Different epidemiology of bloodstream infections in COVID-19 compared to non-COVID-19 critically ill patients: a descriptive analysis of the Eurobact II study

doi:10.1186/s13054-022-04166-y

Observational Study

. 2022 Oct 18;26(1):319.

doi: 10.1186/s13054-022-04166-y.

Different epidemiology of bloodstream infections in COVID-19 compared to non-COVID-19 critically ill patients: a descriptive analysis of the Eurobact II study

Niccolò Buetti^{1

2}, Alexis Tabah^{3

4

5}, Ambre Loiodice⁶, Stéphane Ruckly⁶, Abdullah Tarik Aslan⁷, Giorgia Montrucchio^{8

9}, Andrea Cortegiani^{10

11}, Nese Saltoglu¹², Bircan Kayaaslan¹³, Firdevs Aksoy¹⁴, Akova Murat¹⁵, Özlem Akdoğan¹⁶, Kemal Tolga Saracoglu¹⁷, Cem Erdogan¹⁸, Marc Leone¹⁹, Ricard Ferrer²⁰, José-Artur Paiva^{21

22}, Yoshiro Hayashi²³, Mahesh Ramanan^{24

25

26}, Andrew Conway Morris^{27

28

29}, François Barbier^{30

31}, Jean-François Timsit^{32

33}; Eurobact 2 study group

Collaborators, Affiliations

Collaborators

Eurobact 2 study group:
Jeffrey Lipman, Edward Litton, Anna Maria Palermo, Timothy Yap, Ege Eroglu, Koji Hosokawa, Hideki Yoshida, Shigeki Fujitani, Farid Zand, Ata Mahmoodpoor, Seyed Mohammad Nasirodin Tabatabaei, Omar Elrabi, Ghaleb A Almekhlafi, Gabriela Vidal, Marta Aparicio, Irene Alonzo, Silvio A Namendys-Silva, Mariana Hermosillo, Roberto Alejandro Castillo, Liesbet De Bus, Jan De Waele, Isabelle Hollevoet, Nicolas De Schryver, Nicolas Serck, Pedja Kovacevic, Biljana Zlojutro, Etienne Ruppe, Philippe Montravers, Thierry Dulac, Jérémy Castanera, Alexandre Massri, Charlotte Guesdon, Pierre Garcon, Matthieu Duprey, François Philippart, Marc Tran, Cédric Bruel, Pierre Kalfon, Gaëtan Badre, Sophie Demeret, Loïc Le Guennec, Matteo Bassetti, Daniele Giacobbe, Gabriele Sales, Ivan Daroui, Giovanni Lodi, Mariachiara Ippolito, Davide Bellina, Andrea Di Guardo, Monica Rocco, Silvia Fiorelli, Adam Mikstacki, Mariusz Peichota, Iwona Pietraszek-Grzywaczewska, Pedro Póvoa, Andriy Krystopchuk, Ana Teresa, António Manuel Pereira de Figueiredo, Isabel Botelho, Vasco Costa, Rui Pedro Cunha, Alexey Gritsan, Vladislav Belskiy, Mikhail Furman, Maria Martinez, Vanessa Casares, Maria Pilar Gracia Arnillas, Rosana Munoz Bermudez, Alejandro Ubeda, Maria Salgado, Emilio Maseda, Alejandro Suarez De La Rica, Miguel Angel Blasco-Navalpotro, Alberto Orejas Gallego, Josef Prazak, J L Pagani, S Abed-Maillard, Arzu Topeli Iskit, Selcuk Mehtap, Solakoğlu Ceyhun, Ayşe Kaya Kalem, Ibrahim Kurt, Murat Telli, Barcin Ozturk, Nurcan Baykam, Ridvan Karaali, Iftihar Koksal, Yeliz Bilir, Seda Guzeldag, Gulden Ersoz, Guliz Evik, Yasar Bayindir, Yasemin Ersoy, Ari Ercole, Ashok Raj, Artemis Zormpa, George Tinaslanidis, Reena Khade, Ashraf Roshdy, Santhana Kannan, Supriya Antrolikar, Nicholas Marsden, Ben Attwood, Jamie Patel, Mohan Gurjar, Carol Dsilva, Jagadish Chandran, Bashir El Sanousi, Elfayadh Saidahmed, Hytham K S Hamid

