Multicenter Study

. 2021 Feb;47(2):188-198.

doi: 10.1007/s00134-020-06323-9. Epub 2021 Jan 3.

Relationship between SARS-CoV-2 infection and the incidence of ventilator-associated lower respiratory tract infections: a European multicenter cohort study

Anahita Rouzé^{1

2}, Ignacio Martin-Loeches^{3

4}, Pedro Povoa^{5

6}, Demosthenes Makris⁷, Antonio Artigas⁸, Mathilde Bouchereau¹, Fabien Lambiotte⁹, Matthieu Metzelard¹⁰, Pierre Cuchet¹¹, Claire Boulle Geronimi¹², Marie Labruyere¹³, Fabienne Tamion¹⁴, Martine Nyunga¹⁵, Charles-Edouard Luyt¹⁶, Julien Labreuche¹⁷, Olivier Pouly¹⁸, Justine Bardin¹⁹, Anastasia Saade²⁰, Pierre Asfar²¹, Jean-Luc Baudel²², Alexandra Beurton²³, Denis Garot²⁴, Iliana Ioannidou²⁵, Louis Kreitmann²⁶, Jean-François Llitjos²⁷, Eleni Magira²⁸, Bruno Mégarbane²⁹, David Meguerditchian³⁰, Edgar Moglia³¹, Armand Mekontso-Dessap³², Jean Reignier³³, Matthieu Turpin³⁴, Alexandre Pierre³⁵, Gaetan Plantefeve³⁶, Christophe Vinsonneau³⁷, Pierre-Edouard Floch³⁸, Nicolas Weiss³⁹, Adrian Ceccato⁴⁰, Antoni Torres⁴¹, Alain Duhamel¹⁷, Saad Nseir^{42

43}; coVAPid study Group

Collaborators, Affiliations

Collaborators

coVAPid study Group:
Raphaël Favory, Sébastien Preau, Mercé Jourdain, Julien Poissy, Chaouki Bouras, Piehr Saint Leger, Hanane Fodil, François Aptel, Thierry Van Der Linden, Arnaud W Thille, Elie Azoulay, Frédéric Pène, Keyvan Razazi, François Bagate, Damien Contou, Guillaume Voiriot, Didier Thevenin, Bertrand Guidet, Loïc Le Guennec, Achille Kouatchet, Stephan Ehrmann, Guillaume Brunin, Elise Morawiec, Alexandre Boyer, Laurent Argaud, Sebastian Voicu, Ania Nieszkowska, Benjamin Kowalski, Gemma Goma, Emilio Diaz, Luis Morales, Vassiliki Tsolaki, George Gtavriilidis, Spyros D Mentzelopoulos, David Nora, Sean Boyd, Luis Coelho, Julien Maizel, Damien Du Cheyron, Mehdi Imouloudene, Jean-Pierre Quenot, Arnaud Guilbert, Catia Cilloniz

