Characteristics and prognosis of bloodstream infection in patients with COVID-19 admitted in the ICU: an ancillary study of the COVID-ICU study
Authors: Massart Nicolas , Maxime Virginie , Fillatre Pierre , Razazi Keyvan , Ferré Alexis , Moine Pierre , Legay Francois , Voiriot Guillaume , Amara Marlene , Santi Francesca , Nseir Saad , Marque-Juillet Stephanie , Bounab Rania , Barbarot Nicolas , Bruneel Fabrice , Luyt Charles-Edouard ,   the COVID ICU Bacteremia Study Group on behalf of the COVID-ICU Investigators, Mercat Alain , Asfar Pierre , Beloncle François , Demiselle Julien , Pham Tài , Pavot Arthur , Monnet Xavier , Richard Christian , Demoule Alexandre , Dres Martin , Mayaux Julien , Beurton Alexandra , Daubin Cédric , Descamps Richard , Joret Aurélie , Du Cheyron Damien , Pene Frédéric , Chiche Jean-Daniel , Jozwiak Mathieu , Jaubert Paul , Voiriot Guillaume , Fartoukh Muriel , Teulier Marion , Blayau Clarisse , Bodenes Laetitia , Ferriere Nicolas , Auchabie Johann , Le Meur Anthony , Pignal Sylvain , Mazzoni Thierry , Quenot Jean-Pierre , Andreu Pascal , Roudau Jean-Baptiste , Labruyère Marie , Nseir Saad , Preau Sébastien , Poissy Julien , Mathieu Daniel , Benhamida Sarah , Paulet Rémi , Roucaud Nicolas , Thyrault Martial , Daviet Florence , Hraiech Sami , Parzy Gabriel , Sylvestre Aude , Jochmans Sébastien , Bouilland Anne-Laure , Monchi Mehran , Déserts Marc Danguy des , Mathais Quentin , Rager Gwendoline , Pasquier Pierre , Reignier Jean , Seguin Amélie , Garret Charlotte , Canet Emmanuel , Dellamonica Jean , Saccheri Clément , Lombardi Romain , Kouchit Yanis , Jacquier Sophie , Mathonnet Armelle , Nay Mai-Ahn , Runge Isabelle , Martino Frédéric , Flurin Laure , Rolle Amélie , Carles Michel , Coudroy Rémi , Thille Arnaud W. , Frat Jean-Pierre , Rodriguez Maeva , Beuret Pascal , Tientcheu Audrey , Vincent Arthur , Michelin Florian , Tamion Fabienne , Carpentier Dorothée , Boyer Déborah , Girault Christophe , Gissot Valérie , Ehrmann Stéphan , Gandonniere Charlotte Salmon , Elaroussi Djlali , Delbove Agathe , Fedun Yannick , Huntzinger Julien , Lebas Eddy , Kisoka Grâce , Grégoire Céline , Marchetta Stella , Lambermont Bernard , Argaud Laurent , Baudry Thomas , Bertrand Pierre-Jean , Dargent Auguste , Guitton Christophe , Chudeau Nicolas , Landais Mickaël , Darreau Cédric , Ferre Alexis , Gros Antoine , Lacave Guillaume , Bruneel Fabrice , Neuville Mathilde , Devaquet Jérôme , Tachon Guillaume , Gallo Richard , Chelha Riad , Galbois Arnaud , Jallot Anne , Lemoine Ludivine Chalumeau , Kuteifan Khaldoun , Pointurier Valentin , Jandeaux Louise-Marie , Mootien Joy , Damoisel Charles , Sztrymf Benjamin , Schmidt Matthieu , Combes Alain , Chommeloux Juliette , Luyt Charles Edouard , Schortgen Frédérique , Rusel Leon , Jung Camille , Gobert Florent , Vimpere Damien , Lamhaut Lionel , Sauneuf Bertrand , Charrrier Liliane , Calus Julien , Desmeules Isabelle , Painvin Benoît , Tadie Jean-Marc , Castelain Vincent , Michard Baptiste , Herbrecht Jean-Etienne , Baldacini Mathieu , Weiss Nicolas , Demeret Sophie , Marois Clémence , Rohaut Benjamin , Moury Pierre-Henri , Savida Anne-Charlotte , Couadau Emmanuel , Série Mathieu , Alexandru Nica , Bruel Cédric , Fontaine Candice , Garrigou Sonia , Mahler Juliette Courtiade , Leclerc Maxime , Ramakers Michel , Garçon Pierre , Massou Nicole , Van Vong Ly , Sen Juliane , Lucas Nolwenn , Chemouni Franck , Stoclin Annabelle , Avenel Alexandre , Faure Henri , Gentilhomme Angélie , Ricome Sylvie , Abraham Paul , Monard Céline , Textoris Julien , Rimmele Thomas , Montini Florent , Lejour Gabriel , Lazard Thierry , Etienney Isabelle , Kerroumi Younes , Dupuis Claire , Bereiziat Marine , Coupez Elisabeth , Thouy François , Hoffmann Clément , Donat Nicolas , Chrisment Anne , Blot Rose-Marie , Kimmoun Antoine , Jacquot Audrey , Mattei Matthieu , Levy Bruno , Ravan Ramin , Dopeux Loïc , Liteaudon Jean-Mathias , Roux Delphine , Rey Brice , Anghel Radu , Schenesse Deborah , Gevrey Vincent , Castanera Jermy , Petua Philippe , Madeux Benjamin , Hartman Otto , Piagnerelli Michael , Joosten Anne , Noel Cinderella , Biston Patrick , Noel Thibaut , Bouar Gurvan L. E. , Boukhanza Messabi , Demarest Elsa , Bajolet Marie-France , Charrier Nathanaël , Quenet Audrey , Zylberfajn Cécile , Dufour Nicolas , Mégarbane Buno , Voicu Sébastian , Deye Nicolas , Malissin Isabelle , Legay François , Debarre Matthieu , Barbarot Nicolas , Fillatre Pierre , Delord Bertrand , Laterrade Thomas , Saghi Tahar , Pujol Wilfried , Cungi Pierre Julien , Esnault Pierre , Cardinale Mickael , Ha Vivien Hong Tuan , Fleury Grégory , Brou Marie-Ange , Zafimahazo Daniel , Tran-Van David , Avargues Patrick , Carenco Lisa , Robin Nicolas , Ouali Alexandre , Houdou Lucie , Le Terrier Christophe , Suh Noémie , Primmaz Steve , Pugin Jérome , Weiss Emmanuel , Gauss Tobias , Moyer Jean-Denis , Burtz Catherine Paugam , La Combe Béatrice , Smonig Rolland , Violleau Jade , Cailliez Pauline , Chelly Jonathan , Marchalot Antoine , Saladin Cécile , Bigot Christelle , Fayolle Pierre-Marie , Fatséas Jules , Ibrahim Amr , Resiere Dabor , Hage Rabih , Cholet Clémentine , Cantier Marie , Trouiler Pierre , Montravers Philippe , Lortat-Jacob Brice , Tanaka Sebastien , Dinh Alexy Tran , Duranteau Jacques , Harrois Anatole , Dubreuil Guillaume , Werner Marie , Godier Anne , Hamada Sophie , Zlotnik Diane , Nougue Hélène , Mekontso-Dessap Armand , Carteaux Guillaume , Razazi Keyvan , De Prost Nicolas , Mongardon Nicolas , Lamraoui Meriam , Alessandri Claire , de Roux Quentin , de Roquetaillade Charles , Chousterman Benjamin G. , Mebazaa Alexandre , Gayat Etienne , Garnier Marc , Pardo Emmanuel , Satre-Buisson Lea , Gutton Christophe , Yvin Elise , Marcault Clémence , Azoulay Elie , Darmon Michael , Oufella Hafid Ait , Hariri Geoffroy , Urbina Tomas , Mazerand Sandie , Heming Nicholas , Santi Francesca , Moine Pierre , Annane Djillali , Bouglé Adrien , Omar Edris , Lancelot Aymeric , Begot Emmanuelle , Plantefeve Gaétan , Contou Damien , Mentec Hervé , Pajot Olivier , Faguer Stanislas , Cointault Olivier , Lavayssiere Laurence , Nogier Marie-Béatrice , Jamme Matthieu , Pichereau Claire , Hayon Jan , Outin Hervé , Dépret François , Coutrot Maxime , Chaussard Maité , Guillemet Lucie , Goffin Pierre , Thouny Romain , Guntz Julien , Jadot Laurent , Persichini Romain , Jean-Michel Vanessa , Georges Hugues , Caulier Thomas , Pradel Gaël , Hausermann Marie-Hélène , Nguyen-Valat Thi My Hue , Boudinaud Michel , Vivier Emmanuel , Rosseli Sylvène , Bourdin Gaël , Pommier Christian , Vinclair Marc , Poignant Simon , Mons Sandrine , Bougouin Wulfran , Bruna Franklin , Maestraggi Quentin , Roth Christian , Bitker Laurent , Dhelft François , Bonnet-Chateau Justine , Filippelli Mathilde , Morichau-Beauchant Tristan , Thierry Stéphane , Le Roy Charlotte , Jouan Mélanie Saint , Goncalves Bruno , Mazeraud Aurélien , Daniel Matthieu , Sharshar Tarek , Cadoz Cyril , Gaci Rostane , Gette Sébastien , Louis Guillaune , Sacleux Sophe-Caroline , Ordan Marie-Amélie , Cravoisy Aurélie , Conrad Marie , Courte Guilhem , Gibot Sébastien , Benzidi Younès , Casella Claudia , Serpin Laurent , Setti Jean-Lou , Besse Marie-Catherine , Bourreau Anna , Pillot Jérôme , Rivera Caroline , Vinclair Camille , Robaux Marie-Aline , Achino Chloé , Delignette Marie-Charlotte , Mazard Tessa , Aubrun Frédéric , Bouchet Bruno , Frérou Aurélien , Muller Laura , Quentin Charlotte , Degoul Samuel , Stihle Xavier , Sumian Claude , Bergero Nicoletta , Lanaspre Bernard , Quintard Hervé , Maiziere Eve Marie , Egreteau Pierre-Yves , Leloup Guillaume , Berteau Florin , Cottrel Marjolaine , Bouteloup Marie , Jeannot Matthieu , Blanc Quentin , Saison Julien , Geneau Isabelle , Grenot Romaric , Ouchike Abdel , Hazera Pascal , Masse Anne-Lyse , Demiri Suela , Vezinet Corinne , Baron Elodie , Benchetrit Deborah , Monsel Antoine , Trebbia Grégoire , Schaack Emmanuelle , Lepecq Raphaël , Bobet Mathieu , Vinsonneau Christophe , Dekeyser Thibault , Delforge Quentin , Rahmani Imen , Vivet Bérengère , Paillot Jonathan , Hierle Lucie , Chaignat Claire , Valette Sarah , Her Benoït , Brunet Jennifier , Page Mathieu , Boiste Fabienne , Collin Anthony , Bavozet Florent , Garin Aude , Dlala Mohamed , Mhamdi Kais , Beilouny Bassem , Lavalard Alexandra , Perez Severine , Veber Benoit , Guitard Pierre-Gildas , Gouin Philippe , Lamacz Anna , Plouvier Fabienne , Delaborde Bertrand P. , Kherchache Aïssa , Chaalal Amina , Ricard Jean-Damien , Amouretti Marc , Freita-Ramos Santiago , Roux Damien , Constantin Jean-Michel , Assefi Mona , Lecore Marine , Selves Agathe , Prevost Florian , Lamer Christian , Shi Ruiying , Knani Lyes , Floury Sébastien Pili , Vettoretti Lucie , Levy Michael , Marsac Lucile , Dauger Stéphane , Guilmin-Crépon Sophie , Winiszewski Hadrien , Piton Gael , Soumagne Thibaud , Capellier Gilles , Putegnat Jean-Baptiste , Bayle Frédérique , Perrou Maya , Thao Ghyslaine , Géri Guillaume , Charron Cyril , Repessé Xavier , Vieillard-Baron Antoine , Guilbart Mathieu , Roger Pierre-Alexandre , Hinard Sébastien , Macq Pierre-Yves , Chaulier Kevin , Goutte Sylvie , Chillet Patrick , Pitta Anaïs , Darjent Barbara , Bruneau Amandine , Lasocki Sigismond , Leger Maxime , Gergaud