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

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, Josiah Radder, Charles Cruz, Daniel A. Okin, Ching‐Ying Huang, Daria Tyne, Panayiotis V. Benos, Barbara Methé, Peggy Lai, Alison Morris and Bryan J. McVerry
Additional contact information
Georgios D. Kitsios: University of Pittsburgh
Khaled Sayed: University of Florida
Adam Fitch: University of Pittsburgh
Haopu Yang: Tsinghua University
Noel Britton: Johns Hopkins University School of Medicine
Faraaz Shah: University of Pittsburgh
William Bain: University of Pittsburgh
John W. Evankovich: University of Pittsburgh
Shulin Qin: University of Pittsburgh
Xiaohong Wang: University of Pittsburgh
Kelvin Li: University of Pittsburgh
Asha Patel: University of Pittsburgh
Yingze Zhang: University of Pittsburgh
Josiah Radder: 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
Peggy Lai: Massachusetts General Hospital and Harvard Medical School
Alison Morris: University of Pittsburgh
Bryan J. McVerry: University of Pittsburgh

Nature Communications, 2024, vol. 15, issue 1, 1-18

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-48819-8

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