff rho value of 0.4 and p < 0.05. Blue lines indicate positive correlations and red lines negative correlations
Fig. 8
Fig. 8
Concentration of IL-6 (a), IL-17 (b), and IL-33 (c) in saliva of healthy subjects (control) and patients with Systemic Lupus Erythematosus (SLE) with chronic periodontitis (CP) and Non-CP (NCP). Cytokine measurement was determined by CBA and ELISA, and values were normalized by stimulated salivary flux.*Statistically different compared to NCP subjects within the same group. #Statistically different compared to healthy subjects with CP. p < 0.05, Kruskal-Wallis test with Dunn’s post hoc test

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