Alterations in the human oral microbiota in systemic lupus erythematosus

Abstract Background Alterations in oral microbiota in patients with systemic lupus erythematosus (SLE) is less evaluated. The aim of this study was to compare the characteristics of the oral microbiome in SLE patients and healthy controls, and construct an SLE classifier based on the oral microbiota...

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Main Authors: Jinyan Guo, Guangying Cui, Wei Huang, Zhaohui Zheng, Tianfang Li, Guanmin Gao, Zhen Huang, Yuwei Zhan, Suying Ding, Shengyun Liu, Zujiang Yu, Zhigang Ren
Format: Article
Language:English
Published: BMC 2023-02-01
Series:Journal of Translational Medicine
Subjects:
Online Access:https://doi.org/10.1186/s12967-023-03892-3
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author Jinyan Guo
Guangying Cui
Wei Huang
Zhaohui Zheng
Tianfang Li
Guanmin Gao
Zhen Huang
Yuwei Zhan
Suying Ding
Shengyun Liu
Zujiang Yu
Zhigang Ren
author_facet Jinyan Guo
Guangying Cui
Wei Huang
Zhaohui Zheng
Tianfang Li
Guanmin Gao
Zhen Huang
Yuwei Zhan
Suying Ding
Shengyun Liu
Zujiang Yu
Zhigang Ren
author_sort Jinyan Guo
collection DOAJ
description Abstract Background Alterations in oral microbiota in patients with systemic lupus erythematosus (SLE) is less evaluated. The aim of this study was to compare the characteristics of the oral microbiome in SLE patients and healthy controls, and construct an SLE classifier based on the oral microbiota. Methods We sequenced tongue-coating samples of individuals in treatment-naïve SLE (n = 182) and matched healthy controls (n = 280). We characterized the oral microbiome and constructed a microbial classifier in the derivation cohort and validated the results in the validation cohorts. Furthermore, the oral microbiome of posttreatment SLE (n = 73) was characterized. Results The oral microbial diversity of SLE was increased, and the microbial community was different between SLE and healthy controls. The genera Prevotella and Veillonella were enriched, while Streptococcus and Porphyromonas were reduced in SLE. In addition, an increase was noted in 27 predicted microbial functions, while a decrease was noted in 34 other functions. Thirty-nine operational taxonomy units (OTUs) were identified to be related with seven clinical indicators. Two OTUs were identified to construct a classifier, which yielded area under the curve values of 0.9166 (95% CI 0.8848–0.9483, p < 0.0001), 0.8422 (95% CI 0.7687–0.9157, p < 0.0001), and 0.8406 (95% CI 0.7677–0.9135, p < 0.0001) in the derivation, validation, and cross-regional validation groups, respectively. Moreover, as disease activity increased, Abiotrophia and Lactobacillales increased, while Phyllobacterium and unclassified Micrococcusaceae decreased. Finally, nine OTUs were selected to construct a classifier distinguishing posttreatment SLE patients from healthy controls, which achieved a diagnostic efficacy of 0.9942 (95% CI 0.9884–1, p < 0.0001). Conclusions Our study comprehensively characterizes the oral microbiome of SLE and shows the potential of the oral microbiota as a non-invasive diagnostic biomarker in SLE.
