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.
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Availability of data and material
The datasets used and/or analysed during the current study are available from the OUTCOMEREA organisation on reasonable request.
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Acknowledgements
The EUROBACT-2 study was endorsed by the European Society of Intensive Care Medicine (ESICM), the infection section of the ESCIM and the European Society of Clinical Microbiology and Infectious Diseases (ESCMID) study Group for Infections in Critically Ill Patients (ESGCIP), with scientific input of the OUTCOMEREA network. The members of the Eurobact 2 Study Group are: Alexis Tabah, Hamish Pollock, Ben Margetts, Meredith Young, Neeraj Bhadange, Steven Tyler, Anne Ledtischke, Mackenzie Finnis, Anne Ledtischke, Mackenzie Finnis, Jyotsna Dwivedi, Manoj Saxena, Vishwanath Biradar, Natalie Soar, Vineet Sarode, David Brewster, Adrian Regli, Elizabeth Weeda, Samiul Ahmed, Cheryl Fourie, Kevin Laupland, Mahesh Ramanan, James Walsham, Jason Meyer, Edward Litton, Anna Maria Palermo, Timothy Yap, Ege Eroglu, Antony George Attokaran, C'havala Jaramillo, Khalid Mahmood Khan Nafees, Nurhikmahtul Aqilah Haji Abd Rashid, Haji Adi Muhamad Ibnu Walid, Tomas Mon, P. Dhakshina Moorthi, Shah Sudhirchandra, Dhadappa Damodar Sridharan, Qiu Haibo, Xie Jianfeng, Lu Wei-Hua, Wang Zhen, Chuanyun Qian, Jili Luo, Xiaomei Chen, Hao Wang, Peng Zhao, Juan Zhao, Qiu Wusi, Chen Mingmin, Lei Xu, Chengfen Yin, Ruilan Wang, Jinfeng Wang, Yongjie Yin, Min Zhang, Jilu Ye, Chungfang Hu, Suming Zhou, Min Huang, Jing Yan, Yan Wang, Bingyu Qin, Ling Ye, Xie Weifeng, Li Peije, Nan Geng, Yoshiro Hayashi, Toshiyuki Karumai, Masaki Yamasaki, Satoru Hashimoto, Koji Hosokawa, Jun Makino, Takeo Matsuyoshi, Akira Kuriyama, Hidenobu Shigemitsu, Yuka Mishima, Michio Nagashima, Hideki Yoshida, Shigeki Fujitani, Koichiro Omori, Hiroshi Rinka, Hiroki Saito, Kaori Atobe, Hideaki Kato, Shunsuke Takaki, M. Shahnaz Hasan, Muhamad Fadhil Hadi Jamaluddin, Lee See Pheng, Sheshendrasurian Visvalingam, Mun Thing Liew, Siong Ling Danny Wong, Kean Khang Fong, Hamizah Bt Abdul Rahman, Zuraini Md Noor, Lee Kok Tong, Abd. Hamid Azman, Mohd Zulfakar Mazlan, Saedah Ali, Kyeongman Jeon, Sang-Min Lee, Sunghoon Park, Seung Yong Park, Sung Yoon Lim, Qing Yuan Goh, Shin Yi Ng, Sui An Lie, Andrea Lay Hoon Kwa, Ken Junyang Goh, Andrew Yunkai Li, Caroline Yu Ming Ong, Jia Yan Lim, Jessica Lishan Quah, Kangqi Ng, Louis Xiang Long Ng, Yu Chang Yeh, Nai-Kuan Chou, Cong-Tat Cia, Ting-Yu Hu, Li-Kuo Kuo, Shih-Chi Ku, Phunsup Wongsurakiat, Yutthana Apichatbutr, Supattra Chiewroongroj, Rashid Nadeem, Ashraf El Houfi, Adel Alsisi, Amr Elhadidy, Mina Barsoum, Nermin Osman, Tarek Mostafa, Mohamed Elbahnasawy, Ahmed Saber, Amer Aldhalia, Omar Elmandouh, Ahmed Elsayed, Merihan A. Elbadawy, Ahmed