Affiliations

¹ Infection Control Program and WHO Collaborating Centre on Patient Safety, Geneva University Hospitals and Faculty of Medicine, Rue Gabrielle-Perret-Gentil 4, 1205, Geneva, Switzerland. niccolo.buetti@gmail.com.
² INSERM, IAME, Université Paris-Cité, 75006, Paris, France. niccolo.buetti@gmail.com.
³ Intensive Care Unit, Redcliffe Hospital, Metro North Hospital and Health Services, Brisbane, QLD, Australia.
⁴ Queensland University of Technology, Brisbane, QLD, Australia.
⁵ Faculty of Medicine, University of Queensland, Brisbane, QLD, Australia.
⁶ ICURESEARCH, 26 rue Garibaldi, Fontaine, France.
⁷ Department of Internal Medicine, Hacettepe University, Sihhiye, Ankara, Turkey.
⁸ Department of Surgical Sciences, University of Turin, Turin, Italy.
⁹ Department of Anaesthesia, Critical Care and Emergency, Città Della Salute e Della Scienza Hospital, Turin, Italy.
¹⁰ Department of Surgical Oncological and Oral Science (Di.Chir.On.S.), University of Palermo, Palermo, Italy.
¹¹ Department of Anesthesia, Intensive Care and Emergency, Policlinico Paolo Giaccone, Palermo, Italy.
¹² Department of Infectious Diseases and Clinical Microbiology, Istanbul University-Cerrahpasa, Istanbul, Turkey.
¹³ Department of Infectious Diseases and Clinical Microbiology, Ankara City Hospital, Ankara Yıldırım Beyazıt University, Ankara, Turkey.
¹⁴ Department of Infectious Diseases and Clinical Microbiology, Karadeniz Technical University, Ortahisar, Turkey.
¹⁵ Department of Infectious Diseases and Clinical Microbiology, Hacettepe University, Ankara, Turkey.
¹⁶ Department of Infectious Diseases and Clinical Microbiology, Erol Olçok Research and Training Hospital, Hitit University, Çorum Merkez, Turkey.
¹⁷ Department of Anesthesiology and Reanimation, Kartal Dr. Lütfi Kırdar City Hospital, Kartal, Turkey.
¹⁸ Department of Anesthesiology and Reanimation, Medipol Mega Hospital, Bağcılar, Turkey.
¹⁹ Department of Anesthesiology and Intensive Care Unit, Hospital Nord, Assistance Publique Hôpitaux Universitaires de Marseille, Aix Marseille University, Marseille, France.
²⁰ Intensive Care Department. SODIR Research Group, Vall d'Hebron Institute of Research VHIR, Hospital Universitari Vall d'Hebron, Barcelona, Spain.
²¹ Intensive Care Medicine Department, Centro Hospitalar Universitário São João (CHUSJ), Porto, Portugal.
²² Department of Medicine, Faculty of Medicine, University of Porto (FMUP), Porto, Portugal.
²³ Department of Intensive Care Medicine, Kameda General Hospital, Kamogawa, Japan.
²⁴ Caboolture and The Prince Charles Hospitals, Metro North Hospital and Health Services, Brisbane, QLD, Australia.
²⁵ Critical Care Division, The George Institute for Global Health, University of New South Wales, Sydney, Australia.
²⁶ School of Medicine, University of Queensland, St Lucia, Australia.
²⁷ Division of Anaesthesia, Department of Medicine, University of Cambridge, Cambridge, UK.
²⁸ Division of Immunology, Department of Pathology, University of Cambridge, Cambridge, UK.
²⁹ JVF Intensive Care Unit, Addenbrooke's Hospital, Cambridge, UK.
³⁰ Médecine Intensive Réanimation, Centre Hospitalier Régional d'Orléans, Orléans, France.
³¹ Centre d'Étude des Pathologies Respiratoires (CEPR), INSERM U1100, Université de Tours, Tours, France.
³² INSERM, IAME, Université Paris-Cité, 75006, Paris, France.
³³ Medical and Infectious Diseases Intensive Care Unit, AP-HP, Bichat-Claude Bernard University Hospital, 46 rue Henri Huchard, 75877, Paris Cedex, France.