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spelling doaj.art-1b2e2df8d3844b61a9880068a6e959512023-02-12T12:20:56ZengBMCJournal of Translational Medicine1479-58762023-02-0121111310.1186/s12967-023-03892-3Alterations in the human oral microbiota in systemic lupus erythematosusJinyan Guo0Guangying Cui1Wei Huang2Zhaohui Zheng3Tianfang Li4Guanmin Gao5Zhen Huang6Yuwei Zhan7Suying Ding8Shengyun Liu9Zujiang Yu10Zhigang Ren11Department of Rheumatology and Immunology, The First Affiliated Hospital of Zhengzhou UniversityDepartment of Infectious Disease, The First Affiliated Hospital of Zhengzhou UniversityDepartment of Rheumatology and Immunology, Hainan General HospitalDepartment of Rheumatology and Immunology, The First Affiliated Hospital of Zhengzhou UniversityDepartment of Rheumatology and Immunology, The First Affiliated Hospital of Zhengzhou UniversityDepartment of Rheumatology and Immunology, The First Affiliated Hospital of Zhengzhou UniversityDepartment of Cardiovascular Disease, The First Affiliated Hospital of Zhengzhou UniversityDepartment of Rheumatology and Immunology, Hainan General HospitalHealth Management Center, The First Affiliated Hospital of Zhengzhou UniversityDepartment of Rheumatology and Immunology, The First Affiliated Hospital of Zhengzhou UniversityDepartment of Infectious Disease, The First Affiliated Hospital of Zhengzhou UniversityDepartment of Infectious Disease, The First Affiliated Hospital of Zhengzhou UniversityAbstract Background Alterations in oral microbiota in patients with systemic lupus erythematosus (SLE) is less evaluated. The aim of this study was to compare the characteristics of the oral microbiome in SLE patients and healthy controls, and construct an SLE classifier based on the oral microbiota. Methods We sequenced tongue-coating samples of individuals in treatment-naïve SLE (n = 182) and matched healthy controls (n = 280). We characterized the oral microbiome and constructed a microbial classifier in the derivation cohort and validated the results in the validation cohorts. Furthermore, the oral microbiome of posttreatment SLE (n = 73) was characterized. Results The oral microbial diversity of SLE was increased, and the microbial community was different between SLE and healthy controls. The genera Prevotella and Veillonella were enriched, while Streptococcus and Porphyromonas were reduced in SLE. In addition, an increase was noted in 27 predicted microbial functions, while a decrease was noted in 34 other functions. Thirty-nine operational taxonomy units (OTUs) were identified to be related with seven clinical indicators. Two OTUs were identified to construct a classifier, which yielded area under the curve values of 0.9166 (95% CI 0.8848–0.9483, p < 0.0001), 0.8422 (95% CI 0.7687–0.9157, p < 0.0001), and 0.8406 (95% CI 0.7677–0.9135, p < 0.0001) in the derivation, validation, and cross-regional validation groups, respectively. Moreover, as disease activity increased, Abiotrophia and Lactobacillales increased, while Phyllobacterium and unclassified Micrococcusaceae decreased. Finally, nine OTUs were selected to construct a classifier distinguishing posttreatment SLE patients from healthy controls, which achieved a diagnostic efficacy of 0.9942 (95% CI 0.9884–1, p < 0.0001). Conclusions Our study comprehensively characterizes the oral microbiome of SLE and shows the potential of the oral microbiota as a non-invasive diagnostic biomarker in SLE.https://doi.org/10.1186/s12967-023-03892-3Systemic lupus erythematosusOral microbiotaCharacteristicsDiagnostic biomarkerDisease activity
spellingShingle Jinyan Guo
Guangying Cui
Wei Huang
Zhaohui Zheng
Tianfang Li
Guanmin Gao
Zhen Huang
Yuwei Zhan
Suying Ding
Shengyun Liu
Zujiang Yu
Zhigang Ren
Alterations in the human oral microbiota in systemic lupus erythematosus
Journal of Translational Medicine
Systemic lupus erythematosus
Oral microbiota
Characteristics
Diagnostic biomarker
Disease activity
title Alterations in the human oral microbiota in systemic lupus erythematosus
title_full Alterations in the human oral microbiota in systemic lupus erythematosus
title_fullStr Alterations in the human oral microbiota in systemic lupus erythematosus
title_full_unstemmed Alterations in the human oral microbiota in systemic lupus erythematosus
title_short Alterations in the human oral microbiota in systemic lupus erythematosus
title_sort alterations in the human oral microbiota in systemic lupus erythematosus
topic Systemic lupus erythematosus
Oral microbiota
Characteristics
Diagnostic biomarker
Disease activity
url https://doi.org/10.1186/s12967-023-03892-3
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