Affiliations

¹ CHU de Lille, Médecine Intensive-Réanimation, 59000, Lille, France.
² Université de Lille, INSERM U995, Team Fungal Associated Invasive and Inflammatory Diseases, Lille Inflammation Research International Center, Lille, France.
³ Department of Intensive Care Medicine, Multidisciplinary Intensive Care Research Organization (MICRO), St. James's Hospital, St. James Street, Dublin 8, Dublin, Eire, Ireland.
⁴ Hospital Clinic, IDIBAPS, Universided de Barcelona, CIBERes, Barcelona, Spain.
⁵ Polyvalent Intensive Care Unit, São Francisco Xavier Hospital, Centro Hospitalar de Lisboa Ocidental, and NOVA Medical School, CHRC, New University of Lisbon, Lisbon, Portugal.
⁶ Center for Clinical Epidemiology and Research Unit of Clinical Epidemiology, OUH Odense University Hospital, Odense, Denmark.
⁷ Intensive Care Unit, University Hospital of Larissa, University of Thessaly, Biopolis Larissa, 41110, Vólos, Greece.
⁸ Critical Care Center, Corporacion Sanitaria Universitaria Parc Tauli, CIBER Enfermedades Respiratorias, Autonomous University of Barcelona, Parc Tauli 1, 08028, Sabadell, Spain.
⁹ Service de Réanimation Polyvalente, Centre Hospitalier de Valenciennes, Valenciennes, France.
¹⁰ Medical ICU, Amiens University Hospital, Amiens, France.
¹¹ Department of Medical Intensive Care, Caen University Hospital, 14000, Caen, France.
¹² Service de Réanimation et de Soins Intensifs, Centre Hospitalier de Douai, Route de Cambrai, Douai, France.
¹³ Department of Intensive Care, François Mitterrand University Hospital, Dijon, France.
¹⁴ Medical Intensive Care Unit, Rouen University Hospital, Normandie Université, UNIROUEN, Inserm U1096, FHU-REMOD-VHF, 76000, Rouen, France.
¹⁵ ICU, Roubaix Hospital, Roubaix, France.
¹⁶ Service de Médecine Intensive Réanimation, Institut de Cardiologie, Hôpital Pitié-Salpêtrière, Assistance Publique-Hôpitaux de Paris (APHP), Sorbonne Université, 47-83, Boulevard de l'Hôpital, 75651, Paris Cedex 13, France.
¹⁷ Univ. Lille, CHU Lille, ULR 2694-METRICS: Évaluation des Technologies de santé et des Pratiques Médicales, 59000, Lille, France.
¹⁸ Médecine Intensive Réanimation, Hôpital Saint Philibert GHICL, Université Catholique, Lille, France.
¹⁹ CHU de Poitiers, Médecine Intensive Réanimation, CIC 1402 ALIVE, Université de Poitiers, Poitiers, France.
²⁰ Service de Médecine Intensive et Réanimation, Hôpital Saint-Louis, 1 Avenue Claude Vellefaux, 75010, Paris, France.
²¹ Département de Médecine Intensive-Réanimation, CHU d'Angers, Université d'Angers, 4 rue Larrey, 49933, Angers Cedex 9, France.
²² Service de Médecine Intensive Réanimation, AP-HP, Hôpital Saint-Antoine, Assistance Publique-Hôpitaux de Paris, 184 rue du Faubourg Saint-Antoine, Paris, 75571, Cedex 12, France.
²³ Service de Pneumologie, Médecine Intensive, Réanimation (Département "R3S"), AP-HP, Sorbonne Université, Groupe Hospitalier Universitaire Pitié-Salpêtrière Charles Foix, 75013, Paris, France.
²⁴ Service de Médecine Intensive Réanimation, CHU de Tours, Hôpital Bretonneau, 2 Bd Tonnellé, 37000, Tours, France.
²⁵ 1st Department of Pulmonary Medicine and Intensive Care Unit, "Sotiria" Chest Hospital, National and Kapodistrian University of Athens, Athens, Greece.
²⁶ Service de Médecine Intensive, Réanimation, Hospices Civils de Lyon, Hôpital Edouard Herriot, 5, place d'Arsonval, 69437, Lyon Cedex 03, France.
²⁷ Medical Intensive Care Unit, Cochin Hospital, AP-HP, Centre, Université de Paris, Paris, France.
²⁸ 1st Department of Intensive Care Medicine, Evaggelismos Hospital, National and Kapodistrian University of Athens Medical School, Athens, Greece.
²⁹ Réanimation Médicale et Toxicologique, Hôpital Lariboisière, Université de Paris, INSERM UMRS-1144, Paris, France.
³⁰ Intensive Care Unit, Pellegrin-Tripode Hospital, University Hospital of Bordeaux, Bordeaux, France.
³¹ Critical Care Department, Hospital Universitari Parc Taulí, Sabadell, Spain.
³² Assistance Publique-Hôpitaux de Paris, CHU Henri Mondor, Service de réanimation médicale, Créteil, France.
³³ Service de Médecine Intensive Réanimation, CHU de Nantes, Nantes, France.
³⁴ Sorbonne Université, Assistance Publique-Hôpitaux de Paris, Service de Médecine Intensive Réanimation, Hôpital Tenon, Paris, France.
³⁵ Réanimation polyvalente, CH Lens, Lens, France.
³⁶ Réanimation Polyvalente, CH Victor Dupouy, Argenteuil, France.
³⁷ Intensive Care Unit, Hôpital de Béthune, 62408, Béthune, France.
³⁸ Service de Réanimation, Hôpital Duchenne, Rue Monod, 62200, Boulogne-sur-Mer, France.
³⁹ Sorbonne Université, AP-HP, Hôpital de la Pitié-Salpêtrière, Département de Neurologie, Unité de Médecine Intensive Réanimation Neurologique, Paris, France.
⁴⁰ Intensive Care Unit, Hospital Universitari Sagrat Cor, and Ciber de Enfermedades Respiratorias (Ciberes, CB06/06/0028)-Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain.
⁴¹ Department of Pulmonology, Hospital Clinic Barcelona, University of Barcelona, IDIBAPS, CIBERES, ICREA, Barcelona, Spain.
⁴² CHU de Lille, Médecine Intensive-Réanimation, 59000, Lille, France. s-nseir@chru-lille.fr.
⁴³ Université de Lille, INSERM U995, Team Fungal Associated Invasive and Inflammatory Diseases, Lille Inflammation Research International Center, Lille, France. s-nseir@chru-lille.fr.

