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Relationship between COVID-19 and ICU-acquired colonization and infection related to multidrug-resistant bacteria: a prospective multicenter before-after study

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Abstract

Purpose

Patients presenting the most severe form of coronavirus disease 2019 (COVID-19) pneumonia, caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), have a prolonged intensive care unit (ICU) stay and are exposed to broad-spectrum antibiotics, but the impact of COVID-19 on antimicrobial resistance is unknown.

Methods

Observational prospective before-after study in 7 ICUs in France. All consecutive patients with an ICU stay > 48 h and a confirmed SARS-CoV-2 infection were included prospectively and followed for 28 days. Patients underwent systematic screening for colonization with multidrug-resistant (MDR) bacteria upon admission and every week subsequently. COVID-19 patients were compared to a recent prospective cohort of control patients from the same ICUs. The primary objective was to investigate the association of COVID-19 with the cumulative incidence of a composite outcome including ICU-acquired colonization and/or infection related to MDR bacteria (ICU-MDR-col and ICU-MDR-inf, respectively).

Results

From February 27th, 2020 to June 2nd, 2021, 367 COVID-19 patients were included, and compared to 680 controls. After adjustment for prespecified baseline confounders, the cumulative incidence of ICU-MDR-col and/or ICU-MDR-inf was not significantly different between groups (adjusted sub-hazard ratio [sHR] 1.39, 95% confidence interval [CI] 0.91–2.09). When considering both outcomes separately, COVID-19 patients had a higher incidence of ICU-MDR-inf than controls (adjusted sHR 2.50, 95% CI 1.90–3.28), but the incidence of ICU-MDR-col was not significantly different between groups (adjusted sHR 1.27, 95% CI 0.85–1.88).

Conclusion

COVID-19 patients had an increased incidence of ICU-MDR-inf compared to controls, but the difference was not significant when considering a composite outcome including ICU-MDR-col and/or ICU-MDR-inf.

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Abbreviations

3GC:

Third-generation cephalosporins

AMR:

Antimicrobial resistance

CARB:

Carbapenem-resistant Acinetobacter baumannii

COPD:

Chronic obstructive pulmonary disease

COVID-19:

Coronavirus disease 2019

ECLS:

Extracorporeal life support

ECMO:

Extracorporeal membrane oxygenation

ESBL:

Extended-spectrum beta-lactamase

EUCAST:

European Committee on Antimicrobial Susceptibility Testing

HAI:

Healthcare-associated infection

HAP:

Healthcare-associated pneumonia

HIV:

Human immunodeficiency virus

ICU:

Intensive care unit

ICU-MDR-col:

ICU-acquired colonization with multidrug-resistant bacteria

ICU-MDR-inf:

ICU-acquired infection with multidrug-resistant bacteria

IQR:

Interquartile range

IMV:

Invasive mechanical ventilation

MDR:

Multidrug-resistant

MRSA:

Methicillin-resistant Staphylococcus aureus

PCR:

Polymerase chain reaction

SAPS-II:

Simplified Acute Physiology Score II

SARS-CoV-2:

Severe acute respiratory syndrome coronavirus 2

SOFA:

Sequential organ failure assessment

SOT:

Solid organ transplant

VAP:

Ventilator-associated pneumonia

VRE:

Vancomycin-resistant Enterococcus sp.

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Acknowledgements

We thank Hugo Coronado, Apolline Briatte, Nafas Abdallah Paune, Hajar Chouiki, Stéphanie Beaussart, Fabienne Jarosz-Thévenin, Anne Dewatine and Sabine Janowski for their help in data curation and study supervision. We thank Alison Holmes and Ho Kwong Li for their critical appraisal of the manuscript.

Funding

There was no funding for this study.

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Authors and Affiliations

  1. Médecine Intensive Réanimation, Hôpital R. Salengro, CHU de Lille, Rue E. Laine, 59037, Lille Cedex, France

    Louis Kreitmann, Sonia Jermoumi, Margot Vasseur & Saad Nseir

  2. Médecine Intensive Réanimation, Hospices Civils de Lyon, Hôpital Edouard Herriot, 69437, Lyon Cedex 03, France

    Louis Kreitmann, Myriam Chabani & Emilie Nourry

  3. Médecine Intensive Réanimation, Hospices Civils de Lyon, Hôpital de la Croix Rousse, 69004, Lyon, France

    Jean-Christophe Richard

  4. Service de Réanimation, Hospices Civils de Lyon, Groupement Hospitalier Sud, 69637, Pierre Bénite, France

    Florent Wallet

  5. Centre International de Recherche en Infectiologie (CIRI), INSERM U1111, CNRS UMR5308, ENS Lyon, Université Claude Bernard Lyon, Lyon, France

    Florent Wallet

  6. Réanimation, Grand Hôpital de l’Est Francilien, Site de Marne-la-Vallée, Jossigny, France

    Pierre Garçon & Safaâ Kachmar

  7. Médecine Intensive Réanimation, Centre Hospitalier Universitaire Amiens-Picardie, Amiens, France

    Yoann Zerbib

  8. Service de Réanimation Polyvalente, Centre Hospitalier de Lens, Lens, France

    Nicolas Van Grunderbeeck

  9. Intensive Care Unit, Hôpital de Béthune, 62408, Béthune, France

    Christophe Vinsonneau

  10. Department of Biostatistics, CHU Lille, 59000, Lille, France

    Alain Duhamel & Julien Labreuche

  11. Inserm U1285, Université de Lille, CNRS, UMR 8576-UGSF, 59000, Lille, France

    Saad Nseir

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  1. Louis Kreitmann
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Contributions

Study conception and design: LK, SN. Statistical analysis: AD, JL. Data curation: LK, SJ, MV, MC, EN, JCR, FW, PG, SK, YZ, NVG, CV. Manuscript drafting: LK, JL, SN. Critical revision: all authors.

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Correspondence to Saad Nseir.

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Conflicts of interest

LK has received speaking fees and a research scholarship from BioMérieux, and has been employed by Transgene. SN has received speaking fees from MSD, Pfizer, Gilead, BioMérieux, Fischer and Paykel, and BioRad. JCR received a grant from Hamilton Medical for an experimental study. Other authors have no competing interest.

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Kreitmann, L., Jermoumi, S., Vasseur, M. et al. Relationship between COVID-19 and ICU-acquired colonization and infection related to multidrug-resistant bacteria: a prospective multicenter before-after study. Intensive Care Med 49, 796–807 (2023). https://doi.org/10.1007/s00134-023-07109-5

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