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Published in: Critical Care 1/2024

Open Access 01-12-2024 | ECMO | Research

Healthcare-associated infections in patients with severe COVID-19 supported with extracorporeal membrane oxygenation: a nationwide cohort study

Authors: Nicolas Nesseler, Alexandre Mansour, Matthieu Schmidt, Marylou Para, Alizée Porto, Pierre-Emmanuel Falcoz, Nicolas Mongardon, Claire Fougerou, James T. Ross, Antoine Beurton, Lucie Gaide-Chevronnay, Pierre-Grégoire Guinot, Guillaume Lebreton, Erwan Flecher, André Vincentelli, Nicolas Massart, ECMOSARS Investigators, SFAR Research Network

Published in: Critical Care | Issue 1/2024

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Abstract

Background

Both critically ill patients with coronavirus disease 2019 (COVID-19) and patients receiving extracorporeal membrane oxygenation (ECMO) support exhibit a high incidence of healthcare-associated infections (HAI). However, data on incidence, microbiology, resistance patterns, and the impact of HAI on outcomes in patients receiving ECMO for severe COVID-19 remain limited. We aimed to report HAI incidence and microbiology in patients receiving ECMO for severe COVID-19 and to evaluate the impact of ECMO-associated infections (ECMO-AI) on in-hospital mortality.

Methods

For this study, we analyzed data from 701 patients included in the ECMOSARS registry which included COVID-19 patients supported by ECMO in France.

Results

Among 602 analyzed patients for whom HAI and hospital mortality data were available, 214 (36%) had ECMO-AI, resulting in an incidence rate of 27 ECMO-AI per 1000 ECMO days at risk. Of these, 154 patients had bloodstream infection (BSI) and 117 patients had ventilator-associated pneumonia (VAP). The responsible microorganisms were Enterobacteriaceae (34% for BSI and 48% for VAP), Enterococcus species (25% and 6%, respectively) and non-fermenting Gram-negative bacilli (13% and 20%, respectively). Fungal infections were also observed (10% for BSI and 3% for VAP), as were multidrug-resistant organisms (21% and 15%, respectively). Using a Cox multistate model, ECMO-AI were not found associated with hospital death (HR = 1.00 95% CI [0.79–1.26], p = 0.986).

