Gut microbiota dysbiosis and associated immune response in systemic lupus erythematosus: impact of disease and treatment.

IF 4.3 3区医学 Q1 GASTROENTEROLOGY & HEPATOLOGY

Gut Pathogens Pub Date : 2025-02-18 DOI:10.1186/s13099-025-00683-7

Aya Y Ali, Sara A Zahran, Mervat Eissa, Mona T Kashef, Amal Emad Ali

{"title":"Gut microbiota dysbiosis and associated immune response in systemic lupus erythematosus: impact of disease and treatment.","authors":"Aya Y Ali, Sara A Zahran, Mervat Eissa, Mona T Kashef, Amal Emad Ali","doi":"10.1186/s13099-025-00683-7","DOIUrl":null,"url":null,"abstract":"Background: Gut microbial dysbiosis and leaky gut play a role in systemic lupus erythematosus (SLE). Geographical location and dietary habits affect the microbiome composition in diverse populations. This study explored the gut microbiome dysbiosis, leaky gut, and systemic immune response to gut bacterial consortium in patients with SLE exhibiting mild/moderate and severe disease activity.Methods: Fecal and blood samples were collected from patients with SLE and healthy volunteers. Genomic DNA was extracted from the stool samples and subjected to 16S rRNA amplicon sequencing and microbiome profiling. Additionally, enzyme-linked immunosorbent assays were employed to determine the serum lipopolysaccharide level, as an assessment of gut permeability, and the systemic immune response against gut bacteria.Results: Patients with SLE showed significantly lower gut bacterial richness and diversity, indicated by observed OTUs (56.6 vs. 74.44; p = 0.0289), Shannon (3.05 vs. 3.45; p = 0.017) and Simpson indices (0.91 vs. 0.94; p = 0.033). A lower Firmicutes-to-Bacteroidetes ratio (1.07 vs. 1.69; p = 0.01) was observed, with reduced genera such as Ruminococcus 2 (0.003 vs. 0.026; p = 0.0009) and Agathobacter (0.003 vs. 0.012; p < 0.0001) and elevated Escherichia-Shigella (0.04 vs. 0.006; p < 0.0001) and Bacteroides (0.206 vs. 0.094; p = 0.033). Disease severity was associated with a higher relative abundance of Prevotella (0.001 vs. 0.0001; p = 0.04). Medication effects included lower Romboutsia (0.0009 vs. 0.011; p = 0.005) with azathioprine and higher Prevotella (0.003 vs. 0.0002; p = 0.038) with cyclophosphamide. Furthermore, categorization by prednisolone dosage revealed significantly higher relative abundances of Slackia (0.0007 vs. 0.00002; p = 0.0088), Romboutsia (0.009 vs. 0.002; p = 0.0366), and Comamonas (0.002 vs. 0.00007; p = 0.0249) in patients receiving high-dose prednisolone (> 10 mg/day). No differences in serum lipopolysaccharide levels were found, but SLE patients exhibited elevated serum gut bacterial antibody levels, suggesting a systemic immune response.Conclusion: This study confirms the gut microbiome dysbiosis in patients with SLE, influenced by disease severity and specific medication usage.","PeriodicalId":12833,"journal":{"name":"Gut Pathogens","volume":"17 1","pages":"10"},"PeriodicalIF":4.3000,"publicationDate":"2025-02-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11834511/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Gut Pathogens","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1186/s13099-025-00683-7","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"GASTROENTEROLOGY & HEPATOLOGY","Score":null,"Total":0}

引用次数: 0

Abstract

Background: Gut microbial dysbiosis and leaky gut play a role in systemic lupus erythematosus (SLE). Geographical location and dietary habits affect the microbiome composition in diverse populations. This study explored the gut microbiome dysbiosis, leaky gut, and systemic immune response to gut bacterial consortium in patients with SLE exhibiting mild/moderate and severe disease activity.

Methods: Fecal and blood samples were collected from patients with SLE and healthy volunteers. Genomic DNA was extracted from the stool samples and subjected to 16S rRNA amplicon sequencing and microbiome profiling. Additionally, enzyme-linked immunosorbent assays were employed to determine the serum lipopolysaccharide level, as an assessment of gut permeability, and the systemic immune response against gut bacteria.

