Alterations in the human oral microbiota in systemic lupus erythematosus

Jinyan Guo; Guangying Cui; Wei Huang; Zhaohui Zheng; Tianfang Li; Guanmin Gao; Zhen Huang; Yuwei Zhan; Suying Ding; Shengyun Liu; Zujiang Yu; Zhigang Ren

doi:10.1186/s12967-023-03892-3

Alterations in the human oral microbiota in systemic lupus erythematosus

J Transl Med. 2023 Feb 8;21(1):95. doi: 10.1186/s12967-023-03892-3.

Authors

Jinyan Guo^#¹, Guangying Cui^#^{2

3}, Wei Huang^#⁴, Zhaohui Zheng¹, Tianfang Li¹, Guanmin Gao¹, Zhen Huang⁵, Yuwei Zhan⁴, Suying Ding⁶, Shengyun Liu⁷, Zujiang Yu^{8

9}, Zhigang Ren^{10

11

12}

Affiliations

¹ Department of Rheumatology and Immunology, The First Affiliated Hospital of Zhengzhou University, #1 Jianshe East Road, Zhengzhou, 450052, China.
² Department of Infectious Disease, The First Affiliated Hospital of Zhengzhou University, #1 Jianshe East Road, Zhengzhou, 450052, China.
³ Gene Hospital of Henan Province, Precision Medicine Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, 450052, China.
⁴ Department of Rheumatology and Immunology, Hainan General Hospital, Haikou, 570100, China.
⁵ Department of Cardiovascular Disease, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, 450052, China.
⁶ Health Management Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, 450052, China.
⁷ Department of Rheumatology and Immunology, The First Affiliated Hospital of Zhengzhou University, #1 Jianshe East Road, Zhengzhou, 450052, China. fccliusy@zzu.edu.cn.
⁸ Department of Infectious Disease, The First Affiliated Hospital of Zhengzhou University, #1 Jianshe East Road, Zhengzhou, 450052, China. johnyuem@zzu.edu.cn.
⁹ Gene Hospital of Henan Province, Precision Medicine Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, 450052, China. johnyuem@zzu.edu.cn.
¹⁰ Department of Infectious Disease, The First Affiliated Hospital of Zhengzhou University, #1 Jianshe East Road, Zhengzhou, 450052, China. fccrenzg@zzu.edu.cn.
¹¹ Gene Hospital of Henan Province, Precision Medicine Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, 450052, China. fccrenzg@zzu.edu.cn.
¹² Jinan Microecological Biomedicine Shandong Laboratory, Jinan, 250000, China. fccrenzg@zzu.edu.cn.

^# Contributed equally.

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.

Keywords: Characteristics; Diagnostic biomarker; Disease activity; Oral microbiota; Systemic lupus erythematosus.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Humans
Lupus Erythematosus, Systemic*
Microbiota*