Epidemiology and outcomes of hospital-acquired bloodstream infections in intensive care unit patients: the EUROBACT-2 international cohort study

Tabah, Alexis; Buetti, Niccolò; Staiquly, Quentin; Ruckly, Stéphane; Akova, Murat; Aslan, Abdullah Tarik; Leone, Marc; Conway Morris, Andrew; Bassetti, Matteo; Arvaniti, Kostoula; Lipman, Jeffrey; Ferrer, Ricard; Qiu, Haibo; Paiva, José-Artur; Póvoa, Pedro; De Bus, Liesbet; De Waele, Jan; Zand, Farid; Gurjar, Mohan; Alsisi, Adel; Abidi, Khalid; Bracht, Hendrik; Hayashi, Yoshiro; Jeon, Kyeongman; Elhadi, Muhammed; Barbier, François; Timsit, Jean-François

doi:10.1007/s00134-022-06944-2

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Epidemiology and outcomes of hospital-acquired bloodstream infections in intensive care unit patients: the EUROBACT-2 international cohort study

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Author(s): Alexis Tabah ¹ ^, ² ^, ³ ^, ⁴ ^, , Niccolò Buetti ⁵ ^, ⁶ , Quentin Staiquly ⁷ , Stéphane Ruckly ⁶ ^, ⁷ , Murat Akova ⁸ , Abdullah Tarik Aslan ⁹ , Marc Leone ¹⁰ , Andrew Conway Morris ¹¹ ^, ¹² ^, ¹³ , Matteo Bassetti ¹⁴ , Kostoula Arvaniti ¹⁵ , Jeffrey Lipman ⁴ ^, ¹⁶ ^, ¹⁷ , Ricard Ferrer ¹⁸ , Haibo Qiu ¹⁹ , José-Artur Paiva ²⁰ ^, ²¹ ^, ²² , Pedro Povoa ²³ ^, ²⁴ ^, ²⁵ , Liesbet De Bus ²⁶ , Jan De Waele ²⁷ ^, ²⁸ , Farid Zand ²⁹ , Mohan Gurjar ³⁰ , Adel Alsisi ³¹ ^, ³² , Khalid Abidi ³³ , Hendrik Bracht ³⁴ , Yoshiro Hayashi ³⁵ , Kyeongman Jeon ³⁶ , Muhammed Elhadi ³⁷ , François Barbier ³⁸ , Jean-François Timsit ³⁹ ^, ⁴⁰ , on behalf of the EUROBACT-2 Study Group, ESICM, ESCMID ESGCIP and the OUTCOMEREA Network

Publication date (Electronic): 10 February 2023

Journal: Intensive Care Medicine

Publisher: Springer Berlin Heidelberg

Keywords: bloodstream infection, bacteremia, hospital-acquired, antibiotic resistance

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Abstract

Purpose

In the critically ill, hospital-acquired bloodstream infections (HA-BSI) are associated with significant mortality. Granular data are required for optimizing management, and developing guidelines and clinical trials.

Methods

We carried out a prospective international cohort study of adult patients (≥ 18 years of age) with HA-BSI treated in intensive care units (ICUs) between June 2019 and February 2021.

Results

2600 patients from 333 ICUs in 52 countries were included. 78% HA-BSI were ICU-acquired. Median Sequential Organ Failure Assessment (SOFA) score was 8 [IQR 5; 11] at HA-BSI diagnosis. Most frequent sources of infection included pneumonia (26.7%) and intravascular catheters (26.4%). Most frequent pathogens were Gram-negative bacteria (59.0%), predominantly Klebsiella spp. (27.9%), Acinetobacter spp . (20.3%), Escherichia coli (15.8%), and Pseudomonas spp . (14.3%). Carbapenem resistance was present in 37.8%, 84.6%, 7.4%, and 33.2%, respectively. Difficult-to-treat resistance (DTR) was present in 23.5% and pan-drug resistance in 1.5%. Antimicrobial therapy was deemed adequate within 24 h for 51.5%. Antimicrobial resistance was associated with longer delays to adequate antimicrobial therapy. Source control was needed in 52.5% but not achieved in 18.2%. Mortality was 37.1%, and only 16.1% had been discharged alive from hospital by day-28.