Results: Patients with SLE showed significantly lower gut bacterial richness and diversity, indicated by observed OTUs (56.6 vs. 74.44; p = 0.0289), Shannon (3.05 vs. 3.45; p = 0.017) and Simpson indices (0.91 vs. 0.94; p = 0.033). A lower Firmicutes-to-Bacteroidetes ratio (1.07 vs. 1.69; p = 0.01) was observed, with reduced genera such as Ruminococcus 2 (0.003 vs. 0.026; p = 0.0009) and Agathobacter (0.003 vs. 0.012; p < 0.0001) and elevated Escherichia-Shigella (0.04 vs. 0.006; p < 0.0001) and Bacteroides (0.206 vs. 0.094; p = 0.033). Disease severity was associated with a higher relative abundance of Prevotella (0.001 vs. 0.0001; p = 0.04). Medication effects included lower Romboutsia (0.0009 vs. 0.011; p = 0.005) with azathioprine and higher Prevotella (0.003 vs. 0.0002; p = 0.038) with cyclophosphamide. Furthermore, categorization by prednisolone dosage revealed significantly higher relative abundances of Slackia (0.0007 vs. 0.00002; p = 0.0088), Romboutsia (0.009 vs. 0.002; p = 0.0366), and Comamonas (0.002 vs. 0.00007; p = 0.0249) in patients receiving high-dose prednisolone (> 10 mg/day). No differences in serum lipopolysaccharide levels were found, but SLE patients exhibited elevated serum gut bacterial antibody levels, suggesting a systemic immune response.

Conclusion: This study confirms the gut microbiome dysbiosis in patients with SLE, influenced by disease severity and specific medication usage.

查看原文本刊更多论文

系统性红斑狼疮的肠道菌群失调和相关免疫反应：疾病和治疗的影响。

背景：肠道微生物失调和肠漏在系统性红斑狼疮（SLE）中起作用。地理位置和饮食习惯影响不同人群的微生物组组成。本研究探讨了轻度/中度和重度疾病活动性SLE患者肠道菌群失调、肠漏和对肠道菌群的全身免疫反应。方法：采集SLE患者和健康志愿者的粪便和血液样本。从粪便样本中提取基因组DNA，进行16S rRNA扩增子测序和微生物组分析。此外，采用酶联免疫吸附法测定血清脂多糖水平，以评估肠道通透性和对肠道细菌的全身免疫反应。结果：SLE患者肠道细菌丰富度和多样性明显降低，观察到的OTUs (56.6 vs 74.44；p = 0.0289), Shannon (3.05 vs. 3.45；p = 0.017)和Simpson指数(0.91 vs. 0.94；p = 0.033)。较低的厚壁菌与拟杆菌的比值(1.07比1.69；p = 0.01)，减少属如瘤胃球菌2 (0.003 vs. 0.026；p = 0.0009)和Agathobacter (0.003 vs. 0.012；p 10毫克/天)。血清脂多糖水平未见差异，但SLE患者血清肠道细菌抗体水平升高，提示系统性免疫反应。结论：本研究证实SLE患者的肠道微生物群失调受疾病严重程度和特定药物使用的影响。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

求助全文

约1分钟内获得全文求助全文

来源期刊

Gut Pathogens GASTROENTEROLOGY & HEPATOLOGY-MICROBIOLOGY

CiteScore

7.70

自引率

2.40%

发文量

期刊介绍： Gut Pathogens is a fast publishing, inclusive and prominent international journal which recognizes the need for a publishing platform uniquely tailored to reflect the full breadth of research in the biology and medicine of pathogens, commensals and functional microbiota of the gut. The journal publishes basic, clinical and cutting-edge research on all aspects of the above mentioned organisms including probiotic bacteria and yeasts and their products. The scope also covers the related ecology, molecular genetics, physiology and epidemiology of these microbes. The journal actively invites timely reports on the novel aspects of genomics, metagenomics, microbiota profiling and systems biology. Gut Pathogens will also consider, at the discretion of the editors, descriptive studies identifying a new genome sequence of a gut microbe or a series of related microbes (such as those obtained from new hosts, niches, settings, outbreaks and epidemics) and those obtained from single or multiple hosts at one or different time points (chronological evolution).