Causal relationship between gut microbiota and idiopathic pulmonary fibrosis: A bi-directional two-sample Mendelian randomization study_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

WU Xuanyu ¹ , XIAO Xiang ¹ , CHEN Jiajing ¹ , YU Xiaomin ² ,  YANG Han ³

1. Clinical Medical College/Hospital of Chengdu University of Traditional Chinese Medicine, Chengdu University of Traditional Chinese Medicine, Chengdu, 610072, P. R. China;
2. Classical Chinese Medicine Ward, Hospital of Chengdu University of Traditional Chinese Medicine, Chengdu, 610072, P. R. China;
3. Department of Geriatrics, Hospital of Chengdu University of Traditional Chinese Medicine, Chengdu, 610072, P. R.China;

Corresponding?author：

YANG Han, Email: 15882458490@163.com

Keywords：

Gut microbiota; idiopathic pulmonary fibrosis; causal association; Mendelian randomization; inverse variance weighted; genome-wide association studies; single nucleotide polymorphisms

DOI：

10.7507/1007-4848.202403050

Video：

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Objective To investigate the causal relationship between gut microbiota and idiopathic pulmonary fibrosis (IPF). Methods Genome-wide association studies (GWAS) data of gut microbiota and IPF were obtained from MiBioGen and IEU OpenGWAS, respectively. Instrumental variables were screened by means of significance, linkage disequilibrium, weak instrumental variable screening, and removal of confounding factors (genetics, smoking, host characteristics). Inverse variance weighted (IVW) was used as the main Mendelian randomization (MR) analysis method, and the weighted median, simple mode, MR-Egger, and weighted mode were used to perform MR to reveal the causal effect of gut microbiota and IPF. The Cochrane's Q, leave-one-out, MR-Egger-intercept, and Mendelian randomization pleiotropy residual sum and outlier (MR-PRESSO) and Steiger tests were used to analyze the heterogeneity, horizontal pleiotropy, outliers, and directionality, respectively. Results IVW analysis results showed that Actinobacteria [OR=1.773, 95%CI (1.323, 2.377), P<0.001], Erysipelatoclostridium [OR=2.077, 95%CI (1.107, 3.896), P=0.023], and Streptococcus [OR=1.35, 95%CI (1.100, 1.657), P=0.004] could increase the risk of IPF. Bifidobacterium [OR=0.668, 95%CI (0.620, 0.720), P<0.001], Ruminococcus [OR=0.434, 95%CI (0.222, 0.848), P=0.015], and Tyzzerella [OR=0.479, 95%CI (0.304, 0.755), P=0.001] could reduce the risk of IPF. No significant heterogeneity, horizontal pleiotropy, outliers, and reverse causality were found. Conclusion Actinobacteria, Erysipelatoclostridium and Streptococcus may increase the risk of IPF, while Bifidobacterium, Ruminococcus and Tyzzerella may reduce the risk of IPF. Regulation of the above gut microbiota may become a new direction in the study of the pathogenesis of IPF.

Citation： WU Xuanyu, XIAO Xiang, CHEN Jiajing, YU Xiaomin, YANG Han. Causal relationship between gut microbiota and idiopathic pulmonary fibrosis: A bi-directional two-sample Mendelian randomization study. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2026, 33(4): 584-591. doi: 10.7507/1007-4848.202403050 Copy