K. Awad, Hanan M. Hemead, Farid Zand, Maryam Ouhadian, Seyed Hamid Borsi, Zahra Mehraban, Davood Kashipazha, Fatemeh Ahmadi, Mohsen Savaie, Farhad Soltani, Mahboobeh Rashidi, Reza Baghbanian, Fatemeh Javaherforoosh, Fereshteh Amiri, Arash Kiani, Mohammad Amin Zargar, Ata Mahmoodpoor, Fatemeh Aalinezhad, Gholamreza Dabiri, Golnar Sabetian, Hakimeh Sarshad, Mansoor Masjedi, Ramin Tajvidi, Seyed Mohammad Nasirodin Tabatabaei, Abdullah Khudhur Ahmed, Pierre Singer, Ilya Kagan, Merav Rigler, Daniel Belman, Phillip Levin, Belal Harara, Adei Diab, Fayez Abilama, Rebecca Ibrahim, Aya Fares, Ahmad Buimsaedah, Marwa Gamra, Ahmed Aqeelah, Almajdoub Ali Mohammed Ali, Ahmed Gaber Sadik Homaidan, Bushray Almiqlash, Hala Bilkhayr, Ahmad Bouhuwaish, Ahmed Sa Taher, Eman Abdulwahed, Fathi A. Abousnina, Aisha Khaled Hdada, Rania Jobran, Hayat Ben Hasan, Rabab Shaban Ben Hasan, Issam Serghini, Rachid Seddiki, Brahim Boukatta, Nabil Kanjaa, Doumiri Mouhssine, Maazouzi Ahmed Wajdi, Tarek Dendane, Amine Ali Zeggwagh, Brahim Housni, Oujidi Younes, Abdelhamid Hachimi, A. Ghannam, Z. Belkhadir, Sarah Amro, Mustafa Abu Jayyab, Ali Ait Hssain, Abdurahaman Elbuzidi, Edin Karic, Marcus Lance, Shaikh Nissar, Hend Sallam, Omar Elrabi, Ghaleb A. Almekhlafi, Maher Awad, Ahmed Aljabbary, Mohammad Karam Chaaban, Natalia Abu-Sayf, Mohammad Al-Jadaan, Lubna Bakr, Mounir Bouaziz, Olfa Turki, Walid Sellami, Pablo Centeno, Lic Natalia Morvillo, José Oscar Acevedo, Patricia Mabel Lopez, Rubén Fernández, Matías Segura, Dra Marta Aparicio, Microbiologa Irene Alonzo, Yanina Nuccetelli, Pablo Montefiore, Luis Felipe Reyes, Luis Felipe Reyes, Silvio A. Ñamendys-Silva, Juan P. Romero-Gonzalez, Mariana Hermosillo, Roberto Alejandro Castillo, Jesús Nicolás Pantoja Leal, Candy Garcia Aguilar, Mara Ocotlan Gonzalez Herrera, Missael Vladimir Espinoza Villafuerte, Manuel Lomeli-Teran, Jose G. Dominguez-Cherit, Adrian Davalos-Alvarez, Silvio A. Ñamendys-Silva, Luis Sánchez-Hurtado, Brigitte Tejeda-Huezo, Orlando R. Perez-Nieto, Ernesto Deloya Tomas, Liesbet De Bus, Jan De Waele, Isabelle Hollevoet, Wouter Denys, Marc Bourgeois, Sofie F. M. Vanderhaeghen, Jean-Baptiste Mesland, Pierre Henin, Lionel Haentjens, Patrick Biston, Cindérella Noel, Nathalie Layos, Benoît Misset, Nicolas De Schryver, Nicolas Serck, Xavier Wittebole, Elisabeth De Waele, Godelive Opdenacker, Pedja Kovacevic, Biljana Zlojutro, Aida Custovic, Ina Filipovic-Grcic, Radovan Radonic, Ana Vujaklija Brajkovic, Jasminka Persec, Sanja Sakan, Mario Nikolic, Hrvoje Lasic, Marc Leone, Charlotte Arbelot, Jean-François Timsit, Juliette Patrier, N. Zappela, P. 