Conclusions

In a nationwide cohort of COVID-19 patients receiving ECMO support, we observed a high incidence of ECMO-AI. ECMO-AI were not found associated with hospital death.
Trial registration number NCT04397588 (May 21, 2020).
Appendix
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Literature
1.
go back to reference Schmidt M, Bréchot N, Hariri S, Guiguet M, Luyt CE, Makri R, et al. Nosocomial Infections in adult cardiogenic shock patients supported by venoarterial extracorporeal membrane oxygenation. Clin Infect Dis. 2012;55:1633–41.CrossRefPubMedPubMedCentral Schmidt M, Bréchot N, Hariri S, Guiguet M, Luyt CE, Makri R, et al. Nosocomial Infections in adult cardiogenic shock patients supported by venoarterial extracorporeal membrane oxygenation. Clin Infect Dis. 2012;55:1633–41.CrossRefPubMedPubMedCentral
2.
go back to reference Grasselli G, Scaravilli V, Bella SD, Biffi S, Bombino M, Patroniti N, et al. Nosocomial infections during extracorporeal membrane oxygenation. Crit Care Med. 2017;45:1726–33.CrossRefPubMed Grasselli G, Scaravilli V, Bella SD, Biffi S, Bombino M, Patroniti N, et al. Nosocomial infections during extracorporeal membrane oxygenation. Crit Care Med. 2017;45:1726–33.CrossRefPubMed
3.
go back to reference Vacheron C-H, Lepape A, Savey A, Machut A, Timsit JF, Vanhems P, et al. Increased incidence of ventilator-acquired pneumonia in coronavirus disease 2019 patients: a multicentric cohort study*. Crit Care Med. 2022;50:449–59.CrossRefPubMed Vacheron C-H, Lepape A, Savey A, Machut A, Timsit JF, Vanhems P, et al. Increased incidence of ventilator-acquired pneumonia in coronavirus disease 2019 patients: a multicentric cohort study*. Crit Care Med. 2022;50:449–59.CrossRefPubMed
4.
go back to reference Lepape A, Machut A, Bretonnière C, Friggeri A, Vacheron C-H, Savey A, et al. Effect of SARS-CoV-2 infection and pandemic period on healthcare-associated infections acquired in intensive care units. Clin Microbiol Infect. 2023;29:530–6.CrossRefPubMed Lepape A, Machut A, Bretonnière C, Friggeri A, Vacheron C-H, Savey A, et al. Effect of SARS-CoV-2 infection and pandemic period on healthcare-associated infections acquired in intensive care units. Clin Microbiol Infect. 2023;29:530–6.CrossRefPubMed
5.
go back to reference Rouzé A, Martin-Loeches I, Povoa P, Makris D, Artigas A, Bouchereau M, et al. Relationship between SARS-CoV-2 infection and the incidence of ventilator-associated lower respiratory tract infections: a European multicenter cohort study. Intensiv Care Med. 2021;47:188–98.CrossRef Rouzé A, Martin-Loeches I, Povoa P, Makris D, Artigas A, Bouchereau M, et al. Relationship between SARS-CoV-2 infection and the incidence of ventilator-associated lower respiratory tract infections: a European multicenter cohort study. Intensiv Care Med. 2021;47:188–98.CrossRef
6.
go back to reference Frerou A, Lesouhaitier M, Gregoire M, Uhel F, Gacouin A, Reizine F, et al. Venoarterial extracorporeal membrane oxygenation induces early immune alterations. Crit Care. 2021;25:9.CrossRefPubMedPubMedCentral Frerou A, Lesouhaitier M, Gregoire M, Uhel F, Gacouin A, Reizine F, et al. Venoarterial extracorporeal membrane oxygenation induces early immune alterations. Crit Care. 2021;25:9.CrossRefPubMedPubMedCentral
7.
go back to reference Reizine F, Lesouhaitier M, Gregoire M, Pinceaux K, Gacouin A, Maamar A, et al. SARS-CoV-2-Induced ARDS associates with MDSC expansion, lymphocyte dysfunction, and arginine shortage. J Clin Immunol. 2021;41:515–25.CrossRefPubMedPubMedCentral Reizine F, Lesouhaitier M, Gregoire M, Pinceaux K, Gacouin A, Maamar A, et al. SARS-CoV-2-Induced ARDS associates with MDSC expansion, lymphocyte dysfunction, and arginine shortage. J Clin Immunol. 2021;41:515–25.CrossRefPubMedPubMedCentral
8.
