. 2024 Feb 20;28(1):54.

doi: 10.1186/s13054-024-04832-3.

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

Nicolas Nesseler^{1

2

3

4}, Alexandre Mansour^{5

6}, Matthieu Schmidt^{7

8}, Marylou Para^{9

10}, Alizée Porto¹¹, Pierre-Emmanuel Falcoz^{12

13

14}, Nicolas Mongardon^{15

16

17}, Claire Fougerou^{18

19}, James T Ross²⁰, Antoine Beurton^{21

22}, Lucie Gaide-Chevronnay²³, Pierre-Grégoire Guinot²⁴, Guillaume Lebreton^{25

26}, Erwan Flecher²⁷, André Vincentelli^{28

29}, Nicolas Massart³⁰; ECMOSARS Investigators; SFAR Research Network

Collaborators, Affiliations

Collaborators

Olivier Fouquet, Marc Pierrot, Sidney Chocron, Guillaume Flicoteaux, Philippe Mauriat, Alexandre Ouattara, Hadrien Roze, Olivier Huet, Marc-Olivier Fischer, Raphel Bellaïche, Ophélie Constant, Quentin De Roux, L Y André, Arnaud Meffert, Jean-Claude Merle, Lucile Picard, Elena Skripkina, Thierry Folliguet, Antonio Fiore, Nicolas D'ostrevy, Marie-Catherine Morgan, Maxime Nguyen, Nicolas Terzi, Gwenhaël Colin, Olivier Fabre, Arash Astaneh, Justin Issard, Elie Fadel, Dominique Fabre, Julien Guihaire, Iolande Ion, Jean Baptiste Menager, Delphine Mitilian, Olaf Mercier, François Stephan, Jacques Thes, Jerôme Jouan, Thibault Duburcq, Valentin Loobuyck, Mouhammed Moussa, Sabrina Manganiello, Agnes Mugnier, Natacha Rousse, Olivier Desebbe, Jean-Luc Fellahi, Roland Henaine, Matteo Pozzi, Zakaria Riad, Christophe Guervilly, Sami Hraiech, Laurent Papazian, Matthias Castanier, Charles Chanavaz, Cyril Cadoz, Sebastien Gette, Guillaume Louis, Erick Portocarrero, Philippe Gaudard, Kais Brini, Nicolas Bischoff, Antoine Kimmoun, Bruno Levy, Pierre Perez, Alexandre Bourdiol, Yannick Hourmant, Pierre-Joachim Mahé, Bertrand Rozec, Mickaël Vourc'h, Stéphane Aubert, Florian Bazalgette, Claire Roger, Pierre Jaquet, Brice Lortat-Jacob, Pierre Mordant, Patrick Nataf, Juliette Patrier, Sophie Provenchere, Morgan Roué, Romain Sonneville, Alexy Tran-Dinh, Paul-Henri Wicky, Charles Al Zreibi, Bernard Cholley, Yannis Guyonvarch, Sophie Hamada, Claudio Barbanti, Astrid Bertier, Anatole Harrois, Jordi Matiello, Thomas Kerforne, Corentin Lacroix, Nicolas Brechot, Alain Combes, Juliette Chommeloux, Cosimo D'alessandro, Pierre Demondion, Alexandre Demoule, Martin Dres, Guillaume Fadel, Muriel Fartoukh, Guillaume Hekimian, Charles Juvin, Pascal Leprince, David Levy, Charles Edouard Luyt, Thibaut Schoell, Pierre Fillâtre, Nicolas Massart, Maud Jonas, Nicolas Allou, Salvatore Muccio, Dario Di Perna, Vito-Giovanni Ruggieri, Bruno Mourvillier, Amedeo Anselmi, Karl Bounader, Yoann Launey, Thomas Lebouvier, Alessandro Parasido, Florian Reizine, Maxime Esvan, Philippe Seguin, Emmanuel Besnier, Dorothée Carpentier, Thomas Clavier, Anne Olland, Marion Villard, Fanny Bounes, François Labaste, Vincent Minville, Antoine Guillon, Yannick Fedun