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6.	Sack C, Raghu G. Idiopathic pulmonary fibrosis: unmasking cryptogenic environmental factors. Eur Respir J, 2019, 53(2): 1801699.
7.	Yang L, Sakandar HA, Sun Z, et al. Recent advances of intestinal microbiota transmission from mother to infant. J Funct Foods. 2021, 87: 104719.
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9.	武文娟, 吳紀珍, 黃改榮, 等. 老年腸道菌群失調與特發性肺纖維化患者心力衰竭的相關性研究. 中華老年心腦血管病雜志. 2022, 24 (1): 14-16.Wu WJ, Wu JZ, Huang GR, et al. Correlation between intestinal flora imbalance and HF in elderly idiopathic pulmonary fibrosis patients. Chin J Geriatr Heart Brain Vessel Dis, 2022, 24(1): 14-16.
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1. Spagnolo P, Kropski JA, Jones MG, et al. Idiopathic pulmonary fibrosis: disease mechanisms and drug development. Pharmacol Ther, 2021, 222: 107798.
2. Cottin V, Hirani NA, Hotchkin DL, et al. Presentation, diagnosis and clinical course of the spectrum of progressive-fibrosing interstitial lung diseases. Eur Respir Rev, 2018, 27(150): 180076.
3. Sgalla G, Kulkarni T, Antin-Ozerkis D, et al. Update in pulmonary fibrosis 2018. Am J Respir Crit Care Med, 2019, 200(3): 292-300.
4. Vaz M, Hwang SY, Kagiampakis I, et al. Chronic cigarette smoke-induced epigenomic changes precede sensitization of bronchial epithelial cells to single-step transformation by KRAS mutations. Cancer Cell, 2017, 32(3): 360-376.
5. Moore BB, Moore TA. Viruses in idiopathic pulmonary fibrosis. Etiology and exacerbation. Ann Am Thorac Soc, 2015, 12 Suppl 2(Suppl 2): S186-S192.
6. Sack C, Raghu G. Idiopathic pulmonary fibrosis: unmasking cryptogenic environmental factors. Eur Respir J, 2019, 53(2): 1801699.
7. Yang L, Sakandar HA, Sun Z, et al. Recent advances of intestinal microbiota transmission from mother to infant. J Funct Foods. 2021, 87: 104719.
8. 師曉棟, 趙晗, 劉東山. 腸道菌群在肺纖維化疾病中的調節作用. 生物化學與生物物理進展, 2023, 50(2): 252-264.Shi XD, Zhao H, Liu DS. Regulation of intestinal microbiota in pulmonary fibrosis diseases. Prog Biochem Biophys, 2023, 50(2): 252-264.
9. 武文娟, 吳紀珍, 黃改榮, 等. 老年腸道菌群失調與特發性肺纖維化患者心力衰竭的相關性研究. 中華老年心腦血管病雜志. 2022, 24 (1): 14-16.Wu WJ, Wu JZ, Huang GR, et al. Correlation between intestinal flora imbalance and HF in elderly idiopathic pulmonary fibrosis patients. Chin J Geriatr Heart Brain Vessel Dis, 2022, 24(1): 14-16.
10. Gong GC, Song SR, Su J. Pulmonary fibrosis alters gut microbiota and associated metabolites in mice: an integrated 16S and metabolomics analysis. Life Sci, 2021, 264: 118616.
11. Zhou A, Lei Y, Tang L, et al. Gut microbiota: the emerging link to lung homeostasis and disease. J Bacteriol, 2021, 203(4): e00454-420.
12. Budden KF, Gellatly SL, Wood DL, et al. Emerging pathogenic links between microbiota and the gut-lung axis. Nat Rev Microbiol, 2017, 15(1): 55-63.
13. Bird L. Gut microbiota influences liver disease. Nat Rev Immunol, 2012, 12(3): 153.
14. Smith GD, Ebrahim S. 'Mendelian randomization': can genetic epidemiology contribute to understanding environmental determinants of disease? Int J Epidemiol, 2003, 32(1): 1-22.
15. Lawlor DA, Harbord RM, Sterne JA, et al. Mendelian randomization: using genes as instruments for making causal inferences in epidemiology. Stat Med, 2008, 27(8): 1133-1163.
16. Weith M, Beyer A. The next step in Mendelian randomization. Elife, 2023, 12: e86416.
17. Shi H, Zhao T, Geng R, et al. The associations between gut microbiota and chronic respiratory diseases: a Mendelian randomization study. Front Microbiol, 2023, 14: 1200937.