Conclusions

HA-BSI was frequently caused by Gram-negative, carbapenem-resistant and DTR pathogens. Antimicrobial resistance led to delays in adequate antimicrobial therapy. Mortality was high, and at day-28 only a minority of the patients were discharged alive from the hospital. Prevention of antimicrobial resistance and focusing on adequate antimicrobial therapy and source control are important to optimize patient management and outcomes.

Supplementary Information

The online version contains supplementary material available at 10.1007/s00134-022-06944-2.

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Most cited references 31

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The Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3).

Mervyn Singer, Clifford S Deutschman, Christopher Warren Seymour … (2016)

Definitions of sepsis and septic shock were last revised in 2001. Considerable advances have since been made into the pathobiology (changes in organ function, morphology, cell biology, biochemistry, immunology, and circulation), management, and epidemiology of sepsis, suggesting the need for reexamination.

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The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies.

Erik von Elm, Douglas G. Altman, Matthias Egger … (2008)

Much of biomedical research is observational. The reporting of such research is often inadequate, which hampers the assessment of its strengths and weaknesses and of a study's generalizability. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Initiative developed recommendations on what should be included in an accurate and complete report of an observational study. We defined the scope of the recommendations to cover three main study designs: cohort, case-control, and cross-sectional studies. We convened a 2-day workshop in September 2004, with methodologists, researchers, and journal editors to draft a checklist of items. This list was subsequently revised during several meetings of the coordinating group and in e-mail discussions with the larger group of STROBE contributors, taking into account empirical evidence and methodological considerations. The workshop and the subsequent iterative process of consultation and revision resulted in a checklist of 22 items (the STROBE Statement) that relate to the title, abstract, introduction, methods, results, and discussion sections of articles. Eighteen items are common to all three study designs and four are specific for cohort, case-control, or cross-sectional studies. A detailed Explanation and Elaboration document is published separately and is freely available on the web sites of PLoS Medicine, Annals of Internal Medicine, and Epidemiology. We hope that the STROBE Statement will contribute to improving the quality of reporting of observational studies.

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Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis

(2022)