Affiliations

¹ Department of Anesthesia and Critical Care, Pontchaillou, University Hospital of Rennes, Rennes, France. nicolas.nesseler@chu-rennes.fr.
² Univ Rennes, CHU Rennes, Inserm, CIC 1414 (Centre d'Investigation Clinique de Rennes), 35000, Rennes, France. nicolas.nesseler@chu-rennes.fr.
³ Univ Rennes, CHU de Rennes, Inra, Inserm, Institut NUMECAN - UMR_A 1341, UMR_S 1241, 35000, Rennes, France. nicolas.nesseler@chu-rennes.fr.
⁴ Hôpital Pontchaillou, Pôle Anesthésie, SAMU, Urgences, Réanimations, Médecine Interne Et Gériatrie (ASUR-MIG), 2 Rue Henri Le Guilloux, 35033, Rennes Cedex 9, France. nicolas.nesseler@chu-rennes.fr.
⁵ Department of Anesthesia and Critical Care, Pontchaillou, University Hospital of Rennes, Rennes, France.
⁶ Univ Rennes, CHU Rennes, Inserm, IRSET, UMR_S 1085, CIC 1414 (Centre d'Investigation Clinique de Rennes), 35000, Rennes, France.
⁷ Sorbonne Université, INSERM, UMRS_1166-ICAN, Institute of Cardiometabolism and Nutrition, 75013, PARIS, France.
⁸ Service de Médecine Intensive-Réanimation, Institut de Cardiologie, APHP Sorbonne Université Hôpital Pitié-Salpêtrière, 75013, Paris, France.
⁹ Department of Cardiovascular Surgery and Transplantation, Bichat Hospital, AP-HP, Paris, France.
¹⁰ Laboratory of Vascular Translational Science, University of Paris, UMR 1148, Paris, France.
¹¹ Department of Cardiac Surgery, Timone Hospital, APHM, 13005, Marseille, France.
¹² INSERM, UMR 1260, Regenerative Nanomedicine (RNM), FMTS, 67000, Strasbourg, France.
¹³ Faculté de Médecine et Pharmacie, Université de Strasbourg, 67000, Strasbourg, France.
¹⁴ Hôpitaux Universitaire de Strasbourg, Service de Chirurgie Thoracique - Nouvel Hôpital Civil, Strasbourg, France.
¹⁵ Service d'anesthésie-Réanimation, DMU CARE, DHU A-TVB, Assistance Publique-Hôpitaux de Paris (AP-HP), Hôpitaux Universitaires Henri Mondor, 94010, Créteil, France.
¹⁶ Faculté de Santé, Univ Paris Est Créteil, 94010, Créteil, France.
¹⁷ U955-IMRB, Equipe 03 « Pharmacologie et Technologies pour les Maladies Cardiovasculaires (PROTECT), Inserm, Univ Paris Est Créteil (UPEC), Ecole Nationale Vétérinaire d'Alfort (EnVA), 94700, Maisons-Alfort, France.
¹⁸ Department of Clinical Pharmacology, University Hospital, Rennes 1 University, 35033, Rennes, France.
¹⁹ Inserm CIC 1414, Clinical Investigation Centre, University Hospital, Rennes 1 University, 35033, Rennes, France.
²⁰ Department of Surgery, University Hospitals Cleveland and Case Western Reserve University, Cleveland, USA.
²¹ Department of Anaesthesia and Critical Care, CHU Bordeaux, Magellan Medico-Surgical Centre, 33000, Bordeaux, France.
²² UMR 1034, Biology of Cardiovascular Diseases, Univ. Bordeaux, INSERM, 33600, Pessac, France.
²³ Department of Anesthesiology and Critical Care Medicine, University Hospital of Grenoble, Grenoble, France.
²⁴ Department of Anesthesiology and Critical Care Medicine, Dijon University Hospital, Dijon, France.
²⁵ Sorbonne Université, INSERM, UMRS_1166-ICAN, Institute of Cardiometabolism and Nutrition, Paris, France.
²⁶ Service de Chirurgie Thoracique et Cardiovasculaire, Institut de Cardiologie, APHP, Sorbonne Université, Hôpital Pitié-Salpêtrière, Paris, France.
²⁷ Department of Thoracic and Cardiovascular Surgery, Signal and Image Treatment Laboratory (LTSI), Pontchaillou University Hospital, University of Rennes 1, Inserm U1099, Rennes, France.
²⁸ Cardiac Surgery, Univ. Lille, CHU Lille, 59000, Lille, France.
²⁹ Univ. Lille, Inserm, CHU Lille, Institut Pasteur de Lille, U1011-EGID, 59000, Lille, France.
³⁰ Intensive Care Unit, Centre Hospitalier Yves Le Foll, Saint-Brieuc, France.