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Papanikolaou, C. Kampolis, Marina Oikonomou, Evangelos Kogkopoulos, Charikleia Nikolaou, Anastasios Sakkalis, Marinos Chatzis, Maria Georgopoulou, Anna Efthymiou, Vasiliki Chantziara, Aikaterini Sakagianni, Zoi Athanasa, Eirini Papageorgiou, Fadi Ali, Georges Dimopoulos, Mariota Panagiota Almiroudi, Polychronis Malliotakis, Diamantina Marouli, Vasiliki Theodorou, Ioannis Retselas, Vasilios Kouroulas, Georgios Papathanakos, Giorgia Montrucchio, Gabriele Sales, Gennaro De Pascale, Luca Maria Montini, Simone Carelli, Joel Vargas, Valentina Di Gravio, Daniele Roberto Giacobbe, Angelo Gratarola, Elisa Porcile, Michele Mirabella, Ivan Daroui, Giovanni Lodi, Francesco Zuccaro, Maria Grazia Schlevenin, Paolo Pelosi, Denise Battaglini, Andrea Cortegiani, Mariachiara Ippolito, Davide Bellina, Andrea Di Guardo, Lorella Pelagalli, Marco Covotta, Monica Rocco, Silvia Fiorelli, Antonella Cotoia, Anna Chiara Rizzo, Adam Mikstacki, Barbara Tamowicz, Irmina Kaptur Komorowska, Anna Szczesniak, Jozef Bojko, Anna Kotkowska, Paulina Walczak-Wieteska, Dominika Wasowska, Tomasz Nowakowski, Hanna Broda, Mariusz Peichota, Iwona Pietraszek-Grzywaczewska, Ignacio Martin-Loeches, Alessandra Bisanti, Nuno Cartoze, Tiago Pereira, Nádia Guimarães, Madalena Alves, Ana Josefina Pinheiro Marques, Ana Rios Pinto, Andriy Krystopchuk, Ana Teresa, António Manuel Pereira de Figueiredo, Isabel Botelho, Tiago Duarte, Vasco Costa, Rui Pedro Cunha, Elena Molinos, Tito da Costa, Sara Ledo, Joana Queiró, Dulce Pascoalinho, Cristina Nunes, José Pedro Moura, Énio Pereira, António Carvalho Mendes, Liana Valeanu, Serban Bubenek-Turconi, Ioana Marina Grintescu, Cristian Cobilinschi, Daniela Carmen Filipescu, Cornelia Elena Predoi, Dana Tomescu, Mihai Popescu, Alexandra Marcu, Ioana Grigoras, Olguta Lungu, Alexey Gritsan, Anastasia Anderzhanova, Yulia Meleshkina, Marat Magomedov, Nadezhda Zubareva, Maksim Tribulev, Denis Gaigolnik, Aleksandr Eremenko, Natala Vistovskaya, Maria Chukina, Vladislav Belskiy, Mikhail Furman, Ricard Ferrer Rocca, Maria Martinez, Vanessa Casares, Paula Vera, Matias Flores, Joaquin Amador Amerigo, Maria Pilar Gracia Arnillas, Rosana Munoz Bermudez, Fernando Armestar, Beatriz Catalan, Regina Roig, Laura Raguer, María Dolores Quesada, Emilio Diaz Santos, Gemma Gomà, Alejandro Ubeda, Dra Maria Salgado, Lorena Forcelledo Espina, Emilio Garcia Prieto, Dra Mj Asensio, Dra M. Rodriguez, Emilio Maseda, Alejandro Suarez De La Rica, J. Ignacio Ayestaran, Mariana Novo, Miguel Angel Blasco-Navalpotro, Alberto Orejas Gallego, Fredrik Sjövall, Dzana Spahic, Carl Johan Svensson, Michael Haney, Alicia Edin, Joyce Åkerlund, Lina De Geer, Josef Prazak, Stephan Jakob, Jl Pagani, S. Abed-Maillard, Murat Akova, Abdullah Tarik Aslan, Arif Timuroglu, Sesin Kocagoz, Hulya Kusoglu, Selcuk Mehtap, Solakoğlu Ceyhun, Neriman Defne Altintas, Leyla Talan, Bircan Kayaaslan, Ayşe Kaya Kalem, Ibrahim Kurt, Murat Telli, Barcin Ozturk, Çiğdem Erol, Emine Kubra Dindar Demiray, Sait Çolak, Türkay Akbas, Kursat Gundogan, Ali Sari, Canan Agalar, Onur Çolak, Nurcan N. Baykam, Ozlem O. Akdogan, Mesut Yilmaz, Burcu Tunay, Rumeysa