Subgingival microbiota dysbiosis in systemic lupus erythematosus: association with periodontal status

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Reviewed Marked as Reviewed by Svetlana up on 2025-2-24
study design
Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
URI
Authors
Corrêa JD, Calderaro DC, Ferreira GA, Mendonça SM, Fernandes GR, Xiao E, Teixeira AL, Leys EJ, Graves DT, Silva TA
Journal
Microbiome
Year
2017
Keywords:
Cytokine, Illumina sequencing, Lupus, Oral microbiota, Periodontitis, Subgingival dental plaque
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.

Experiment 1


Reviewed Marked as Reviewed by Svetlana up on 2025-2-24

Curated date: 2025/02/14

Curator: Taofeecoh

Revision editor(s): Taofeecoh, WikiWorks

Subjects

Location of subjects
Brazil
Host species Species from which microbiome was sampled. Contact us to have more species added.
Homo sapiens
Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
Subgingival dental plaque Subgingival plaque,Subgingival dental plaque,subgingival dental plaque
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Systemic lupus erythematosus Disease, Libman-Sacks,disseminated lupus erythematosus,excess LMW-DNA,excess lymphocyte low molecular weight DNA,LIBMAN SACKS DIS,Libman Sacks Disease,Libman-Sacks Disease,lupus,Lupus Erythematosus Disseminatus,Lupus Erythematosus, Systemic,lupus erythematosus, systemic,SLE,SLE - lupus erythematosus, systemic,systemic lupus erythematosus,systemic lupus erythematosus (disease),Systemic lupus erythematosus
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Control with Non-periodontitis (C-NCP)
Group 1 name Corresponds to the case (exposed) group for case-control studies
Systemic Lupus Erythematosus with Non-periodontitis (SLE-NCP)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Systemic Lupus Erythematosus (SLE) patients with Non-periodontitis (NCP)
Group 0 sample size Number of subjects in the control (unexposed) group
24
Group 1 sample size Number of subjects in the case (exposed) group
17
Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)
3 months

Lab analysis

Sequencing type
16S
16S variable region One or more hypervariable region(s) of the bacterial 16S gene
V4
Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance
Illumina

Statistical Analysis

Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).
raw counts
Statistical test
DESeq2
Significance threshold p-value or FDR threshold used for differential abundance testing (if any)
0.05
MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?
Yes
Matched on Factors on which subjects have been matched on in a case-control study
age, sex

Alpha Diversity

Chao1 Abundance-based estimator of species richness
increased
Richness Number of species
increased

Signature 1

Reviewed Marked as Reviewed by Svetlana up on 2025-2-24

Curated date: 2025/02/15

Curator: Taofeecoh

Revision editor(s): Taofeecoh, WikiWorks

Source: Figures 5a, 5b

Description: OTUs with different relative abundance in control subjects and SLE patients in non-periodontitis.

Abundance in Group 1: increased abundance in Systemic Lupus Erythematosus with Non-periodontitis (SLE-NCP)

NCBI Quality ControlLinks
unclassified Lachnospiraceae A IR009unclassified Lachnospiraceae A IR009

Revision editor(s): Taofeecoh, WikiWorks

Signature 2

Reviewed Marked as Reviewed by Svetlana up on 2025-2-24

Curated date: 2025/02/15

Curator: Taofeecoh

Revision editor(s): Taofeecoh, WikiWorks

Source: Figures 5a, 5b

Description: OTUs with different relative abundance in control subjects and SLE samples in non-periodontitis.

Abundance in Group 1: decreased abundance in Systemic Lupus Erythematosus with Non-periodontitis (SLE-NCP)

NCBI Quality ControlLinks
Mogibacterium
Sphingomonas

Revision editor(s): Taofeecoh, WikiWorks

Experiment 2


Reviewed Marked as Reviewed by Svetlana up on 2025-2-24

Curated date: 2025/02/15

Curator: Taofeecoh

Revision editor(s): Taofeecoh, WikiWorks

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Controls with Chronic periodontitis (C-CP)
Group 1 name Corresponds to the case (exposed) group for case-control studies
Systemic Lupus Erythematosus with Chronic periodontitis (SLE-CP)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Systemic Lupus Erythematosus (SLE) patients with Chronic periodontitis (CP)
Group 0 sample size Number of subjects in the control (unexposed) group
28
Group 1 sample size Number of subjects in the case (exposed) group
35

Lab analysis

Statistical Analysis

Alpha Diversity

Chao1 Abundance-based estimator of species richness
unchanged
Richness Number of species
unchanged

Signature 1

Reviewed Marked as Reviewed by Svetlana up on 2025-2-24

Curated date: 2025/02/15

Curator: Taofeecoh

Revision editor(s): Taofeecoh, WikiWorks

Source: Figures 5c, 5d

Description: OTUs with different relative abundance in control subjects and SLE samples in Chronic periodontitis.

Abundance in Group 1: increased abundance in Systemic Lupus Erythematosus with Chronic periodontitis (SLE-CP)

NCBI Quality ControlLinks
Hoylesella pleuritidis
Pseudomonas
Segatella oulorum
Treponema maltophilum
Actinomyces IP073Actinomyces IP073
Bifidobacterium/ScardoviaBifidobacterium/Scardovia
Mogibacterium neglectum/vescumMogibacterium neglectum/vescum
Fretibacterium fastidiosum

Revision editor(s): Taofeecoh, WikiWorks

Signature 2

Reviewed Marked as Reviewed by Svetlana up on 2025-2-24

Curated date: 2025/02/15

Curator: Taofeecoh

Revision editor(s): Taofeecoh, WikiWorks

Source: Figures 5c, 5d

Description: OTUs with different relative abundance in control subjects and SLE samples in Chronic periodontitis.