PMID: 38374103
PMCID: PMC10877839
DOI: 10.1186/s13054-024-04832-3

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

Nicolas Nesseler et al. Crit Care. 2024.

. 2024 Feb 20;28(1):54.

doi: 10.1186/s13054-024-04832-3.

Authors

Collaborators

Olivier Fouquet, Marc Pierrot, Sidney Chocron, Guillaume Flicoteaux, Philippe Mauriat, Alexandre Ouattara, Hadrien Roze, Olivier Huet, Marc-Olivier Fischer, Raphel Bellaïche, Ophélie Constant, Quentin De Roux, L Y André, Arnaud Meffert, Jean-Claude Merle, Lucile Picard, Elena Skripkina, Thierry Folliguet, Antonio Fiore, Nicolas D'ostrevy, Marie-Catherine Morgan, Maxime Nguyen, Nicolas Terzi, Gwenhaël Colin, Olivier Fabre, Arash Astaneh, Justin Issard, Elie Fadel, Dominique Fabre, Julien Guihaire, Iolande Ion, Jean Baptiste Menager, Delphine Mitilian, Olaf Mercier, François Stephan, Jacques Thes, Jerôme Jouan, Thibault Duburcq, Valentin Loobuyck, Mouhammed Moussa, Sabrina Manganiello, Agnes Mugnier, Natacha Rousse, Olivier Desebbe, Jean-Luc Fellahi, Roland Henaine, Matteo Pozzi, Zakaria Riad, Christophe Guervilly, Sami Hraiech, Laurent Papazian, Matthias Castanier, Charles Chanavaz, Cyril Cadoz, Sebastien Gette, Guillaume Louis, Erick Portocarrero, Philippe Gaudard, Kais Brini, Nicolas Bischoff, Antoine Kimmoun, Bruno Levy, Pierre Perez, Alexandre Bourdiol, Yannick Hourmant, Pierre-Joachim Mahé, Bertrand Rozec, Mickaël Vourc'h, Stéphane Aubert, Florian Bazalgette, Claire Roger, Pierre Jaquet, Brice Lortat-Jacob, Pierre Mordant, Patrick Nataf, Juliette Patrier, Sophie Provenchere, Morgan Roué, Romain Sonneville, Alexy Tran-Dinh, Paul-Henri Wicky, Charles Al Zreibi, Bernard Cholley, Yannis Guyonvarch, Sophie Hamada, Claudio Barbanti, Astrid Bertier, Anatole Harrois, Jordi Matiello, Thomas Kerforne, Corentin Lacroix, Nicolas Brechot, Alain Combes, Juliette Chommeloux, Cosimo D'alessandro, Pierre Demondion, Alexandre Demoule, Martin Dres, Guillaume Fadel, Muriel Fartoukh, Guillaume Hekimian, Charles Juvin, Pascal Leprince, David Levy, Charles Edouard Luyt, Thibaut Schoell, Pierre Fillâtre, Nicolas Massart, Maud Jonas, Nicolas Allou, Salvatore Muccio, Dario Di Perna, Vito-Giovanni Ruggieri, Bruno Mourvillier, Amedeo Anselmi, Karl Bounader, Yoann Launey, Thomas Lebouvier, Alessandro Parasido, Florian Reizine, Maxime Esvan, Philippe Seguin, Emmanuel Besnier, Dorothée Carpentier, Thomas Clavier, Anne Olland, Marion Villard, Fanny Bounes, François Labaste, Vincent Minville, Antoine Guillon, Yannick Fedun