PMID: 33388794
PMCID: PMC7778569
DOI: 10.1007/s00134-020-06323-9

Multicenter Study

Relationship between SARS-CoV-2 infection and the incidence of ventilator-associated lower respiratory tract infections: a European multicenter cohort study

Anahita Rouzé et al. Intensive Care Med. 2021 Feb.

. 2021 Feb;47(2):188-198.

doi: 10.1007/s00134-020-06323-9. Epub 2021 Jan 3.

Authors

Collaborators

coVAPid study Group:
Raphaël Favory, Sébastien Preau, Mercé Jourdain, Julien Poissy, Chaouki Bouras, Piehr Saint Leger, Hanane Fodil, François Aptel, Thierry Van Der Linden, Arnaud W Thille, Elie Azoulay, Frédéric Pène, Keyvan Razazi, François Bagate, Damien Contou, Guillaume Voiriot, Didier Thevenin, Bertrand Guidet, Loïc Le Guennec, Achille Kouatchet, Stephan Ehrmann, Guillaume Brunin, Elise Morawiec, Alexandre Boyer, Laurent Argaud, Sebastian Voicu, Ania Nieszkowska, Benjamin Kowalski, Gemma Goma, Emilio Diaz, Luis Morales, Vassiliki Tsolaki, George Gtavriilidis, Spyros D Mentzelopoulos, David Nora, Sean Boyd, Luis Coelho, Julien Maizel, Damien Du Cheyron, Mehdi Imouloudene, Jean-Pierre Quenot, Arnaud Guilbert, Catia Cilloniz