Summary Background Antimicrobial resistance (AMR) poses a major threat to human health around the world. Previous publications have estimated the effect of AMR on incidence, deaths, hospital length of stay, and health-care costs for specific pathogen–drug combinations in select locations. To our knowledge, this study presents the most comprehensive estimates of AMR burden to date. Methods We estimated deaths and disability-adjusted life-years (DALYs) attributable to and associated with bacterial AMR for 23 pathogens and 88 pathogen–drug combinations in 204 countries and territories in 2019. We obtained data from systematic literature reviews, hospital systems, surveillance systems, and other sources, covering 471 million individual records or isolates and 7585 study-location-years. We used predictive statistical modelling to produce estimates of AMR burden for all locations, including for locations with no data. Our approach can be divided into five broad components: number of deaths where infection played a role, proportion of infectious deaths attributable to a given infectious syndrome, proportion of infectious syndrome deaths attributable to a given pathogen, the percentage of a given pathogen resistant to an antibiotic of interest, and the excess risk of death or duration of an infection associated with this resistance. Using these components, we estimated disease burden based on two counterfactuals: deaths attributable to AMR (based on an alternative scenario in which all drug-resistant infections were replaced by drug-susceptible infections), and deaths associated with AMR (based on an alternative scenario in which all drug-resistant infections were replaced by no infection). We generated 95% uncertainty intervals (UIs) for final estimates as the 25th and 975th ordered values across 1000 posterior draws, and models were cross-validated for out-of-sample predictive validity. We present final estimates aggregated to the global and regional level. Findings On the basis of our predictive statistical models, there were an estimated 4·95 million (3·62–6·57) deaths associated with bacterial AMR in 2019, including 1·27 million (95% UI 0·911–1·71) deaths attributable to bacterial AMR. At the regional level, we estimated the all-age death rate attributable to resistance to be highest in western sub-Saharan Africa, at 27·3 deaths per 100 000 (20·9–35·3), and lowest in Australasia, at 6·5 deaths (4·3–9·4) per 100 000. Lower respiratory infections accounted for more than 1·5 million deaths associated with resistance in 2019, making it the most burdensome infectious syndrome. The six leading pathogens for deaths associated with resistance (Escherichia coli, followed by Staphylococcus aureus, Klebsiella pneumoniae, Streptococcus pneumoniae, Acinetobacter baumannii, and Pseudomonas aeruginosa) were responsible for 929 000 (660 000–1 270 000) deaths attributable to AMR and 3·57 million (2·62–4·78) deaths associated with AMR in 2019. One pathogen–drug combination, meticillin-resistant S aureus, caused more than 100 000 deaths attributable to AMR in 2019, while six more each caused 50 000–100 000 deaths: multidrug-resistant excluding extensively drug-resistant tuberculosis, third-generation cephalosporin-resistant E coli, carbapenem-resistant A baumannii, fluoroquinolone-resistant E coli, carbapenem-resistant K pneumoniae, and third-generation cephalosporin-resistant K pneumoniae. Interpretation To our knowledge, this study provides the first comprehensive assessment of the global burden of AMR, as well as an evaluation of the availability of data. AMR is a leading cause of death around the world, with the highest burdens in low-resource settings. Understanding the burden of AMR and the leading pathogen–drug combinations contributing to it is crucial to making informed and location-specific policy decisions, particularly about infection prevention and control programmes, access to essential antibiotics, and research and development of new vaccines and antibiotics. There are serious data gaps in many low-income settings, emphasising the need to expand microbiology laboratory capacity and data collection systems to improve our understanding of this important human health threat. Funding Bill & Melinda Gates Foundation, Wellcome Trust, and Department of Health and Social Care using UK aid funding managed by the Fleming Fund.

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Author and article information

Contributors

Alexis Tabah:

ORCID: http://orcid.org/0000-0003-3513-2778

a.tabah@uq.edu.au

Journal

Journal ID (nlm-ta): Intensive Care Med

Journal ID (iso-abbrev): Intensive Care Med

Title: Intensive Care Medicine

Publisher: Springer Berlin Heidelberg (Berlin/Heidelberg )

ISSN (Print): 0342-4642

ISSN (Electronic): 1432-1238

Publication date (Electronic): 10 February 2023

Pages: 1-13

Affiliations

[1 ]GRID grid.490424.f, ISNI 0000000406258387, Intensive Care Unit, , Redcliffe Hospital, ; Brisbane, Australia

[2 ]Queensland Critical Care Research Network (QCCRN), Brisbane, QLD Australia

[3 ]GRID grid.1024.7, ISNI 0000000089150953, Queensland University of Technology, ; Brisbane, QLD Australia

[4 ]GRID grid.1003.2, ISNI 0000 0000 9320 7537, Faculty of Medicine, , The University of Queensland, ; Brisbane, QLD Australia

[5 ]GRID grid.150338.c, ISNI 0000 0001 0721 9812, Infection Control Program and WHO Collaborating Centre on Patient Safety, , Geneva University Hospitals and Faculty of Medicine, ; Geneva, Switzerland

[6 ]GRID grid.512950.a, Université de Paris, INSERM, IAME UMR 1137, ; 75018 Paris, France

[7 ]ICUREsearch, Biometry, 38600 Fontaine, France

[8 ]GRID grid.14442.37, ISNI 0000 0001 2342 7339, Department of Infectious Diseases, , Hacettepe University School of Medicine, ; Ankara, Turkey