Affiliations

¹ Department of Anesthesia and Critical Care, Pontchaillou, University Hospital of Rennes, Rennes, France. nicolas.nesseler@chu-rennes.fr.
² Univ Rennes, CHU Rennes, Inserm, CIC 1414 (Centre d'Investigation Clinique de Rennes), 35000, Rennes, France. nicolas.nesseler@chu-rennes.fr.
³ Univ Rennes, CHU de Rennes, Inra, Inserm, Institut NUMECAN - UMR_A 1341, UMR_S 1241, 35000, Rennes, France. nicolas.nesseler@chu-rennes.fr.
⁴ Hôpital Pontchaillou, Pôle Anesthésie, SAMU, Urgences, Réanimations, Médecine Interne Et Gériatrie (ASUR-MIG), 2 Rue Henri Le Guilloux, 35033, Rennes Cedex 9, France. nicolas.nesseler@chu-rennes.fr.
⁵ Department of Anesthesia and Critical Care, Pontchaillou, University Hospital of Rennes, Rennes, France.
⁶ Univ Rennes, CHU Rennes, Inserm, IRSET, UMR_S 1085, CIC 1414 (Centre d'Investigation Clinique de Rennes), 35000, Rennes, France.
⁷ Sorbonne Université, INSERM, UMRS_1166-ICAN, Institute of Cardiometabolism and Nutrition, 75013, PARIS, France.
⁸ Service de Médecine Intensive-Réanimation, Institut de Cardiologie, APHP Sorbonne Université Hôpital Pitié-Salpêtrière, 75013, Paris, France.
⁹ Department of Cardiovascular Surgery and Transplantation, Bichat Hospital, AP-HP, Paris, France.
¹⁰ Laboratory of Vascular Translational Science, University of Paris, UMR 1148, Paris, France.
¹¹ Department of Cardiac Surgery, Timone Hospital, APHM, 13005, Marseille, France.
¹² INSERM, UMR 1260, Regenerative Nanomedicine (RNM), FMTS, 67000, Strasbourg, France.
¹³ Faculté de Médecine et Pharmacie, Université de Strasbourg, 67000, Strasbourg, France.
¹⁴ Hôpitaux Universitaire de Strasbourg, Service de Chirurgie Thoracique - Nouvel Hôpital Civil, Strasbourg, France.
¹⁵ Service d'anesthésie-Réanimation, DMU CARE, DHU A-TVB, Assistance Publique-Hôpitaux de Paris (AP-HP), Hôpitaux Universitaires Henri Mondor, 94010, Créteil, France.
¹⁶ Faculté de Santé, Univ Paris Est Créteil, 94010, Créteil, France.
¹⁷ U955-IMRB, Equipe 03 « Pharmacologie et Technologies pour les Maladies Cardiovasculaires (PROTECT), Inserm, Univ Paris Est Créteil (UPEC), Ecole Nationale Vétérinaire d'Alfort (EnVA), 94700, Maisons-Alfort, France.
¹⁸ Department of Clinical Pharmacology, University Hospital, Rennes 1 University, 35033, Rennes, France.
¹⁹ Inserm CIC 1414, Clinical Investigation Centre, University Hospital, Rennes 1 University, 35033, Rennes, France.
²⁰ Department of Surgery, University Hospitals Cleveland and Case Western Reserve University, Cleveland, USA.
²¹ Department of Anaesthesia and Critical Care, CHU Bordeaux, Magellan Medico-Surgical Centre, 33000, Bordeaux, France.
²² UMR 1034, Biology of Cardiovascular Diseases, Univ. Bordeaux, INSERM, 33600, Pessac, France.
²³ Department of Anesthesiology and Critical Care Medicine, University Hospital of Grenoble, Grenoble, France.
²⁴ Department of Anesthesiology and Critical Care Medicine, Dijon University Hospital, Dijon, France.
²⁵ Sorbonne Université, INSERM, UMRS_1166-ICAN, Institute of Cardiometabolism and Nutrition, Paris, France.
²⁶ Service de Chirurgie Thoracique et Cardiovasculaire, Institut de Cardiologie, APHP, Sorbonne Université, Hôpital Pitié-Salpêtrière, Paris, France.
²⁷ Department of Thoracic and Cardiovascular Surgery, Signal and Image Treatment Laboratory (LTSI), Pontchaillou University Hospital, University of Rennes 1, Inserm U1099, Rennes, France.
²⁸ Cardiac Surgery, Univ. Lille, CHU Lille, 59000, Lille, France.
²⁹ Univ. Lille, Inserm, CHU Lille, Institut Pasteur de Lille, U1011-EGID, 59000, Lille, France.
³⁰ Intensive Care Unit, Centre Hospitalier Yves Le Foll, Saint-Brieuc, France.

PMID: 38374103
PMCID: PMC10877839
DOI: 10.1186/s13054-024-04832-3

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).