go back to reference Schmidt M, Hajage D, Landoll M, Pequignot B, Langouet E, Amalric M, et al. Comparative outcomes of extracorporeal membrane oxygenation for COVID-19 delivered in experienced European centres during successive SARS-CoV-2 variant outbreaks (ECMO-SURGES): an international, multicentre, retrospective cohort study. Lancet Respir Med. 2023;11:163–75.CrossRefPubMedPubMedCentral Schmidt M, Hajage D, Landoll M, Pequignot B, Langouet E, Amalric M, et al. Comparative outcomes of extracorporeal membrane oxygenation for COVID-19 delivered in experienced European centres during successive SARS-CoV-2 variant outbreaks (ECMO-SURGES): an international, multicentre, retrospective cohort study. Lancet Respir Med. 2023;11:163–75.CrossRefPubMedPubMedCentral
9.
go back to reference Luyt C-E, Sahnoun T, Gautier M, Vidal P, Burrel S, de Chambrun MP, et al. Ventilator-associated pneumonia in patients with SARS-CoV-2-associated acute respiratory distress syndrome requiring ECMO: a retrospective cohort study. Ann Intensiv Care. 2020;10:158.CrossRef Luyt C-E, Sahnoun T, Gautier M, Vidal P, Burrel S, de Chambrun MP, et al. Ventilator-associated pneumonia in patients with SARS-CoV-2-associated acute respiratory distress syndrome requiring ECMO: a retrospective cohort study. Ann Intensiv Care. 2020;10:158.CrossRef
10.
go back to reference Nesseler N, Fadel G, Mansour A, Para M, Falcoz P-E, Mongardon N, et al. Extracorporeal membrane oxygenation for respiratory failure related to COVID-19: a nationwide cohort study. Anesthesiology. 2022;136:732–48.CrossRefPubMed Nesseler N, Fadel G, Mansour A, Para M, Falcoz P-E, Mongardon N, et al. Extracorporeal membrane oxygenation for respiratory failure related to COVID-19: a nationwide cohort study. Anesthesiology. 2022;136:732–48.CrossRefPubMed
11.
go back to reference Massart N, Guervilly C, Mansour A, Porto A, Flécher E, Esvan M, et al. Impact of prone position in COVID-19 patients on extracorporeal membrane oxygenation*. Crit Care Med. 2023;51:36–46.CrossRefPubMed Massart N, Guervilly C, Mansour A, Porto A, Flécher E, Esvan M, et al. Impact of prone position in COVID-19 patients on extracorporeal membrane oxygenation*. Crit Care Med. 2023;51:36–46.CrossRefPubMed
12.
go back to reference Mansour A, Flecher E, Schmidt M, Rozec B, Gouin-Thibault I, Esvan M, et al. Bleeding and thrombotic events in patients with severe COVID-19 supported with extracorporeal membrane oxygenation: a nationwide cohort study. Intensiv Care Med. 2022;48:1039–52.CrossRef Mansour A, Flecher E, Schmidt M, Rozec B, Gouin-Thibault I, Esvan M, et al. Bleeding and thrombotic events in patients with severe COVID-19 supported with extracorporeal membrane oxygenation: a nationwide cohort study. Intensiv Care Med. 2022;48:1039–52.CrossRef
13.
go back to reference Lebreton G, Schmidt M, Ponnaiah M, Folliguet T, Para M, Guihaire J, et al. Extracorporeal membrane oxygenation network organisation and clinical outcomes during the COVID-19 pandemic in Greater Paris, France: a multicentre cohort study. Lancet Respir Med. 2021;9:851–62.CrossRefPubMedPubMedCentral Lebreton G, Schmidt M, Ponnaiah M, Folliguet T, Para M, Guihaire J, et al. Extracorporeal membrane oxygenation network organisation and clinical outcomes during the COVID-19 pandemic in Greater Paris, France: a multicentre cohort study. Lancet Respir Med. 2021;9:851–62.CrossRefPubMedPubMedCentral
14.
go back to reference Tabah A, Koulenti D, Laupland K, Misset B, Valles J, de Carvalho FB, et al. Characteristics and determinants of outcome of hospital-acquired bloodstream infections in intensive care units: the EUROBACT international cohort study. Intensiv Care Med. 2012;38:1930–45.CrossRef Tabah A, Koulenti D, Laupland K, Misset B, Valles J, de Carvalho FB, et al. Characteristics and determinants of outcome of hospital-acquired bloodstream infections in intensive care units: the EUROBACT international cohort study. Intensiv Care Med. 2012;38:1930–45.CrossRef