PMID: 36258239
PMCID: PMC9578203
DOI: 10.1186/s13054-022-04166-y

Observational Study

Different epidemiology of bloodstream infections in COVID-19 compared to non-COVID-19 critically ill patients: a descriptive analysis of the Eurobact II study

Niccolò Buetti et al. Crit Care. 2022.

. 2022 Oct 18;26(1):319.

doi: 10.1186/s13054-022-04166-y.

Authors

Collaborators

Eurobact 2 study group:
Jeffrey Lipman, Edward Litton, Anna Maria Palermo, Timothy Yap, Ege Eroglu, Koji Hosokawa, Hideki Yoshida, Shigeki Fujitani, Farid Zand, Ata Mahmoodpoor, Seyed Mohammad Nasirodin Tabatabaei, Omar Elrabi, Ghaleb A Almekhlafi, Gabriela Vidal, Marta Aparicio, Irene Alonzo, Silvio A Namendys-Silva, Mariana Hermosillo, Roberto Alejandro Castillo, Liesbet De Bus, Jan De Waele, Isabelle Hollevoet, Nicolas De Schryver, Nicolas Serck, Pedja Kovacevic, Biljana Zlojutro, Etienne Ruppe, Philippe Montravers, Thierry Dulac, Jérémy Castanera, Alexandre Massri, Charlotte Guesdon, Pierre Garcon, Matthieu Duprey, François Philippart, Marc Tran, Cédric Bruel, Pierre Kalfon, Gaëtan Badre, Sophie Demeret, Loïc Le Guennec, Matteo Bassetti, Daniele Giacobbe, Gabriele Sales, Ivan Daroui, Giovanni Lodi, Mariachiara Ippolito, Davide Bellina, Andrea Di Guardo, Monica Rocco, Silvia Fiorelli, Adam Mikstacki, Mariusz Peichota, Iwona Pietraszek-Grzywaczewska, Pedro Póvoa, Andriy Krystopchuk, Ana Teresa, António Manuel Pereira de Figueiredo, Isabel Botelho, Vasco Costa, Rui Pedro Cunha, Alexey Gritsan, Vladislav Belskiy, Mikhail Furman, Maria Martinez, Vanessa Casares, Maria Pilar Gracia Arnillas, Rosana Munoz Bermudez, Alejandro Ubeda, Maria Salgado, Emilio Maseda, Alejandro Suarez De La Rica, Miguel Angel Blasco-Navalpotro, Alberto Orejas Gallego, Josef Prazak, J L Pagani, S Abed-Maillard, Arzu Topeli Iskit, Selcuk Mehtap, Solakoğlu Ceyhun, Ayşe Kaya Kalem, Ibrahim Kurt, Murat Telli, Barcin Ozturk, Nurcan Baykam, Ridvan Karaali, Iftihar Koksal, Yeliz Bilir, Seda Guzeldag, Gulden Ersoz, Guliz Evik, Yasar Bayindir, Yasemin Ersoy, Ari Ercole, Ashok Raj, Artemis Zormpa, George Tinaslanidis, Reena Khade, Ashraf Roshdy, Santhana Kannan, Supriya Antrolikar, Nicholas Marsden, Ben Attwood, Jamie Patel, Mohan Gurjar, Carol Dsilva, Jagadish Chandran, Bashir El Sanousi, Elfayadh Saidahmed, Hytham K S Hamid