Affiliations

¹ CHU de Lille, Médecine Intensive-Réanimation, 59000, Lille, France.
² Université de Lille, INSERM U995, Team Fungal Associated Invasive and Inflammatory Diseases, Lille Inflammation Research International Center, Lille, France.
³ Department of Intensive Care Medicine, Multidisciplinary Intensive Care Research Organization (MICRO), St. James's Hospital, St. James Street, Dublin 8, Dublin, Eire, Ireland.
⁴ Hospital Clinic, IDIBAPS, Universided de Barcelona, CIBERes, Barcelona, Spain.
⁵ Polyvalent Intensive Care Unit, São Francisco Xavier Hospital, Centro Hospitalar de Lisboa Ocidental, and NOVA Medical School, CHRC, New University of Lisbon, Lisbon, Portugal.
⁶ Center for Clinical Epidemiology and Research Unit of Clinical Epidemiology, OUH Odense University Hospital, Odense, Denmark.
⁷ Intensive Care Unit, University Hospital of Larissa, University of Thessaly, Biopolis Larissa, 41110, Vólos, Greece.
⁸ Critical Care Center, Corporacion Sanitaria Universitaria Parc Tauli, CIBER Enfermedades Respiratorias, Autonomous University of Barcelona, Parc Tauli 1, 08028, Sabadell, Spain.
⁹ Service de Réanimation Polyvalente, Centre Hospitalier de Valenciennes, Valenciennes, France.
¹⁰ Medical ICU, Amiens University Hospital, Amiens, France.
¹¹ Department of Medical Intensive Care, Caen University Hospital, 14000, Caen, France.
¹² Service de Réanimation et de Soins Intensifs, Centre Hospitalier de Douai, Route de Cambrai, Douai, France.
¹³ Department of Intensive Care, François Mitterrand University Hospital, Dijon, France.
¹⁴ Medical Intensive Care Unit, Rouen University Hospital, Normandie Université, UNIROUEN, Inserm U1096, FHU-REMOD-VHF, 76000, Rouen, France.
¹⁵ ICU, Roubaix Hospital, Roubaix, France.
¹⁶ Service de Médecine Intensive Réanimation, Institut de Cardiologie, Hôpital Pitié-Salpêtrière, Assistance Publique-Hôpitaux de Paris (APHP), Sorbonne Université, 47-83, Boulevard de l'Hôpital, 75651, Paris Cedex 13, France.
¹⁷ Univ. Lille, CHU Lille, ULR 2694-METRICS: Évaluation des Technologies de santé et des Pratiques Médicales, 59000, Lille, France.
¹⁸ Médecine Intensive Réanimation, Hôpital Saint Philibert GHICL, Université Catholique, Lille, France.
¹⁹ CHU de Poitiers, Médecine Intensive Réanimation, CIC 1402 ALIVE, Université de Poitiers, Poitiers, France.
²⁰ Service de Médecine Intensive et Réanimation, Hôpital Saint-Louis, 1 Avenue Claude Vellefaux, 75010, Paris, France.
²¹ Département de Médecine Intensive-Réanimation, CHU d'Angers, Université d'Angers, 4 rue Larrey, 49933, Angers Cedex 9, France.
²² Service de Médecine Intensive Réanimation, AP-HP, Hôpital Saint-Antoine, Assistance Publique-Hôpitaux de Paris, 184 rue du Faubourg Saint-Antoine, Paris, 75571, Cedex 12, France.
²³ Service de Pneumologie, Médecine Intensive, Réanimation (Département "R3S"), AP-HP, Sorbonne Université, Groupe Hospitalier Universitaire Pitié-Salpêtrière Charles Foix, 75013, Paris, France.
²⁴ Service de Médecine Intensive Réanimation, CHU de Tours, Hôpital Bretonneau, 2 Bd Tonnellé, 37000, Tours, France.
²⁵ 1st Department of Pulmonary Medicine and Intensive Care Unit, "Sotiria" Chest Hospital, National and Kapodistrian University of Athens, Athens, Greece.
²⁶ Service de Médecine Intensive, Réanimation, Hospices Civils de Lyon, Hôpital Edouard Herriot, 5, place d'Arsonval, 69437, Lyon Cedex 03, France.
²⁷ Medical Intensive Care Unit, Cochin Hospital, AP-HP, Centre, Université de Paris, Paris, France.
²⁸ 1st Department of Intensive Care Medicine, Evaggelismos Hospital, National and Kapodistrian University of Athens Medical School, Athens, Greece.
²⁹ Réanimation Médicale et Toxicologique, Hôpital Lariboisière, Université de Paris, INSERM UMRS-1144, Paris, France.
³⁰ Intensive Care Unit, Pellegrin-Tripode Hospital, University Hospital of Bordeaux, Bordeaux, France.
³¹ Critical Care Department, Hospital Universitari Parc Taulí, Sabadell, Spain.
³² Assistance Publique-Hôpitaux de Paris, CHU Henri Mondor, Service de réanimation médicale, Créteil, France.
³³ Service de Médecine Intensive Réanimation, CHU de Nantes, Nantes, France.
³⁴ Sorbonne Université, Assistance Publique-Hôpitaux de Paris, Service de Médecine Intensive Réanimation, Hôpital Tenon, Paris, France.
³⁵ Réanimation polyvalente, CH Lens, Lens, France.
³⁶ Réanimation Polyvalente, CH Victor Dupouy, Argenteuil, France.
³⁷ Intensive Care Unit, Hôpital de Béthune, 62408, Béthune, France.
³⁸ Service de Réanimation, Hôpital Duchenne, Rue Monod, 62200, Boulogne-sur-Mer, France.
³⁹ Sorbonne Université, AP-HP, Hôpital de la Pitié-Salpêtrière, Département de Neurologie, Unité de Médecine Intensive Réanimation Neurologique, Paris, France.
⁴⁰ Intensive Care Unit, Hospital Universitari Sagrat Cor, and Ciber de Enfermedades Respiratorias (Ciberes, CB06/06/0028)-Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain.
⁴¹ Department of Pulmonology, Hospital Clinic Barcelona, University of Barcelona, IDIBAPS, CIBERES, ICREA, Barcelona, Spain.
⁴² CHU de Lille, Médecine Intensive-Réanimation, 59000, Lille, France. s-nseir@chru-lille.fr.
⁴³ Université de Lille, INSERM U995, Team Fungal Associated Invasive and Inflammatory Diseases, Lille Inflammation Research International Center, Lille, France. s-nseir@chru-lille.fr.

PMID: 33388794
PMCID: PMC7778569
DOI: 10.1007/s00134-020-06323-9

Erratum in

Correction to: Relationship between SARS-CoV-2 infection and the incidence of ventilator-associated lower respiratory tract infections: a European multicenter cohort study.
Rouzé A, Martin-Loeches I, Povoa P, Makris D, Artigas A, Bouchereau M, Lambiotte F, Metzelard M, Cuchet P, Boulle Geronimi C, Labruyere M, Tamion F, Nyunga M, Luyt CE, Labreuche J, Pouly O, Bardin J, Saade A, Asfar P, Baudel JL, Beurton A, Garot D, Ioannidou I, Kreitmann L, Llitjos JF, Magira E, Mégarbane B, Meguerditchian D, Moglia E, Mekontso-Dessap A, Reignier J, Turpin M, Pierre A, Plantefeve G, Vinsonneau C, Floch PE, Weiss N, Ceccato A, Torres A, Duhamel A, Nseir S; coVAPid study Group. Rouzé A, et al. Intensive Care Med. 2022 Apr;48(4):514-515. doi: 10.1007/s00134-021-06588-8. Intensive Care Med. 2022. PMID: 34817634 Free PMC article. No abstract available.