Soizic , Lemarie Pierre , Terzi Nicolas , Schwebel Carole , Dartevel Anaïs , Galerneau Louis-Marie , Diehl Jean-Luc , Hauw-Berlemont Caroline , Péron Nicolas , Guérot Emmanuel , Amoli Abolfazl Mohebbi , Benhamou Michel , Deyme Jean-Pierre , Andremont Olivier , Lena Diane , Cady Julien , Causeret Arnaud , De La Chapelle Arnaud , Cracco Christophe , Rouleau Stéphane , Schnell David , Foucault Camille , Lory Cécile , Chapelle Thibault , Bruckert Vincent , Garcia Julie , Sahraoui Abdlazize , Abbosh Nathalie , Bornstain Caroline , Pernet Pierre , Poirson Florent , Pasem Ahmed , Karoubi Philippe , Poupinel Virginie , Gauthier Caroline , Bouniol François , Feuchere Philippe , Heron Anne , Carreira Serge , Emery Malo , Le Floch Anne Sophie , Giovannangeli Luana , Herzog Nicolas , Giacardi Christophe , Baudic Thibaut , Thill Chloé , Lebbah Said , Palmyre Jessica , Tubach Florence , Hajage David , Bonnet Nicolas , Ebstein Nathan , Gaudry Stéphane , Cohen Yves , Noublanche Julie , Lesieur Olivier , Sément Arnaud , Roca-Cerezo Isabel , Pascal Michel , Sma Nesrine , Colin Gwenhaël , Lacherade Jean-Claude , Bionz Gauthier , Maquigneau Natacha , Bouzat Pierre , Durand Michel , Hérault Marie-Christine , Payen Jean-Francois 
Published: December 2021

Abstract
Background
Patients infected with the severe acute respiratory syndrome coronavirus 2 (SARS-COV 2) and requiring intensive care unit (ICU) have a high incidence of hospital-acquired infections; however, data regarding hospital acquired bloodstream infections (BSI) are scarce. We aimed to investigate risk factors and outcome of BSI in critically ill coronavirus infectious disease-19 (COVID-19) patients.

Patients and methods
We performed an ancillary analysis of a multicenter prospective international cohort study (COVID-ICU study) that included 4010 COVID-19 ICU patients. For the present analysis, only those with data regarding primary outcome (death within 90 days from admission) or BSI status were included. Risk factors for BSI were analyzed using Fine and Gray competing risk model. Then, for outcome comparison, 537 BSI-patients were matched with 537 controls using propensity score matching.

Results
Among 4010 included patients, 780 (19.5%) acquired a total of 1066 BSI (10.3 BSI per 1000 patients days at risk) of whom 92% were acquired in the ICU. Higher SAPS II, male gender, longer time from hospital to ICU admission and antiviral drug before admission were independently associated with an increased risk of BSI, and interestingly, this risk decreased over time. BSI was independently associated with a shorter time to death in the overall population (adjusted hazard ratio (aHR) 1.28, 95% CI 1.05–1.56) and, in the propensity score matched data set, patients with BSI had a higher mortality rate (39% vs 33% p = 0.036). BSI accounted for 3.6% of the death of the overall population.

Conclusion
COVID-19 ICU patients have a high risk of BSI, especially early after ICU admission, risk that increases with severity but not with corticosteroids use. BSI is associated with an increased mortality rate.