[9 ]GRID grid.14442.37, ISNI 0000 0001 2342 7339, Department of Internal Medicine, , Hacettepe University School of Medicine, ; Ankara, Turkey

[10 ]GRID grid.5399.6, ISNI 0000 0001 2176 4817, Department of Anesthesiology and Intensive Care Unit, Hospital Nord, , Aix Marseille University, Assistance Publique Hôpitaux Universitaires de Marseille, ; Marseille, France

[11 ]GRID grid.5335.0, ISNI 0000000121885934, Division of Anaesthesia, Department of Medicine, , University of Cambridge, Addenbrooke’s Hospital, ; Hills Road, Cambridge, CB2 0QQ UK

[12 ]GRID grid.5335.0, ISNI 0000000121885934, Division of Immunology, Department of Pathology, , University of Cambridge, ; Tennis Court Road, Cambridge, Cb2 1QP UK

[13 ]GRID grid.120073.7, ISNI 0000 0004 0622 5016, JVF Intensive Care Unit, , Addenbrooke’s Hospital, Cambridge, ; Hills Road, Cambridge, CB2 0QQ UK

[14 ]GRID grid.410345.7, ISNI 0000 0004 1756 7871, Infectious Diseases Clinic, Department of Health Sciences, , University of Genoa and Ospedale Policlinico San Martino, ; Genoa, Italy

[15 ]Intensive Care Unit, Papageorgiou University Affiliated Hospital, Thessaloníki, Greece

[16 ]GRID grid.121334.6, ISNI 0000 0001 2097 0141, Nimes University Hospital, , University of Montpellier, ; Nimes, France

[17 ]GRID grid.416100.2, ISNI 0000 0001 0688 4634, Jamieson Trauma Institute, , Royal Brisbane and Women’s Hospital, ; Herston, Australia

[18 ]GRID grid.411083.f, ISNI 0000 0001 0675 8654, Intensive Care Department, SODIR-VHIR Research Group, , Vall d’Hebron University Hospital, ; Barcelona, Spain

[19 ]GRID grid.263826.b, ISNI 0000 0004 1761 0489, Jiangsu Provincial Key Laboratory of Critical Care Medicine, Department of Critical Care Medicine, Nanjing Zhongda Hospital, , Southeast University, ; Nanjing, 210009 China

[20 ]GRID grid.414556.7, ISNI 0000 0000 9375 4688, Intensive Care Medicine Department, , Centro Hospitalar Universitário Sao Joao, ; Porto, Portugal

[21 ]GRID grid.5808.5, ISNI 0000 0001 1503 7226, Department of Medicine, Faculty of Medicine, , University of Porto, ; Porto, Portugal

[22 ]Infection and Sepsis ID Group, Porto, Portugal

[23 ]GRID grid.10772.33, ISNI 0000000121511713, NOVA Medical School, , New University of Lisbon, ; Lisbon, Portugal

[24 ]GRID grid.7143.1, ISNI 0000 0004 0512 5013, Center for Clinical Epidemiology and Research Unit of Clinical Epidemiology, , OUH Odense University Hospital, ; Odense, Denmark

[25 ]GRID grid.418335.8, ISNI 0000 0000 9104 7306, Polyvalent Intensive Care Unit, , Hospital de São Francisco Xavier, CHLO, ; Lisbon, Portugal

[26 ]GRID grid.410566.0, ISNI 0000 0004 0626 3303, Department of Critical Care Medicine, , Ghent University Hospital, ; Ghent, Belgium

[27 ]GRID grid.5342.0, ISNI 0000 0001 2069 7798, Department of Internal Medicine and Pediatrics, Faculty of Medicine and Health Sciences, , Ghent University, ; Ghent, Belgium

[28 ]GRID grid.410566.0, ISNI 0000 0004 0626 3303, Department of Intensive Care Medicine, , Ghent University Hospital, ; Ghent, Belgium

