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Association between primary Sjögren’s syndrome and gut microbiota disruption: a systematic review and meta-analysis

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Abstract

Evidence of gut microbiota disruption for numerous autoimmune diseases has accumulated. Recently, the relationship between the microbiota and primary Sjögren’s disease has been increasingly investigated but has yet to be systematically elucidated. Therefore, a meta-analysis of publications dealing on topic was conducted. Case–control studies comparing primary Sjögren’s syndrome patients and healthy controls (HCs) were systematically searched in nine databases from inception to March 1, 2023. The primary result quantitatively evaluated in this meta-analysis was the α-diversity. The secondary results qualitatively extracted and analyzed were the β-diversity and relative abundance. In total, 22 case–control studies covering 915 pSS patients and 2103 HCs were examined. The quantitative analysis revealed a slight reduction in α-diversity in pSS patients compared to HCs, with a lower Shannon–Wiener index (SMD =  − 0.46, (− 0.68, − 0.25), p < 0.0001, I2 = 71%), Chao1 richness estimator (SMD =  − 0.59, (− 0.86, − 0.32), p < 0.0001, I2 = 81%), and ACE index (SMD =  − 0.92, (− 1.64, − 0.19), p = 0.01, I2 = 86%). However, the Simpson index (SMD = 0.01, (− 0.43, 0.46) p = 0.95, I2 = 86%) was similar in the two groups. The β-diversity significantly differed between pSS patients and HCs. Variations in the abundance of specific microbes and their metabolites and potential functions contribute to the pSS pathogenesis. Notably, the abundance of the phylum Firmicutes decreased, while that of Proteobacteria increased. SCFA-producing microbes including Ruminococcaceae, Lachnospiraceae, Faecalibacterium, Butyricicoccus, and Eubacterium hallii were depleted. In addition to diversity, the abundances of some specific microbes were related to clinical parameters. According to this systematic review and meta-analysis, gut microbiota dysbiosis, including reduced diversity, was associated with proinflammatory bacterium enrichment and anti-inflammatory bacterium depletion in pSS patients. Further research on the relationship between the gut microbiota and pSS is warranted.

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The original contributions presented in the study are included in the article/Supplementary Material. Further inquiries can be directed to the corresponding author.

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Acknowledgements

We would like to acknowledge all members who contributed to the study.

Funding

The work on this review was sponsored by the National Natural Science Foundation of China (82074341). The funder and the data provider had no role in the present study, including collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

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Authors and Affiliations

  1. The Second Clinical Medical College, Zhejiang Chinese Medical University, Hangzhou, China

    Yue Shen, Xue Yu, Xinyi Yao & Dingqi Lu

  2. School of Basic Medical Sciences, Key Laboratory of Chinese Medicine Rheumatology of Zhejiang Province, Zhejiang Chinese Medical University, Hangzhou, China

    Qiao Wang

  3. Department of Rheumatology, The Second Affiliated Hospital of Zhejiang Chinese Medical University, Hangzhou, China

    Donghai Zhou & Xinchang Wang

Authors
  1. Yue Shen
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  2. Xue Yu
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  3. Qiao Wang
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  4. Xinyi Yao
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  5. Dingqi Lu
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  6. Donghai Zhou
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  7. Xinchang Wang
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Contributions

All authors meet the International Committee of Medical Journal Editors (ICMJE) criteria for authorship of this article. SY and YX contributed to the conception or design of the work. WQ, LDQ, and YXY contributed to the analysis of the data for the work. SY and LDQ wrote the first draft of the manuscript. WQ and YX critically revised the manuscript for important intellectual content. All authors agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

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Correspondence to Donghai Zhou or Xinchang Wang.

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Shen, Y., Yu, X., Wang, Q. et al. Association between primary Sjögren’s syndrome and gut microbiota disruption: a systematic review and meta-analysis. Clin Rheumatol 43, 603–619 (2024). https://doi.org/10.1007/s10067-023-06754-x

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