Affiliations

¹ Infection Control Program and WHO Collaborating Centre on Patient Safety, Geneva University Hospitals and Faculty of Medicine, Rue Gabrielle-Perret-Gentil 4, 1205, Geneva, Switzerland. niccolo.buetti@gmail.com.
² INSERM, IAME, Université Paris-Cité, 75006, Paris, France. niccolo.buetti@gmail.com.
³ Intensive Care Unit, Redcliffe Hospital, Metro North Hospital and Health Services, Brisbane, QLD, Australia.
⁴ Queensland University of Technology, Brisbane, QLD, Australia.
⁵ Faculty of Medicine, University of Queensland, Brisbane, QLD, Australia.
⁶ ICURESEARCH, 26 rue Garibaldi, Fontaine, France.
⁷ Department of Internal Medicine, Hacettepe University, Sihhiye, Ankara, Turkey.
⁸ Department of Surgical Sciences, University of Turin, Turin, Italy.
⁹ Department of Anaesthesia, Critical Care and Emergency, Città Della Salute e Della Scienza Hospital, Turin, Italy.
¹⁰ Department of Surgical Oncological and Oral Science (Di.Chir.On.S.), University of Palermo, Palermo, Italy.
¹¹ Department of Anesthesia, Intensive Care and Emergency, Policlinico Paolo Giaccone, Palermo, Italy.
¹² Department of Infectious Diseases and Clinical Microbiology, Istanbul University-Cerrahpasa, Istanbul, Turkey.
¹³ Department of Infectious Diseases and Clinical Microbiology, Ankara City Hospital, Ankara Yıldırım Beyazıt University, Ankara, Turkey.
¹⁴ Department of Infectious Diseases and Clinical Microbiology, Karadeniz Technical University, Ortahisar, Turkey.
¹⁵ Department of Infectious Diseases and Clinical Microbiology, Hacettepe University, Ankara, Turkey.
¹⁶ Department of Infectious Diseases and Clinical Microbiology, Erol Olçok Research and Training Hospital, Hitit University, Çorum Merkez, Turkey.
¹⁷ Department of Anesthesiology and Reanimation, Kartal Dr. Lütfi Kırdar City Hospital, Kartal, Turkey.
¹⁸ Department of Anesthesiology and Reanimation, Medipol Mega Hospital, Bağcılar, Turkey.
¹⁹ Department of Anesthesiology and Intensive Care Unit, Hospital Nord, Assistance Publique Hôpitaux Universitaires de Marseille, Aix Marseille University, Marseille, France.
²⁰ Intensive Care Department. SODIR Research Group, Vall d'Hebron Institute of Research VHIR, Hospital Universitari Vall d'Hebron, Barcelona, Spain.
²¹ Intensive Care Medicine Department, Centro Hospitalar Universitário São João (CHUSJ), Porto, Portugal.
²² Department of Medicine, Faculty of Medicine, University of Porto (FMUP), Porto, Portugal.
²³ Department of Intensive Care Medicine, Kameda General Hospital, Kamogawa, Japan.
²⁴ Caboolture and The Prince Charles Hospitals, Metro North Hospital and Health Services, Brisbane, QLD, Australia.
²⁵ Critical Care Division, The George Institute for Global Health, University of New South Wales, Sydney, Australia.
²⁶ School of Medicine, University of Queensland, St Lucia, Australia.
²⁷ Division of Anaesthesia, Department of Medicine, University of Cambridge, Cambridge, UK.
²⁸ Division of Immunology, Department of Pathology, University of Cambridge, Cambridge, UK.
²⁹ JVF Intensive Care Unit, Addenbrooke's Hospital, Cambridge, UK.
³⁰ Médecine Intensive Réanimation, Centre Hospitalier Régional d'Orléans, Orléans, France.
³¹ Centre d'Étude des Pathologies Respiratoires (CEPR), INSERM U1100, Université de Tours, Tours, France.
³² INSERM, IAME, Université Paris-Cité, 75006, Paris, France.
³³ Medical and Infectious Diseases Intensive Care Unit, AP-HP, Bichat-Claude Bernard University Hospital, 46 rue Henri Huchard, 75877, Paris Cedex, France.

PMID: 36258239
PMCID: PMC9578203
DOI: 10.1186/s13054-022-04166-y

Abstract

Background: The study aimed to describe the epidemiology and outcomes of hospital-acquired bloodstream infections (HABSIs) between COVID-19 and non-COVID-19 critically ill patients.

Methods: We used data from the Eurobact II study, a prospective observational multicontinental cohort study on HABSI treated in ICU. For the current analysis, we selected centers that included both COVID-19 and non-COVID-19 critically ill patients. We performed descriptive statistics between COVID-19 and non-COVID-19 in terms of patients' characteristics, source of infection and microorganism distribution. We studied the association between COVID-19 status and mortality using multivariable fragility Cox models.