Cakmak, Nese Saltoglu, Ridvan Karaali, Iftihar Koksal, Firdevs Aksoy, Ahmet Eroglu, Kemal Tolga Saracoglu, Yeliz Bilir, Seda Guzeldag, Gulden Ersoz, Guliz Evik, Hulya Sungurtekin, Cansu Ozgen, Cem Erdoğan, Yunus Gürbüz, Nilgün Altin, Yasar Bayindir, Yasemin Ersoy, Senay Goksu, Ahmet Akyol, Ayse Batirel, Sabahat Cagan Aktas, Andrew Conway Morris, Matthew Routledge, Andrew Conway Morris, Ari Ercole, David Antcliffe, Roceld Rojo, Kate Tizard, Maria Faulkner, Amanda Cowton, Melanie Kent, Ashok Raj, Artemis Zormpa, George Tinaslanidis, Reena Khade, Tomasz Torlinski, Randeep Mulhi, Shraddha Goyal, Manan Bajaj, Marina Soltan, Aimee Yonan, Rachael Dolan, Aimee Johnson, Caroline Macfie, James Lennard, Maie Templeton, Sonia Sousa Arias, Uwe Franke, Keith Hugill, Hollie Angell, Benjamin J. Parcell, Katherine Cobb, Stephen Cole, Tim Smith, Clive Graham, Jaroslav Cerman, Allison Keegan, Jenny Ritzema, Amanda Sanderson, Ashraf Roshdy, Tamas Szakmany, Tom Baumer, Rebecca Longbottom, Daniel Hall, Kate Tatham, S. Loftus, A. Husain, E. Black, S. Jhanji, R. Rao Baikady, Peter Mcguigan, Rachel Mckee, Santhana Kannan, Supriya Antrolikar, Nicholas Marsden, Valentina Della Torre, Dorota Banach, Ahmed Zaki, Matthew Jackson, Moses Chikungwa, Ben Attwood, Jamie Patel, Rebecca E. Tilley, Miss Sally K. Humphreys, Paul Jean Renaud, Anton Sokhan, Yaroslava Burma, Wendy Sligl, Nadia Baig, Lorena McCoshen, Demetrios J. Kutsogiannis, Wendy Sligl, Patricia Thompson, Tayne Hewer, Raihan Rabbani, Shihan Mahmud Redwanul Huq, Rajib Hasan, Mohammad Motiul Islam, Mohan Gurjar, Arvind Baronia, Nikhil Kothari, Ankur Sharma, Saurabh Karmakar, Priya Sharma, Janardan Nimbolkar, Pratit Samdani, R. Vaidyanathan, Noor Ahmedi Rubina, Nikhilesh Jain, Madhumati Pahuja, Ritu Singh, Saurav Shekhar, Syed Nabeel Muzaffar, Ahmad Ozair, Suhail Sarwar Siddiqui, Payel Bose, Avijatri Datta, Darshana Rathod, Mayur Patel, M. K. Renuka, Sailaja K. Baby, Carol Dsilva, Jagadish Chandran, Pralay Ghosh, Sudipta Mukherjee, Kaladhar Sheshala, Krushna Chandra Misra, Saidu Yusuf Yakubu, Euphemia Mgbosoro Ugwu, John O. Olatosi, Ibironke Desalu, Gabriel Asiyanbi, Motunrayo Oladimeji, Olusola Idowu, Fowotade Adeola, Melanie Mc Cree, Ali Adil Ali Karar, Elfayadh Saidahmed, Hytham K. S. Hamid
Funding
JdW is a senior clinical investigator funded by the Research Foundation Flanders (FWO, Ref. 1881020N). ACM is supported by a Medical Research Council Clinician Scientist Fellowship (MR/ V006118/1). NB received a fellowship grant (Grant number: P4P4PM_194449) from the Swiss National Science Foundation. Research grants were obtained from the European Society of Intensive Care Medicine (ESICM), the European Society of Clinical Microbiology and Infectious Diseases (ESCMID) study Group for Infections in Critically Ill Patients (ESGCIP), the Norva Dahlia foundation and the Redcliffe Hospital Private Practice Trust Fund.