Abundance in Group 1: decreased abundance in Systemic Lupus Erythematosus with Chronic periodontitis (SLE-CP)

NCBI Quality ControlLinks
Capnocytophaga gingivalis
Comamonadaceae
Eubacteriales
Granulicatella adiacens
Haemophilus parainfluenzae
Prevotella fusca
Roseateles puraquae
Sphingomonas
Streptococcus sanguinis
Ralstonia oral taxon 027Ralstonia oral taxon 027
Leptotrichia oral taxon A71Leptotrichia oral taxon A71
Rothia aeria

Revision editor(s): Taofeecoh, WikiWorks

Experiment 3


Reviewed Marked as Reviewed by Svetlana up on 2025-2-24

Curated date: 2025/02/20

Curator: Taofeecoh

Revision editor(s): Taofeecoh

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Control with Non-periodontitis (C-NCP)
Group 1 name Corresponds to the case (exposed) group for case-control studies
Systemic Lupus Erythematosus with Non-periodontitis (SLE-NCP)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Systemic Lupus Erythematosus (SLE) patients with Non-periodontitis (NCP)
Group 0 sample size Number of subjects in the control (unexposed) group
24
Group 1 sample size Number of subjects in the case (exposed) group
17

Lab analysis

Statistical Analysis

Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).
relative abundances
Statistical test
LEfSe
MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?
No
LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
2

Alpha Diversity

Chao1 Abundance-based estimator of species richness
increased
Richness Number of species
increased

Signature 1

Reviewed Marked as Reviewed by Svetlana up on 2025-2-24

Curated date: 2025/02/20

Curator: Taofeecoh

Revision editor(s): Taofeecoh

Source: Figure 6a

Description: OTUs with different relative abundance in control subjects and SLE patients in non-periodontitis.

Abundance in Group 1: increased abundance in Systemic Lupus Erythematosus with Non-periodontitis (SLE-NCP)

NCBI Quality ControlLinks
Aggregatibacter
Cryptobacterium curtum
Hallella multisaccharivorax
Leptotrichia
Oribacterium sinus
Prevotella nigrescens
Segatella oris
Segatella oulorum
Selenomonas noxia
Treponema amylovorum
Streptococcus intermedius/constellatusStreptococcus intermedius/constellatus
Capnocytophaga leadbetteri

Revision editor(s): Taofeecoh

Signature 2

Reviewed Marked as Reviewed by Svetlana up on 2025-2-24

Curated date: 2025/02/20

Curator: Taofeecoh

Revision editor(s): Taofeecoh

Source: Figure 6a

Description: OTUs with different relative abundance in control subjects and SLE samples in non-periodontitis.

Abundance in Group 1: decreased abundance in Systemic Lupus Erythematosus with Non-periodontitis (SLE-NCP)

NCBI Quality ControlLinks
Aggregatibacter aphrophilus
Comamonadaceae
Streptococcus anginosus
Treponema E D 05 72Treponema E D 05 72
unclassified Burkholderiales
Sphingomonas

Revision editor(s): Taofeecoh

Experiment 4


Reviewed Marked as Reviewed by Svetlana up on 2025-2-24

Curated date: 2025/02/20

Curator: Taofeecoh

Revision editor(s): Taofeecoh

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Control with Chronic periodontitis (C-CP)
Group 1 name Corresponds to the case (exposed) group for case-control studies
Systemic Lupus Erythematosus Chronic periodontitis (SLE-CP)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Systemic Lupus Erythematosus (SLE) patients with Chronic periodontitis (CP)
Group 0 sample size Number of subjects in the control (unexposed) group
28
Group 1 sample size Number of subjects in the case (exposed) group
35

Lab analysis

Statistical Analysis

Alpha Diversity

Chao1 Abundance-based estimator of species richness
unchanged
Richness Number of species
unchanged

Signature 1

Reviewed Marked as Reviewed by Svetlana up on 2025-2-24

Curated date: 2025/02/20

Curator: Taofeecoh

Revision editor(s): Taofeecoh

Source: Figure 6b

Description: OTUs with different relative abundance in control subjects and SLE samples in Chronic periodontitis.

Abundance in Group 1: increased abundance in Systemic Lupus Erythematosus Chronic periodontitis (SLE-CP)

NCBI Quality ControlLinks
Segatella oulorum
Fretibacterium oral taxon 360 453Fretibacterium oral taxon 360 453
TM7 oral taxon 437TM7 oral taxon 437
Hallella multisaccharivorax
Fretibacterium fastidiosum
Sphingomonas
Anaeroglobus geminatus

Revision editor(s): Taofeecoh

Signature 2

Reviewed Marked as Reviewed by Svetlana up on 2025-2-24

Curated date: 2025/02/20

Curator: Taofeecoh

Revision editor(s): Taofeecoh

Source: Figure 6b

Description: OTUs with different relative abundance in control subjects and SLE samples in Chronic periodontitis.

Abundance in Group 1: decreased abundance in Systemic Lupus Erythematosus Chronic periodontitis (SLE-CP)

NCBI Quality ControlLinks
Prevotella intermedia
Rothia aeria
Bergeyella 602D02Bergeyella 602D02
Brevundimonas nbw914f05c1Brevundimonas nbw914f05c1
Peptococcus BU014Peptococcus BU014

Revision editor(s): Taofeecoh