Results: A total of 53 centers from 19 countries over the 5 continents were eligible. Overall, 829 patients (median age 65 years [IQR 55; 74]; male, n = 538 [64.9%]) were treated for a HABSI. Included patients comprised 252 (30.4%) COVID-19 and 577 (69.6%) non-COVID-19 patients. The time interval between hospital admission and HABSI was similar between both groups. Respiratory sources (40.1 vs. 26.0%, p < 0.0001) and primary HABSI (25.4% vs. 17.2%, p = 0.006) were more frequent in COVID-19 patients. COVID-19 patients had more often enterococcal (20.5% vs. 9%) and Acinetobacter spp. (18.8% vs. 13.6%) HABSIs. Bacteremic COVID-19 patients had an increased mortality hazard ratio (HR) versus non-COVID-19 patients (HR 1.91, 95% CI 1.49-2.45).

Conclusions: We showed that the epidemiology of HABSI differed between COVID-19 and non-COVID-19 patients. Enterococcal HABSI predominated in COVID-19 patients. COVID-19 patients with HABSI had elevated risk of mortality. Trial registration ClinicalTrials.org number NCT03937245 . Registered 3 May 2019.

Keywords: Bacteremia; Bloodstream infection; COVID-19; Enterococcus; ICU-acquired.

PubMed Disclaimer

Conflict of interest statement

The authors have disclosed that they do not have conflict of interest. Dr. Buetti received a grant from the Swiss National Science Foundation (Grant Number: P4P4PM_194449). Prof. Timsit received fees for lectures to 3M, MSD, Pfizer, and BioMérieux; he received research grants from Astellas, 3M, MSD, and Pfizer; and he participated to advisory boards of 3M, MSD, Bayer Pharma, Nabriva, and Pfizer. Dr. Barbier received consulting and lecture fees from MSD and BioMérieux. Prof. Cortegiani received fees for lectures from Gilead, MSD, Pfizer; and he participated to advisory boards of MSD, Gilead, Pfizer. Dr. Montrucchio received fees for lectures from Gilead, Pfizer, Thermofisher; and she participated to advisory boards of Gilead. Dr. Conway Morris sits on the scientific advisory board of Cambridge Infection Diagnostics. Prof. Akova received grants from Pfizer and Gilead, had lecture fees paid to the institution by Pfizer and Sanofi. Dr. Ramanan acknowledges support from the Metro North Hospital and Health Services Clinician-Researcher Fellowship. Dr. Conway Morris sits on the scientific advisory board of Cambridge Infection Diagnostics. Dr. Conway Morris is supported by a Clinician Scientist Fellowship from the Medical Research Council (MR/V006118/1). Prof. José-Artur Paiva received fees for consulting, advisory boards or lectures from MSD, Pfizer, Astra-Zeneca, Gilead, Jansen, Cepheid, AOP Orphan Pharmaceuticals.

Figures

**Fig. 2**
Distribution of microorganisms between COVID-19 and non-COVID-19 patients in all HABSI and in ICU-acquired HABSI. *HA-BSI* hospital-acquired bloodstream infection, *ICU* intensive care unit, *spp.* species

**Fig. 3**
Survival curves for all, ICU-acquired, enterococcal and DTR Gram-negative HABSI. *ICU* intensive care unit, *HA-BSI* hospital-acquired bloodstream infection, *DTR* difficult to treat resistance, Vs versus

See this image and copyright information in PMC

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References

1. Tabah A, Koulenti D, Laupland K, Misset B, Valles J, Bruzzi de Carvalho F, et al. Characteristics and determinants of outcome of hospital-acquired bloodstream infections in intensive care units: the EUROBACT International Cohort Study. Intensive Care Med. 2012;38(12):1930–1945. doi: 10.1007/s00134-012-2695-9. - DOI - PubMed
1. Vincent JL, Sakr Y, Singer M, Martin-Loeches I, Machado FR, Marshall JC, et al. Prevalence and outcomes of infection among patients in intensive care units in 2017. JAMA. 2020;323(15):1478–1487. doi: 10.1001/jama.2020.2717. - DOI - PMC - PubMed
1. Buetti N, Ruckly S, de Montmollin E, Reignier J, Terzi N, Cohen Y, et al. COVID-19 increased the risk of ICU-acquired bloodstream infections: a case-cohort study from the multicentric OUTCOMEREA network. Intensive Care Med. 2021;47(2):180–187. doi: 10.1007/s00134-021-06346-w. - DOI - PMC - PubMed
1. Langford BJ, So M, Leung V, Raybardhan S, Lo J, Kan T, et al. Predictors and microbiology of respiratory and bloodstream bacterial infection in patients with COVID-19: living rapid review update and meta-regression. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis. 2022;28(4):491–501. - PMC - PubMed
1. Ippolito M, Simone B, Filisina C, Catalanotto FR, Catalisano G, Marino C, et al. Bloodstream infections in hospitalized patients with COVID-19: a systematic review and meta-analysis. Microorganisms. 2021;9(10):2016. doi: 10.3390/microorganisms9102016. - DOI - PMC - PubMed