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Alexis Tabah, Niccolò Buetti, Jean-François Timsit, Quentin Staiquly, and Stéphane Ruckly had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. All the authors approved the manuscript in its final format. Concept and design: Alexis Tabah, Jean-François Timsit, Jan De Waele, Jeffrey Lipman, and Jose Artur Paiva. Coordination: Alexis Tabah, Caroline Dallongeville, Quentin Staiquly, Stéphane Ruckly, Jean-François Timsit, Guy Francois, Murat Akova, Abdullah Tarik Aslan, Marc Leone, Andrew Conway Morris, Matteo Bassetti, Kostoula Arvaniti, Ricard Ferrer, Haibo Qiu, Jose Artur Paiva, Liesbet De Bus, Guy Francois, Farid Zand, Mohan Gurjar, Adel Alsisi, Khalid Abidi, Hendrik Bracht, Yoshiro Hayashi, Adam Mikstacki, Alexey Gritsan, Kyeongman Jeon, Liana Valeanu, Helmi Sulaiman, Tony Yeh, Muhammed Elhadi, Mounir Bouaziz, Khalid Mahmood Khan Nafees, Gabriela Vidal, Qing Yuan Goh, Dmitriy Viderman, Silvio A. Namendys-Silva, Josef Prazak, Phunsup Wongsurakiat, Wendy Sligl, Pierre Singer, Ali Aithssain, Fredrik Sjovall, Pedja Kovacevic, Bashir Kamal Eldin Hamid el Sanousi, Mario Arias, Aaron Mark Hernandez, Ignacio Martin-Loeches, Ina Filipovic-Grcic, Fayez Abillama, Raihan Rabbani, Mervyn Mer, Lowell Ling, Oyebola Olubodun Adekola. Communication, centre registration and coordination: Caroline Dallongeville. Quality control, data curation, analysis, and interpretation: Alexis Tabah, Niccolò Buetti, François Barbier, Caroline Dallongeville, Quentin Staiquly, Stéphane Ruckly, and Jean-François Timsit. Statistical analysis: Quentin Staiquly, Stéphane Ruckly, and Jean-François Timsit. Drafting of the manuscript: Alexis Tabah. Initial revision of the manuscript: Niccolò Buetti, François Barbier, Jean-François Timsit and Jeffrey Lipman. Revision of the manuscript for important intellectual content: All authors. Administrative, technical, or material support: Caroline Dallongeville, Quentin Staiquly, Stéphane Ruckly, and Guy Francois. Group Information: The EUROBACT-2 national coordinators, scientific committee and investigators are listed in the electronic supplement. Additional Contributions: We thank Guy Francois, Division of Scientific Affairs and Research of the ESICM for his unvaluable assistance in recruiting participating ICUs. We thank the health care workers at each study site, laboratory, and beyond that contributed to the EUROBACT-2 study and acknowledge their work during the initial waves of the COVID-19 pandemic. We thank the patients who participated in the EUROBACT-2 study. We thank Professor Andrea Marshall, PhD, and Doctor Mahesh Ramanan, MBBS, FCICM for proofreading and editing the manuscript.
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AT has nothing to disclose, NB has nothing to disclose, QS has nothing to disclose, SR has nothing to disclose, MA reports honoraria paid to his university for educational activities by Pfizer, Sanofi, MSD and Astra Zeneca, ATA has nothing to disclose, ML reported consulting and lecture fees from Amomed Pharma, Aspen, LFB and Gilead, ACM has received payment for speaking on behalf of Boston Scientific and sits on the Scientific Advisory Board of Cambridge Infection Diagnostics, a start-up seeking to develop novel diagnostics for infectious diseases, MB received advisory board, speaker activities from Angelini, Bayer, Biomerieux, Cidara, Gilead, Menarini, MSD, Pfizer, Roche, Shionogi, study grants from: Angelini, Shionogi, Cidara, Gilead, Pfizer, and MSD, KA has nothing to disclose, JL has received lecture fees and honoraria from MSD, RF reports Payment for lectures, speakers bureaus or advisory boards from Grifols, MSD, Pfizer, Gilead, Shionogi, Thermofisher, Hill Rom, AOP Health, BD, HQ has nothing to disclose, JAP reports consulting, advisory boards or lectures fees and honoraria for MSD, Pfizer, Astra-Zeneca, Gilead, Jansen, Cepheid, AOP Orphan Pharmaceuticals, PP reported advisory boards participation for Gilead, Technophage and Sanofi, lectures fees from MSD, Gilead and Pfizer, and research grant from Abionic, LDB has nothing to disclose, JdW has consulted for Pfizer, MSD (honoraria paid to institution), FZ has nothing to disclose, MG has nothing to disclose, AA has nothing to disclose, KA has nothing to disclose, HB has nothing to disclose, YH has nothing to disclose, KJ has nothing to disclose, ME has nothing to disclose, FB reported consulting and lecture fees, conference invitation from MSD and lecture fees from BioMérieux, J-FT reported advisory boards participation for Merck, Gilead, Beckton-Dickinson, Pfizer, Shinogi, Medimune, Paratek, research grants from Merck, Pfizer, Thermofischer.
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The members of the EUROBACT-2 study group are listed in the Acknowledgement section of the manuscript.
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Tabah, A., Buetti, N., Staiquly, Q. et al. Epidemiology and outcomes of hospital-acquired bloodstream infections in intensive care unit patients: the EUROBACT-2 international cohort study. Intensive Care Med 49, 178–190 (2023). https://doi.org/10.1007/s00134-022-06944-2
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DOI: https://doi.org/10.1007/s00134-022-06944-2