15.
go back to reference Leone M, Bouadma L, Bouhemad B, Brissaud O, Dauger S, Gibot S, et al. Hospital-acquired pneumonia in ICU. Anaesth Crit Care Pain Med. 2018;37:83–98.CrossRefPubMed Leone M, Bouadma L, Bouhemad B, Brissaud O, Dauger S, Gibot S, et al. Hospital-acquired pneumonia in ICU. Anaesth Crit Care Pain Med. 2018;37:83–98.CrossRefPubMed
16.
go back to reference Magiorakos A-P, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18:268–81.CrossRefPubMed Magiorakos A-P, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18:268–81.CrossRefPubMed
17.
go back to reference Escolano S, Golmard J, Korinek A, Mallet A. A multi-state model for evolution of intensive care unit patients: prediction of nosocomial infections and deaths. Stat Med. 2000;19:3465–82.CrossRefPubMed Escolano S, Golmard J, Korinek A, Mallet A. A multi-state model for evolution of intensive care unit patients: prediction of nosocomial infections and deaths. Stat Med. 2000;19:3465–82.CrossRefPubMed
18.
go back to reference Abrams D, Grasselli G, Schmidt M, Mueller T, Brodie D. ECLS-associated infections in adults: what we know and what we don’t yet know. Intensiv Care Med. 2020;46:182–91.CrossRef Abrams D, Grasselli G, Schmidt M, Mueller T, Brodie D. ECLS-associated infections in adults: what we know and what we don’t yet know. Intensiv Care Med. 2020;46:182–91.CrossRef
19.
go back to reference Clec’h C, Schwebel C, Français A, Toledano D, Fosse J-P, Garrouste-Orgeas M, et al. Does catheter-associated urinary tract infection increase mortality in critically patient? Infect Control Hosp Epidemiology. 2007;28:1367–73.CrossRef Clec’h C, Schwebel C, Français A, Toledano D, Fosse J-P, Garrouste-Orgeas M, et al. Does catheter-associated urinary tract infection increase mortality in critically patient? Infect Control Hosp Epidemiology. 2007;28:1367–73.CrossRef
20.
go back to reference Lambert M-L, Suetens C, Savey A, Palomar M, Hiesmayr M, Morales I, et al. Clinical outcomes of health-care-associated infections and antimicrobial resistance in patients admitted to European intensive-care units: a cohort study. Lancet Infect Dis. 2011;11:30–8.CrossRefPubMed Lambert M-L, Suetens C, Savey A, Palomar M, Hiesmayr M, Morales I, et al. Clinical outcomes of health-care-associated infections and antimicrobial resistance in patients admitted to European intensive-care units: a cohort study. Lancet Infect Dis. 2011;11:30–8.CrossRefPubMed
21.
go back to reference Martin-Loeches I, Povoa P, Rodríguez A, Curcio D, Suarez D, Mira J-P, et al. Incidence and prognosis of ventilator-associated tracheobronchitis (TAVeM): a multicentre, prospective, observational study. Lancet Respir Med. 2015;3:859–68.CrossRefPubMed Martin-Loeches I, Povoa P, Rodríguez A, Curcio D, Suarez D, Mira J-P, et al. Incidence and prognosis of ventilator-associated tracheobronchitis (TAVeM): a multicentre, prospective, observational study. Lancet Respir Med. 2015;3:859–68.CrossRefPubMed
22.
go back to reference Aubron C, Cheng AC, Pilcher D, Leong T, Magrin G, Cooper DJ, et al. Infections acquired by adults who receive extracorporeal membrane oxygenation risk factors and outcome. Infect Control Hosp Epidemiology. 2013;34:24–30.CrossRef Aubron C, Cheng AC, Pilcher D, Leong T, Magrin G, Cooper DJ, et al. Infections acquired by adults who receive extracorporeal membrane oxygenation risk factors and outcome. Infect Control Hosp Epidemiology. 2013;34:24–30.CrossRef
23.
go back to reference Bonten MJ, Gaillard CA, van Tiel FH, van der Geest S, Stobberingh EE. Colonization and infection with Enterococcus faecalis in intensive care units: the role of antimicrobial agents. Antimicrob Agents Chemother. 1995;39:2783–6.CrossRefPubMedPubMedCentral Bonten MJ, Gaillard CA, van Tiel FH, van der Geest S, Stobberingh EE. Colonization and infection with Enterococcus faecalis in intensive care units: the role of antimicrobial agents. Antimicrob Agents Chemother. 1995;39:2783–6.CrossRefPubMedPubMedCentral