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[1] Tabah A, Koulenti D, Laupland K, Misset B, Valles J, Bruzzi de Carvalho F, et al. Characteristics and determinants of outcome of hospital-acquired bloodstream infections in intensive care units: the EUROBACT International Cohort Study. Intensive Care Med. 2012;38(12):1930–1945. doi: 10.1007/s00134-012-2695-9. - DOI - PubMed

[2] Tabah A, Koulenti D, Laupland K, Misset B, Valles J, Bruzzi de Carvalho F, et al. Characteristics and determinants of outcome of hospital-acquired bloodstream infections in intensive care units: the EUROBACT International Cohort Study. Intensive Care Med. 2012;38(12):1930–1945. doi: 10.1007/s00134-012-2695-9. - DOI - PubMed

[3] Vincent JL, Sakr Y, Singer M, Martin-Loeches I, Machado FR, Marshall JC, et al. Prevalence and outcomes of infection among patients in intensive care units in 2017. JAMA. 2020;323(15):1478–1487. doi: 10.1001/jama.2020.2717. - DOI - PMC - PubMed

[4] Vincent JL, Sakr Y, Singer M, Martin-Loeches I, Machado FR, Marshall JC, et al. Prevalence and outcomes of infection among patients in intensive care units in 2017. JAMA. 2020;323(15):1478–1487. doi: 10.1001/jama.2020.2717. - DOI - PMC - PubMed

[5] Buetti N, Ruckly S, de Montmollin E, Reignier J, Terzi N, Cohen Y, et al. COVID-19 increased the risk of ICU-acquired bloodstream infections: a case-cohort study from the multicentric OUTCOMEREA network. Intensive Care Med. 2021;47(2):180–187. doi: 10.1007/s00134-021-06346-w. - DOI - PMC - PubMed

[6] Buetti N, Ruckly S, de Montmollin E, Reignier J, Terzi N, Cohen Y, et al. COVID-19 increased the risk of ICU-acquired bloodstream infections: a case-cohort study from the multicentric OUTCOMEREA network. Intensive Care Med. 2021;47(2):180–187. doi: 10.1007/s00134-021-06346-w. - DOI - PMC - PubMed

[7] Langford BJ, So M, Leung V, Raybardhan S, Lo J, Kan T, et al. Predictors and microbiology of respiratory and bloodstream bacterial infection in patients with COVID-19: living rapid review update and meta-regression. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis. 2022;28(4):491–501. - PMC - PubMed

[8] Langford BJ, So M, Leung V, Raybardhan S, Lo J, Kan T, et al. Predictors and microbiology of respiratory and bloodstream bacterial infection in patients with COVID-19: living rapid review update and meta-regression. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis. 2022;28(4):491–501. - PMC - PubMed

[9] Ippolito M, Simone B, Filisina C, Catalanotto FR, Catalisano G, Marino C, et al. Bloodstream infections in hospitalized patients with COVID-19: a systematic review and meta-analysis. Microorganisms. 2021;9(10):2016. doi: 10.3390/microorganisms9102016. - DOI - PMC - PubMed

[10] Ippolito M, Simone B, Filisina C, Catalanotto FR, Catalisano G, Marino C, et al. Bloodstream infections in hospitalized patients with COVID-19: a systematic review and meta-analysis. Microorganisms. 2021;9(10):2016. doi: 10.3390/microorganisms9102016. - DOI - PMC - PubMed

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Different epidemiology of bloodstream infections in COVID-19 compared to non-COVID-19 critically ill patients: a descriptive analysis of the Eurobact II study

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Different epidemiology of bloodstream infections in COVID-19 compared to non-COVID-19 critically ill patients: a descriptive analysis of the Eurobact II study

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