[29 ]GRID grid.412571.4, ISNI 0000 0000 8819 4698, Anesthesiology and Critical Care Research Center, , Shiraz University of Medical Sciences, ; Shiraz, Iran

[30 ]GRID grid.263138.d, ISNI 0000 0000 9346 7267, Department of Critical Care Medicine, , Sanjay Gandhi Post Graduate Institute of Medical Sciences (SGPGIMS), ; Lucknow, India

[31 ]ICU Department, Prime Hospital, Dubai, United Arab Emirates

[32 ]GRID grid.7776.1, ISNI 0000 0004 0639 9286, Critical Care Department, Faculty of Medicine, , Cairo University, ; Cairo, Egypt

[33 ]GRID grid.31143.34, ISNI 0000 0001 2168 4024, Medical ICU, Ibn Sina University Hospital, Faculty of Medicine and Pharmacy, , Mohammed V University, ; Rabat, Morocco

[34 ]GRID grid.410712.1, ISNI 0000 0004 0473 882X, Central Interdisciplinary Emergency Medicine, , University Hospital Ulm, ; Ulm, Germany

[35 ]GRID grid.414927.d, ISNI 0000 0004 0378 2140, Department of Intensive Care Medicine, , Kameda General Hospital, ; Kamogawa, Japan

[36 ]GRID grid.264381.a, ISNI 0000 0001 2181 989X, Division of Pulmonary and Critical Care Medicine, Department of Medicine, Samsung Medical Center, , Sungkyunkwan University School of Medicine, ; Seoul, South Korea

[37 ]GRID grid.411306.1, ISNI 0000 0000 8728 1538, Faculty of Medicine, , University of Tripoli, ; Tripoli, Libya

[38 ]GRID grid.413932.e, ISNI 0000 0004 1792 201X, Service de Médecine Intensive-Réanimation, , Centre Hospitalier Régional d’Orléans, ; 14, avenue de L’Hôpital, 45100 Orléans, France

[39 ]GRID grid.512950.a, Université Paris-Cité, INSERM, IAME UMR 1137, ; 75018 Paris, France

[40 ]GRID grid.411119.d, ISNI 0000 0000 8588 831X, Medical and Infectious Diseases Intensive Care Unit, , AP-HP, Bichat-Claude Bernard University Hospital, ; 46 Omdurman maternity hospitalrue Henri Huchard, 75877 Paris Cedex, France

Author information

Alexis Tabah http://orcid.org/0000-0003-3513-2778

Andrew Conway Morris http://orcid.org/0000-0002-3211-3216

Liesbet De Bus https://orcid.org/0000-0003-1456-5857

Jan De Waele http://orcid.org/0000-0003-1017-9748

Mohan Gurjar http://orcid.org/0000-0002-8489-0324

Article

Publisher ID: 6944

DOI: 10.1007/s00134-022-06944-2

PMC ID: 9916499

PubMed ID: 36764959

SO-VID: 51638b5f-a366-4ca4-b160-38c29d0a430d

Copyright © © Springer-Verlag GmbH Germany, part of Springer Nature 2023, Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

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This article is made available via the PMC Open Access Subset for unrestricted research re-use and secondary analysis in any form or by any means with acknowledgement of the original source. These permissions are granted for the duration of the World Health Organization (WHO) declaration of COVID-19 as a global pandemic.

History

Date received : 6 July 2022

Date accepted : 23 November 2022

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100013347, European Society of Intensive Care Medicine;

Funded by: FundRef http://dx.doi.org/10.13039/501100001704, European Society of Clinical Microbiology and Infectious Diseases;

Epidemiology and outcomes of hospital-acquired bloodstream infections in intensive care unit patients: the EUROBACT-2 international cohort study

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Abstract

Purpose

Methods

Results

Conclusions

Supplementary Information

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Preventive and Emergency Medicine Insights

Most cited references 31

The Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3).

The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies.

Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis

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