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Gut to lung translocation and antibiotic mediated selection shape the dynamics of Pseudomonas aeruginosa in an ICU patient

Author

Listed:
  • Rachel M. Wheatley

    (University of Oxford, Department of Biology)

  • Julio Diaz Caballero

    (University of Oxford, Department of Biology)

  • Thomas E. Schalk

    (University of Antwerp)

  • Fien H. R. Winter

    (University of Antwerp)

  • Liam P. Shaw

    (University of Oxford, Department of Biology)

  • Natalia Kapel

    (University of Oxford, Department of Biology)

  • Claudia Recanatini

    (University Medical Center Utrecht, Utrecht University)

  • Leen Timbermont

    (University of Antwerp)

  • Jan Kluytmans

    (University Medical Center Utrecht, Utrecht University)

  • Mark Esser

    (Microbial Sciences, BioPharmaceuticals R&D, AstraZeneca)

  • Alicia Lacoma

    (Universitat Autònoma de Barcelona)

  • Cristina Prat-Aymerich

    (University Medical Center Utrecht, Utrecht University
    Universitat Autònoma de Barcelona)

  • Antonio Oliver

    (Servicio de Microbiología, Hospital Universitari Son Espases, Instituto de Investigación Sanitaria Illes Balears (IdISBa))

  • Samir Kumar-Singh

    (University of Antwerp
    University of Antwerp)

  • Surbhi Malhotra-Kumar

    (University of Antwerp)

  • R. Craig MacLean

    (University of Oxford, Department of Biology)

Abstract

Bacteria have the potential to translocate between sites in the human body, but the dynamics and consequences of within-host bacterial migration remain poorly understood. Here we investigate the link between gut and lung Pseudomonas aeruginosa populations in an intensively sampled ICU patient using a combination of genomics, isolate phenotyping, host immunity profiling, and clinical data. Crucially, we show that lung colonization in the ICU was driven by the translocation of P. aeruginosa from the gut. Meropenem treatment for a suspected urinary tract infection selected for elevated resistance in both the gut and lung. However, resistance was driven by parallel evolution in the gut and lung coupled with organ specific selective pressures, and translocation had only a minor impact on AMR. These findings suggest that reducing intestinal colonization of Pseudomonas may be an effective way to prevent lung infections in critically ill patients.

Suggested Citation

  • Rachel M. Wheatley & Julio Diaz Caballero & Thomas E. Schalk & Fien H. R. Winter & Liam P. Shaw & Natalia Kapel & Claudia Recanatini & Leen Timbermont & Jan Kluytmans & Mark Esser & Alicia Lacoma & Cr, 2022. "Gut to lung translocation and antibiotic mediated selection shape the dynamics of Pseudomonas aeruginosa in an ICU patient," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34101-2
    DOI: 10.1038/s41467-022-34101-2
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    References listed on IDEAS

    as
    1. Hattie Chung & Christina Merakou & Matthew M. Schaefers & Kelly B. Flett & Sarah Martini & Roger Lu & Jennifer A. Blumenthal & Shanice S. Webster & Ashley R. Cross & Roy Al Ahmar & Erin Halpin & Miche, 2022. "Rapid expansion and extinction of antibiotic resistance mutations during treatment of acute bacterial respiratory infections," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    2. Hattie Chung & Tami D. Lieberman & Sara O. Vargas & Kelly B. Flett & Alexander J. McAdam & Gregory P. Priebe & Roy Kishony, 2017. "Global and local selection acting on the pathogen Stenotrophomonas maltophilia in the human lung," Nature Communications, Nature, vol. 8(1), pages 1-7, April.
    3. A. San Millan & R. Peña-Miller & M. Toll-Riera & Z. V. Halbert & A. R. McLean & B. S. Cooper & R. C. MacLean, 2014. "Positive selection and compensatory adaptation interact to stabilize non-transmissible plasmids," Nature Communications, Nature, vol. 5(1), pages 1-11, December.
    4. Rachel Wheatley & Julio Diaz Caballero & Natalia Kapel & Fien H. R. Winter & Pramod Jangir & Angus Quinn & Ester Barrio-Tofiño & Carla López-Causapé & Jessica Hedge & Gabriel Torrens & Thomas Schalk &, 2021. "Rapid evolution and host immunity drive the rise and fall of carbapenem resistance during an acute Pseudomonas aeruginosa infection," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
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    Cited by:

    1. Julio Diaz Caballero & Rachel M. Wheatley & Natalia Kapel & Carla López-Causapé & Thomas Van der Schalk & Angus Quinn & Liam P. Shaw & Lois Ogunlana & Claudia Recanatini & Basil Britto Xavier & Leen T, 2023. "Mixed strain pathogen populations accelerate the evolution of antibiotic resistance in patients," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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