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Longitudinal multicompartment characterization of host-microbiota interactions in patients with acute respiratory failure

Author

Listed:
  • Georgios D. Kitsios

    (University of Pittsburgh
    University of Pittsburgh)

  • Khaled Sayed

    (University of Florida
    University of New Haven)

  • Adam Fitch

    (University of Pittsburgh)

  • Haopu Yang

    (Tsinghua University)

  • Noel Britton

    (Johns Hopkins University School of Medicine)

  • Faraaz Shah

    (University of Pittsburgh
    Veteran’s Affairs Pittsburgh Healthcare System)

  • William Bain

    (University of Pittsburgh
    Veteran’s Affairs Pittsburgh Healthcare System)

  • John W. Evankovich

    (University of Pittsburgh)

  • Shulin Qin

    (University of Pittsburgh
    University of Pittsburgh)

  • Xiaohong Wang

    (University of Pittsburgh
    University of Pittsburgh)

  • Kelvin Li

    (University of Pittsburgh)

  • Asha Patel

    (University of Pittsburgh
    University of Pittsburgh)

  • Yingze Zhang

    (University of Pittsburgh)

  • Josiah Radder

    (University of Pittsburgh
    University of Pittsburgh)

  • Charles Cruz

    (University of Pittsburgh)

  • Daniel A. Okin

    (Massachusetts General Hospital and Harvard Medical School)

  • Ching‐Ying Huang

    (Massachusetts General Hospital and Harvard Medical School)

  • Daria Tyne

    (University of Pittsburgh)

  • Panayiotis V. Benos

    (University of Florida)

  • Barbara Methé

    (University of Pittsburgh
    University of Pittsburgh)

  • Peggy Lai

    (Massachusetts General Hospital and Harvard Medical School)

  • Alison Morris

    (University of Pittsburgh
    University of Pittsburgh)

  • Bryan J. McVerry

    (University of Pittsburgh
    University of Pittsburgh)

Abstract

Critical illness can significantly alter the composition and function of the human microbiome, but few studies have examined these changes over time. Here, we conduct a comprehensive analysis of the oral, lung, and gut microbiota in 479 mechanically ventilated patients (223 females, 256 males) with acute respiratory failure. We use advanced DNA sequencing technologies, including Illumina amplicon sequencing (utilizing 16S and ITS rRNA genes for bacteria and fungi, respectively, in all sample types) and Nanopore metagenomics for lung microbiota. Our results reveal a progressive dysbiosis in all three body compartments, characterized by a reduction in microbial diversity, a decrease in beneficial anaerobes, and an increase in pathogens. We find that clinical factors, such as chronic obstructive pulmonary disease, immunosuppression, and antibiotic exposure, are associated with specific patterns of dysbiosis. Interestingly, unsupervised clustering of lung microbiota diversity and composition by 16S independently predicted survival and performed better than traditional clinical and host-response predictors. These observations are validated in two separate cohorts of COVID-19 patients, highlighting the potential of lung microbiota as valuable prognostic biomarkers in critical care. Understanding these microbiome changes during critical illness points to new opportunities for microbiota-targeted precision medicine interventions.

Suggested Citation

  • Georgios D. Kitsios & Khaled Sayed & Adam Fitch & Haopu Yang & Noel Britton & Faraaz Shah & William Bain & John W. Evankovich & Shulin Qin & Xiaohong Wang & Kelvin Li & Asha Patel & Yingze Zhang & Jos, 2024. "Longitudinal multicompartment characterization of host-microbiota interactions in patients with acute respiratory failure," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48819-8
    DOI: 10.1038/s41467-024-48819-8
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    References listed on IDEAS

    as
    1. Ian Holmes & Keith Harris & Christopher Quince, 2012. "Dirichlet Multinomial Mixtures: Generative Models for Microbial Metagenomics," PLOS ONE, Public Library of Science, vol. 7(2), pages 1-15, February.
    2. Kadi J. Horn & Melissa A. Schopper & Zoe G. Drigot & Sarah E. Clark, 2022. "Airway Prevotella promote TLR2-dependent neutrophil activation and rapid clearance of Streptococcus pneumoniae from the lung," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Verónica Lloréns-Rico & Ann C. Gregory & Johan Van Weyenbergh & Sander Jansen & Tina Van Buyten & Junbin Qian & Marcos Braz & Soraya Maria Menezes & Pierre Van Mol & Lore Vanderbeke & Christophe Dooms, 2021. "Clinical practices underlie COVID-19 patient respiratory microbiome composition and its interactions with the host," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
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    1. Natasha Spottiswoode & Alexandra Tsitsiklis & Victoria T. Chu & Hoang Van Phan & Catherine DeVoe & Christina Love & Rajani Ghale & Joshua Bloomstein & Beth Shoshana Zha & Cole P. Maguire & Abigail Gla, 2024. "Microbial dynamics and pulmonary immune responses in COVID-19 secondary bacterial pneumonia," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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