24.
go back to reference Pultz NJ, Stiefel U, Subramanyan S, Helfand MS, Donskey CJ. Mechanisms by which anaerobic microbiota inhibit the establishment in mice of intestinal colonization by vancomycin-resistant enterococcus. J Infect Dis. 2005;191:949–56.CrossRefPubMed Pultz NJ, Stiefel U, Subramanyan S, Helfand MS, Donskey CJ. Mechanisms by which anaerobic microbiota inhibit the establishment in mice of intestinal colonization by vancomycin-resistant enterococcus. J Infect Dis. 2005;191:949–56.CrossRefPubMed
25.
go back to reference Lund B, Agvald-Öhman C, Hultberg A, Edlund C. Frequent transmission of enterococcal strains between mechanically ventilated patients treated at an intensive care unit. J Clin Microbiol. 2002;40:2084–8.CrossRefPubMedPubMedCentral Lund B, Agvald-Öhman C, Hultberg A, Edlund C. Frequent transmission of enterococcal strains between mechanically ventilated patients treated at an intensive care unit. J Clin Microbiol. 2002;40:2084–8.CrossRefPubMedPubMedCentral
26.
go back to reference Abelenda-Alonso G, Rombauts A, Gudiol C, Oriol I, Simonetti A, Coloma A, et al. Immunomodulatory therapy, risk factors and outcomes of hospital-acquired bloodstream infection in patients with severe COVID-19 pneumonia: a Spanish case–control matched multicentre study (BACTCOVID). Clin Microbiol Infect. 2021;27:1685–92.CrossRefPubMedPubMedCentral Abelenda-Alonso G, Rombauts A, Gudiol C, Oriol I, Simonetti A, Coloma A, et al. Immunomodulatory therapy, risk factors and outcomes of hospital-acquired bloodstream infection in patients with severe COVID-19 pneumonia: a Spanish case–control matched multicentre study (BACTCOVID). Clin Microbiol Infect. 2021;27:1685–92.CrossRefPubMedPubMedCentral
27.
go back to reference de Roux Q, Botterel F, Lepeule R, Taccone FS, Langeron O, Mongardon N. Candida bloodstream infection under veno-arterial ECMO therapy. Crit Care. 2019;23:314.CrossRefPubMedPubMedCentral de Roux Q, Botterel F, Lepeule R, Taccone FS, Langeron O, Mongardon N. Candida bloodstream infection under veno-arterial ECMO therapy. Crit Care. 2019;23:314.CrossRefPubMedPubMedCentral
28.
go back to reference Melsen WG, Rovers MM, Groenwold RH, Bergmans DC, Camus C, Bauer TT, et al. Attributable mortality of ventilator-associated pneumonia: a meta-analysis of individual patient data from randomised prevention studies. Lancet Infect Dis. 2013;13:665–71.CrossRefPubMed Melsen WG, Rovers MM, Groenwold RH, Bergmans DC, Camus C, Bauer TT, et al. Attributable mortality of ventilator-associated pneumonia: a meta-analysis of individual patient data from randomised prevention studies. Lancet Infect Dis. 2013;13:665–71.CrossRefPubMed
29.
go back to reference Peña-López Y, Machado MC, Rello J. Infection in ECMO patients: changes in epidemiology, diagnosis and prevention. Anaesth Crit Care Pain Med. 2024;43: 101319.CrossRefPubMed Peña-López Y, Machado MC, Rello J. Infection in ECMO patients: changes in epidemiology, diagnosis and prevention. Anaesth Crit Care Pain Med. 2024;43: 101319.CrossRefPubMed
Metadata
Title
Healthcare-associated infections in patients with severe COVID-19 supported with extracorporeal membrane oxygenation: a nationwide cohort study
Authors
Nicolas Nesseler
Alexandre Mansour
Matthieu Schmidt
Marylou Para
Alizée Porto
Pierre-Emmanuel Falcoz
Nicolas Mongardon
Claire Fougerou
James T. Ross
Antoine Beurton
Lucie Gaide-Chevronnay
Pierre-Grégoire Guinot
Guillaume Lebreton
Erwan Flecher
André Vincentelli
Nicolas Massart
ECMOSARS Investigators
SFAR Research Network
Publication date
01-12-2024
Publisher
BioMed Central
Published in
Critical Care / Issue 1/2024
Electronic ISSN: 1364-8535
DOI
https://doi.org/10.1186/s13054-024-04832-3

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