18. 馬瑋瑋, 陳虹谷, 李彤彤, 等. 基于孟德爾隨機化分析腸道菌群與骨密度的因果關系. 中國骨質疏松雜志. 2023, 29(12): 1780-1785.Ma WW, Chen HG, Li TT, et al. The causal relationship between gut microbiota and bone mineral density based on Mendelian randomization. Chin J Osteoporos, 2023, 29(12): 1780-1785.
19. Chen J, Ruan X, Yuan S, et al. Antioxidants, minerals and vitamins in relation to Crohn's disease and ulcerative colitis: a Mendelian randomization study. Aliment Pharmacol Ther, 2023, 57(4): 399-408.
20. Reynolds CJ, Del Greco MF, Allen RJ, et al. The causal relationship between gastro-oesophageal reflux disease and idiopathic pulmonary fibrosis: a bidirectional two-sample Mendelian randomisation study. Eur Respir J, 2023, 61(5): 2201585.
21. Zhao W, Wang L, Wang Y, et al. Injured endothelial cell: a risk factor for pulmonary fibrosis. Int J Mol Sci, 2023, 24(10): 8749.
22. Kurilshikov A, Medina-Gomez C, Bacigalupe R, et al. Large-scale association analyses identify host factors influencing human gut microbiome composition. Nat Genet, 2021, 53(2): 156-165.
23. Zhou CC, Pang Y, He Y, et al. A Mendelian randomization study of depression and risk of breast cancer. Chin Ment Health J, 2023, 37(6): 471-478.
24. Desbonnet L, Garrett L, Clarke G, et al. Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neurosci, 2010, 170(4): 1179-1188.
25. Groeger D, O'Mahony L, Murphy EF, et al. Bifidobacterium infantis 35624 modulates host inflammatory processes beyond the gut. Gut Microbes, 2013, 4(4): 325-339.
26. Wu X, Wei X, Li X, et al. Diversity of fungi and bacteria in bronchoalveolar lavage fluid during development of chronic obstructive pulmonary disease. Jpn J Infect Dis, 2022, 75(6): 560-568.
27. Marimón JM, Sorarrain A, Ercibengoa M, et al. Lung microbiome on admission in critically ill patients with acute bacterial and viral pneumonia. Sci Rep, 2023, 13(1): 17724.
28. Alghetaa H, Mohammed A, Zhou J, et al. Resveratrol-mediated attenuation of superantigen-driven acute respiratory distress syndrome is mediated by microbiota in the lungs and gut. Pharmacol Res, 2021, 167: 105548.
29. Man MA, Ungur RA, Motoc NS, et al. Lung microbiota in idiopathic pulmonary fibrosis, hypersensitivity pneumonitis, and unclassified interstitial lung diseases: a preliminary pilot study. Diagnostics (Basel), 2023, 13(19): 3157.
30. Ramphal W, Raaijmakers NJ, van der Klift M, et al. Mycotic aneurysm caused by Clostridium septicum in a patient with colorectal cancer. Infection, 2018, 46(5): 711-716.
31. Macha K, Giede-Jeppe A, Lücking H, et al. Ischaemic stroke and Clostridium septicum sepsis and meningitis in a patient with occult colon carcinoma: a case report and review of the literature. BMC Neurol, 2016, 16(1): 239.
32. Giannos P, Prokopidis K. Gut dysbiosis and long COVID-19: feeling gutted. J Med Virol, 2022, 94(7): 2917-2918.
33. Liu Z, Peng Y, Zhao L, et al. MFE40-the active fraction of Mume Fructus alcohol extract-alleviates Crohn's disease and its complications. J Ethnopharmacol, 2022, 296: 115465.
34. 任清林, 何文博, 岳佳瑞, 等. 兩樣本孟德爾隨機化分析腸道菌群與肺癌的因果關系. 中國胸心血管外科臨床雜志, 2023, 30(11): 1618-1627.Ren QL, He WB, Yue JR, et al. Association of lung cancer and gut microbiota: a two-sample Mendelian randomization analysis. Chin J Clin Thorac Cardiovasc Surg, 2023, 30(11): 1618-1627.
35. Yumoto H, Hirota K, Hirao K, et al. The pathogenic factors from oral streptococci for systemic diseases. Int J Mol Sci, 2019, 20(18): 4571.
36. 王文浩. 基于高通量測序技術分析手術對食管鱗癌患者腸道菌群的影響. 河南大學, 2023.Wang WH. Analysis of the influence of operation on intestinal flora of patients with esophageal squamous cell carcinoma based on high-throughput sequencing technique. Henan University, 2023.