Abstract

Purpose: Although patients with SARS-CoV-2 infection have several risk factors for ventilator-associated lower respiratory tract infections (VA-LRTI), the reported incidence of hospital-acquired infections is low. We aimed to determine the relationship between SARS-CoV-2 pneumonia, as compared to influenza pneumonia or no viral infection, and the incidence of VA-LRTI.

Methods: Multicenter retrospective European cohort performed in 36 ICUs. All adult patients receiving invasive mechanical ventilation > 48 h were eligible if they had: SARS-CoV-2 pneumonia, influenza pneumonia, or no viral infection at ICU admission. VA-LRTI, including ventilator-associated tracheobronchitis (VAT) and ventilator-associated pneumonia (VAP), were diagnosed using clinical, radiological and quantitative microbiological criteria. All VA-LRTI were prospectively identified, and chest-X rays were analyzed by at least two physicians. Cumulative incidence of first episodes of VA-LRTI was estimated using the Kalbfleisch and Prentice method, and compared using Fine-and Gray models.

Results: 1576 patients were included (568 in SARS-CoV-2, 482 in influenza, and 526 in no viral infection groups). VA-LRTI incidence was significantly higher in SARS-CoV-2 patients (287, 50.5%), as compared to influenza patients (146, 30.3%, adjusted sub hazard ratio (sHR) 1.60 (95% confidence interval (CI) 1.26 to 2.04)) or patients with no viral infection (133, 25.3%, adjusted sHR 1.7 (95% CI 1.2 to 2.39)). Gram-negative bacilli were responsible for a large proportion (82% to 89.7%) of VA-LRTI, mainly Pseudomonas aeruginosa, Enterobacter spp., and Klebsiella spp.

Conclusions: The incidence of VA-LRTI is significantly higher in patients with SARS-CoV-2 infection, as compared to patients with influenza pneumonia, or no viral infection after statistical adjustment, but residual confounding may still play a role in the effect estimates.

Keywords: COVID-19; Critical illness; SARS-CoV-2; Ventilator-associated pneumonia; Ventilator-associated tracheobronchitis.

PubMed Disclaimer

Conflict of interest statement

AR received personal fees from MaatPharma, IML received personal fees from MSD, and Gilead. AA received personal fees from Lilly Foundation, and grants from Grifols and Fischer & Paykel. CEL received personal fees from Bayer, Merck, Aerogen, Biomérieux, ThermoFischer Brahms, and Carmat. NW received personal fees from MedDay pharmaceuticals. SN received personal fees from MSD, Bio Rad, BioMérieux, Gilead, and Pfizer. All other authors declare no competing interests.

Figures

**Fig. 1**
The 28-day cumulative incidence of ventilator-associated lower respiratory tract infections. Cumulative incidence estimated using Kalbfleish and Prentice method, considering extubation (dead or alive) within 28 days as competing event. *VA-LRTI* ventilator-associated respiratory tract infection, MV mechanical ventilation

See this image and copyright information in PMC

References

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1. Lewnard JA, Liu VX, Jackson ML, et al. Incidence, clinical outcomes, and transmission dynamics of severe coronavirus disease 2019 in California and Washington: prospective cohort study. BMJ. 2020 doi: 10.1136/BMJ.M1923. - DOI - PMC - PubMed
1. Docherty AB, Harrison EM, Green CA, et al. Features of 20 133 UK patients in hospital with covid-19 using the ISARIC WHO Clinical Characterisation Protocol: prospective observational cohort study. BMJ. 2020 doi: 10.1136/BMJ.M1985. - DOI - PMC - PubMed
1. Martin-Loeches I, Povoa P, Rodríguez A, et al. Incidence and prognosis of ventilator-associated tracheobronchitis (TAVeM): a multicentre, prospective, observational study. Lancet Respir Med. 2015;3:859–868. doi: 10.1016/S2213-2600(15)00326-4. - DOI - PubMed
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Relationship between SARS-CoV-2 infection and the incidence of ventilator-associated lower respiratory tract infections: a European multicenter cohort study

Collaborators

Affiliations

Relationship between SARS-CoV-2 infection and the incidence of ventilator-associated lower respiratory tract infections: a European multicenter cohort study

Authors

Collaborators

Affiliations

Erratum in

Abstract

Conflict of interest statement

Figures

References

Publication types

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources

Other Literature Sources

Medical

Miscellaneous