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Loss of microbial diversity and pathogen domination of the gut microbiota in critically ill patients

Anuradha Ravi, Fenella D Halstead, Amy Bamford, Anna Casey, Nicholas M. Thomson, Willem van Schaik, Catherine Snelson, Robert Goulden, Ebenezer Foster-Nyarko, George M. Savva, Tony Whitehouse, Mark J. Pallen, Beryl A. Oppenheim
doi: https://doi.org/10.1101/582494
Anuradha Ravi
Quadram Institute Bioscience and University of East Anglia, Norwich, NR4 7UA, United Kingdom
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Fenella D Halstead
NIHR Surgical Reconstruction and Microbiology Research Centre, Queen Elizabeth Hospital, Birmingham, B15 2GW, United KingdomQueen Elizabeth Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, B15 2GW, United Kingdom
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Amy Bamford
NIHR Surgical Reconstruction and Microbiology Research Centre, Queen Elizabeth Hospital, Birmingham, B15 2GW, United KingdomQueen Elizabeth Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, B15 2GW, United Kingdom
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Anna Casey
NIHR Surgical Reconstruction and Microbiology Research Centre, Queen Elizabeth Hospital, Birmingham, B15 2GW, United KingdomQueen Elizabeth Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, B15 2GW, United Kingdom
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Nicholas M. Thomson
Quadram Institute Bioscience and University of East Anglia, Norwich, NR4 7UA, United Kingdom
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Willem van Schaik
Institute of Microbiology and Infection, University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom
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Catherine Snelson
Queen Elizabeth Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, B15 2GW, United Kingdom
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Robert Goulden
McGill University, Montréal, QC H3G 2M1, Canada
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Ebenezer Foster-Nyarko
Quadram Institute Bioscience and University of East Anglia, Norwich, NR4 7UA, United Kingdom
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George M. Savva
Quadram Institute Bioscience and University of East Anglia, Norwich, NR4 7UA, United Kingdom
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Tony Whitehouse
Queen Elizabeth Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, B15 2GW, United Kingdom
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Mark J. Pallen
Quadram Institute Bioscience and University of East Anglia, Norwich, NR4 7UA, United Kingdom
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Beryl A. Oppenheim
NIHR Surgical Reconstruction and Microbiology Research Centre, Queen Elizabeth Hospital, Birmingham, B15 2GW, United KingdomQueen Elizabeth Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, B15 2GW, United Kingdom
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Abstract

Background For long-stay patients on the adult intensive care unit, the gut microbiota plays a key role in determining the balance between health and disease. However, it remains unclear which ICU patients might benefit from interventions targeting the gut microbiota or the pathogens therein.

Methods We undertook a prospective observational study of twenty-four ICU patients, in which serial faecal samples were subjected to shotgun metagenomic sequencing, phylogenetic profiling and microbial genome analyses.

Results Two-thirds of patients experienced a marked drop in gut microbial diversity (to an inverse Simpson’s index of <4) at some stage during their stay in ICU, often accompanied by absence or loss of beneficial commensal bacteria. Intravenous administration of the broad-spectrum antimicrobial agent meropenem was significantly associated with loss of gut microbial diversity, but administration of other antibiotics, including piperacillin-tazobactam, failed to trigger statistically detectable changes in microbial diversity. In three quarters of ICU patients, we documented episodes of gut domination by pathogenic strains, with evidence of cryptic nosocomial transmission of Enterococcus faecium. In some patients we also saw domination of the gut microbiota by commensal organisms, such as Methanobrevibacter smithii.

Conclusions Our results support a role for metagenomic surveillance of the gut microbiota and pave the way for patient-specific interventions that maintain or restore gut microbial diversity in the ICU.

  • Abbreviations

    ICU
    Intensive Care Unit
    MAG
    metagenome-assembled genome
    SOFA
    Sequential Organ Failure Assessment
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    Posted March 21, 2019.
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    Loss of microbial diversity and pathogen domination of the gut microbiota in critically ill patients
    Anuradha Ravi, Fenella D Halstead, Amy Bamford, Anna Casey, Nicholas M. Thomson, Willem van Schaik, Catherine Snelson, Robert Goulden, Ebenezer Foster-Nyarko, George M. Savva, Tony Whitehouse, Mark J. Pallen, Beryl A. Oppenheim
    bioRxiv 582494; doi: https://doi.org/10.1101/582494
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    Loss of microbial diversity and pathogen domination of the gut microbiota in critically ill patients
    Anuradha Ravi, Fenella D Halstead, Amy Bamford, Anna Casey, Nicholas M. Thomson, Willem van Schaik, Catherine Snelson, Robert Goulden, Ebenezer Foster-Nyarko, George M. Savva, Tony Whitehouse, Mark J. Pallen, Beryl A. Oppenheim
    bioRxiv 582494; doi: https://doi.org/10.1101/582494

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