37. 趙勇, 鄒倩, 夏方妹, 等. 基于16S rDNA測序的自身免疫性甲狀腺疾病患者腸道菌群研究. 中國微生態學雜志, 2023, 35(7): 765-771,777.Zhao Y, Zou Q, Xia FM, et al. Intestinal flora in patients with autoimmune thyroid disease based on 16S rDNA sequencing. Chin J Microecol, 2023, 35(7): 765-771,777.
38. Haruta I, Kikuchi K, Hashimoto E, et al. A possible role of histone-like DNA-binding protein of Streptococcus intermedius in the pathogenesis of bile duct damage in primary biliary cirrhosis. Clin Immunol, 2008, 127(2): 245-251.
39. Pichavant M, Sharan R, Le Rouzic O, et al. IL-22 defect during Streptococcus pneumoniae infection triggers exacerbation of chronic obstructive pulmonary disease. EBioMedicine, 2015, 2(11): 1686-1696.
40. Yu L, Hong Y, Maishi N, et al. Oral bacterium Streptococcus mutans promotes tumor metastasis through thrombosis formation. Cancer Sci, 2024, 115(2): 648-659.
41. Yu L, Maishi N, Akahori E, et al. The oral bacterium Streptococcus mutans promotes tumor metastasis by inducing vascular inflammation. Cancer Sci, 2022, 113(11): 3980-3994.
42. Han MK, Zhou Y, Murray S, et al. Lung microbiome and disease progression in idiopathic pulmonary fibrosis: an analysis of the COMET study. Lancet Respir Med, 2014, 2(7): 548-556.
43. Knippenberg S, Ueberberg B, Maus R, et al. Streptococcus pneumoniae triggers progression of pulmonary fibrosis through pneumolysin. Thorax, 2015, 70(7): 636-646.
44. Kim H, Shin J, Kim S, et al. Bifidobacterium bifidum BGN4 and Bifidobacterium longum BORI promotes neuronal rejuvenation in aged mice. Biochem Biophys Res Commun, 2022, 603: 41-48.
45. Xia M, Xu Y, Li H, et al. Structural and functional alteration of the gut microbiota in elderly patients with hyperlipidemia. Front Cell Infect Microbiol, 2024, 14: 1333145.
46. Budden KF, Gellatly SL, Vaughan A, et al. Probiotic Bifidobacterium longum subsp. longum protects against cigarette smoke-induced inflammation in mice. Int J Mol Sci, 2022, 24(1): 252.
47. Duranti S, Vivo V, Zini I, et al. Bifidobacterium bifidum PRL2010 alleviates intestinal ischemia/reperfusion injury. PLoS One, 2018, 13(8): e0202670.
48. Chioma OS, Mallott EK, Chapman A, et al. Gut microbiota modulates lung fibrosis severity following acute lung injury in mice. Commun Biol, 2022, 5(1): 1401.
49. 徐婷, 沈佳豪, 趙康, 等. 基于瘤胃球菌微生物群豐度構建疾病類型預測的腸道菌群標簽. 生物技術進展, 2024, 14(2): 323-330.Xu T, Shen JH, Zhao K, et al. Bacterial signature for prediction of disease type based on abundance of Ruminococcus. Biotechnol Bull, 2024, 14(2): 323-330.
50. Aishwarya S, Gunasekaran K. Meta-analysis of the microbial biomarkers in the gut-lung crosstalk in COVID-19, community-acquired pneumonia and Clostridium difficile infections. Lett Appl Microbiol, 2022, 75(5): 1293-1306.
51. Liu JX, Yuan HY, Li YN, et al. Ephedra sinica polysaccharide alleviates airway inflammations of mouse asthma-like induced by PM2.5 and ovalbumin via the regulation of gut microbiota and short chain fatty acid. J Pharm Pharmacol, 2022, 74(12): 1784-1796.
52. Wan Y, Wang S, Niu Y, et al. Effect of metformin on sepsis-associated acute lung injury and gut microbiota in aged rats with sepsis. Front Cell Infect Microbiol, 2023, 13: 1139436.
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Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Causal relationship between gut microbiota and idiopathic pulmonary fibrosis: A bi-directional two-sample Mendelian randomization study

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