Keywords: Bloodstream infections; ECLS; Nosocomial infections; SARS-CoV 2; Ventilator-associated pneumonia.

PubMed Disclaimer

Conflict of interest statement

Nicolas NESSELER declares no competing interests. Alexandre MANSOUR received payments made to his institution from i-SEP for consulting fees, and from LFB, Viatris, Aguettant and Pfizer for lecture fees. Matthieu SCHMIDT received consultancy fees from Getinge, Xenios FMC and Drager. Claire FOUGEROU declares no competing interests. James T. ROSS declares no competing interests. Alizée PORTO declares no competing interests. Marylou PARA declares no competing interests. Pierre-Emmanuel FALCOZ declares no competing interests. Nicolas MONGARDON received consultant fees from Amomed and Baxter. Guillaume LEBRETON reports lecture fees from Livanova and Abiomed. Antoine BEURTON declares no competing interests. Lucie GAIDE-CHEVRONNAY declares no competing interests. Erwan FLECHER declares no competing interests. André VINCENTELLI declares no competing interests. Nicolas MASSART declares no competing interests.

Figures

**Fig. 1**
Flow chart of ECMO patients included in the study

See this image and copyright information in PMC

Cited by

Taste and Smell Disorders: A Critical Look at Olfactory and Gustatory Dysfunction.
Maniaci A, Lechien JR, Vaira LA, La Via L. Maniaci A, et al. Life (Basel). 2024 Feb 26;14(3):301. doi: 10.3390/life14030301. Life (Basel). 2024. PMID: 38541627 Free PMC article.
Which antimicrobial treatment for patients with bloodstream infection during ECMO support?
Massart N, Ortuno S, Vidal C, Henri S, Rozé H, Bouglé A, Manicone F, Bidar F, Assouline B, Masi P, Hraiech S, Nesseler N, de Montmollin E, Luyt CE. Massart N, et al. Eur J Clin Microbiol Infect Dis. 2025 Apr;44(4):905-914. doi: 10.1007/s10096-025-05059-y. Epub 2025 Feb 8. Eur J Clin Microbiol Infect Dis. 2025. PMID: 39920427
Lack of up-to-date studies and data conversion may lead to biased results.
Wang G, Liu F, Xu L, Zhou X. Wang G, et al. Crit Care. 2024 Oct 28;28(1):347. doi: 10.1186/s13054-024-05109-5. Crit Care. 2024. PMID: 39468620 Free PMC article. No abstract available.
Lack of up-to-date studies and data conversion may lead to biased results: a response to Wang et al.
Ait Hssain A, Vahedian-Azimi A, Ibrahim AS, Hassan IF, Azoulay E, Darmon M. Ait Hssain A, et al. Crit Care. 2024 Dec 31;28(1):441. doi: 10.1186/s13054-024-05223-4. Crit Care. 2024. PMID: 39741353 Free PMC article. No abstract available.

References

1. 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;55:1633–1641. doi: 10.1093/cid/cis783. - DOI - PMC - PubMed
1. Grasselli G, Scaravilli V, Bella SD, Biffi S, Bombino M, Patroniti N, et al. Nosocomial infections during extracorporeal membrane oxygenation. Crit Care Med. 2017;45:1726–1733. doi: 10.1097/CCM.0000000000002652. - DOI - PubMed
1. 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;50:449–459. doi: 10.1097/CCM.0000000000005297. - DOI - PMC - PubMed
1. 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;29:530–536. doi: 10.1016/j.cmi.2022.10.023. - DOI - PMC - PubMed
1. 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;47:188–198. doi: 10.1007/s00134-020-06323-9. - DOI - PMC - PubMed

MeSH terms

Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions

Save citation to file

Email citation

Add to Collections

Add to My Bibliography

Your saved search

Create a file for external citation management software

Your RSS Feed

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

Collaborators

Affiliations

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

Authors

Collaborators

Affiliations

Abstract

Conflict of interest statement

Figures

Similar articles

Cited by

References

MeSH terms

Associated data

Grants and funding

LinkOut - more resources

Full Text Sources

Medical

Miscellaneous

Abstract

Conflict of interest statement

Figures

Similar articles

Cited by

References

MeSH terms

Associated data

Related information

Grants and funding

LinkOut - more resources

Full Text Sources

Medical

Miscellaneous