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Abstract
Around one-third of patients diagnosed with COVID-19 develop a severe illness that requires admission to the Intensive Care Unit (ICU). In clinical practice, clinicians have learned that patients admitted to the ICU due to severe COVID-19 frequently develop ventilator-associated lower respiratory tract infections (VA-LRTI). This study aims to describe the clinical characteristics, the factors associated with VA-LRTI, and its impact on clinical outcomes in patients with severe COVID-19. This was a multicentre, observational cohort study conducted in ten countries in Latin America and Europe. We included patients with confirmed rtPCR for SARS-CoV-2 requiring ICU admission and endotracheal intubation. Only patients with a microbiological and clinical diagnosis of VA-LRTI were included. Multivariate Logistic regression analyses and Random Forest were conducted to determine the risk factors for VA-LRTI and its clinical impact in patients with severe COVID-19. In our study cohort of 3287 patients, VA-LRTI was diagnosed in 28.8% [948/3287]. The cumulative incidence of ventilator-associated pneumonia (VAP) was 18.6% [610/3287], followed by ventilator-associated tracheobronchitis (VAT) 10.3% [338/3287]. A total of 1252 bacteria species were isolated. The most frequently isolated pathogens were Pseudomonas aeruginosa (21.2% [266/1252]), followed by Klebsiella pneumoniae (19.1% [239/1252]) and Staphylococcus aureus (15.5% [194/1,252]). The factors independently associated with the development of VA-LRTI were prolonged stay under invasive mechanical ventilation, AKI during ICU stay, and the number of comorbidities. Regarding the clinical impact of VA-LRTI, patients with VAP had an increased risk of hospital mortality (OR [95% CI] of 1.81 [1.40–2.34]), while VAT was not associated with increased hospital mortality (OR [95% CI] of 1.34 [0.98–1.83]). VA-LRTI, often with difficult-to-treat bacteria, is frequent in patients admitted to the ICU due to severe COVID-19 and is associated with worse clinical outcomes, including higher mortality. Identifying risk factors for VA-LRTI might allow the early patient diagnosis to improve clinical outcomes.
Trial registration: This is a prospective observational study; therefore, no health care interventions were applied to participants, and trial registration is not applicable.
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Title
Risk factors for developing ventilator-associated lower respiratory tract infection in patients with severe COVID-19: a multinational, multicentre study, prospective, observational study
Author
Reyes, Luis Felipe 1 ; Rodriguez, Alejandro 2 ; Fuentes, Yuli V. 3 ; Duque, Sara 4 ; García-Gallo, Esteban 4 ; Bastidas, Alirio 4 ; Serrano-Mayorga, Cristian C. 3 ; Ibáñez-Prada, Elsa D. 4 ; Moreno, Gerard 2 ; Ramirez-Valbuena, Paula C. 4 ; Ospina-Tascon, Gustavo 5 ; Hernandez, Glenn 6 ; Silva, Edwin 7 ; Díaz, Ana Maria 8 ; Jibaja, Manuel 8 ; Vera-Alarcon, Magdalena 6 ; Díaz, Emili 9 ; Bodí, María 2 ; Solé-Violán, Jordi 10 ; Ferrer, Ricard 11 ; Albaya-Moreno, Antonio 12 ; Socias, Lorenzo 13 ; Figueroa, William 4 ; Lozano-Villanueva, Jose L. 14 ; Varón-Vega, Fabio 15 ; Estella, Ángel 16 ; Loza-Vazquez, Ana 17 ; Jorge-García, Ruth 18 ; Sancho, Isabel 19 ; Shankar-Hari, Manu 20 ; Martin-Loeches, Ignacio 21 ; Gorordo, Luis Antonio 22 ; Buitrago, Ricardo 23 ; Poveda, Marcela 23 ; Saucedo, Lina Maria 23 ; Estenssoro, Elisa 24 ; Ortiz, Guillermo 25 ; Nin, Nicolas 26 ; Arango, Alfonso Jose 4 ; Aguilar, Alvaro 4 ; Ayala, Andrea Lizeth 4 ; Bayona, Andrea Viviana 4 ; Rodriguez, Angelica 4 ; Aponte, Carol Viviana 4 ; Forero-Carreño, Carolina 4 ; Muñoz, Conny Stefanny 4 ; Estrada, Cristian Augusto 4 ; Romero, Cristopher 4 ; Trujillo, Danilo 4 ; Holguin, Diego 4 ; Chavez-Villegas, Jesus 4 ; Rodriguez, Faure 4 ; Franco, Francisco 4 ; Sánchez, Hernan 4 ; Moncayo, Janett Vanessa 4 ; Pinedo, Jennifer A. 4 ; Bravo, Jesica Valeria 4 ; Cruz, Jose David 4 ; Angel, Jose Miguel 4 ; Castro-Lara, Jovany 4 ; Mantilla, Karen Andrea 4 ; Garcia, Lorena 4 ; Pabón, Lorena 4 ; Lopez, Luis Arturo 4 ; Mamani, Luis Fernando 4 ; Yupa, Marisa Lucrecia 4 ; Quevedo, Valeria Catalina 4 ; Loza, Ana 27 ; Zapata, Diego Matallana 28 ; Torres, Isabel Díaz 29 ; Cuadros, Sonia Ibañez 29 ; Nuñez, María Recuerda 29 ; Pérez, Maria Luz Carmona 29 ; Ramos, Jorge Gómez 29 ; Casas, Alba Villares 29 ; Cantón, María Luisa 30 ; Contreras, José Javier González 30 ; Chomón, Helena Pérez 30 ; Chicote, Nerissa Alvarez 30 ; González, Alberto Sousa 30 ; De Alba Aparicio, María 31 ; García, Ruth Jorge 32 ; Montori, Laura Sánchez 33 ; García, Sandra Herrero 33 ; Moreno, Paula Abanses 33 ; García, Carlos Mayordomo 33 ; Bonet, Tomás Mallor 34 ; Bonafonte, Paula Omedas 34 ; Gonzalez, Enric Franquesa 34 ; Vidales, Nestor Bueno 34 ; Buil, Paula Ocabo 34 ; Arbeloa, Carlos Serón 34 ; Ibañez, Pablo Guerrero 19 ; Gutierrez, Pablo 19 ; Valdovinos, María Concepción 35 ; Canto, Raquel 35 ; Mariño, Ana Luz Balán 36 ; Fernández, María José Gutiérrez 36 ; Cuadrado, Marta Martín 36 ; Arias, Belén García 36 ; Espina, Lorena Forcelledo 37 ; Soria, Lucía Viña 37 ; Iglesias, Lorena Martín 37 ; Amor, Lucía López 37 ; Rey, Elisabet Fernández 37 ; Prieto, Emilio García 37 ; Ruíz, Débora Fernández 38 ; González, Carla Martínez 38 ; Borges‐Sá, Marcio 13 ; Pérez, María Aranda 13 ; Socias, Antonia 13 ; Goytisolo, José Ma Bonell 39 ; Mayayo, Inmaculada Alcalde 39 ; Corradini, Carlos 39 ; Ceniceros, Isabel 39 ; Rodríguez, Edwin 39 ; Rota, Jose Ignacio Ayestarán 40 ; Novo, Mariana Andrea 40 ; Climent, Joaquim Colomina 40 ; Castilla, Albert Figueras 40 ; Rullan, Tomàs Leal 40 ; Sastre, Maria Magdalena Garcias 40 ; Senoff, Rossana Pérez 41 ; Fernández, Ramón 42 ; González, Juan Carlos Martín 43 ; Ortiz, Carmen Pérez 43 ; Santana, José Luciano Cabrera 43 ; Agra, Juan José Cáceres 43 ; Romero, Domingo González 43 ; Ortega, Ana Casamitjana 43 ; Gómez, Luis Alberto Ramos 44 ; Ojeda, Carolina Montelongo 44 ; Rodríguez, Alejandro 45 ; Trefler, Sandra 45 ; Claverias, Laura 45 ; Carbonell, Raquel 45 ; Esteve, Erika 45 ; Olona, Montserrat 45 ; Teixidó, Xavier 45 ; Vidal, Monserrat Vallverdú 46 ; Garrido, Begoña Balsera 46 ; Gallofré, Elisabeth Papiol 11 ; Martell, Raquel Albertos 11 ; Peñarrocha, Rosa Alcaráz 11 ; Casals, Xavier Nuvials 11 ; Roca, Ricard Ferrer 11 ; Vázquez, Eric Adrián Mayor 47 ; Campo, Ferrán Roche 47 ; Martínez, Pablo Concha 47 ; Llasat, Diego Franch 47 ; Masclanz, Joan Ramón 48 ; Corral, Judith Marín‐ 48 ; Pérez, Purificación 48 ; Muñoz, Rosana 48 ; Vila, Clara 48 ; de Molina, Francisco Javier González 49 ; Moya, Elisabeth Navas 49 ; Trenado, Josep 49 ; Vallverdú, Imma 50 ; Castañé, Eric 50 ; Santos, Emili Díaz 51 ; Goma, Gemma 51 ; Edg 51 ; Suberviola, Borja 52 ; Moreno, Antonio Albaya 53 ; Crespo, Carlos Marian 53 ; Pérez, Carmen Carolina Sena 54 ; Linde, Francisca Arbol 54 ; Donaire, Diana Monge 55 ; Martínez, Vega Losada 55 ; Castroviejo, Nuria Rodrigo 55 ; Ferrigno, Gerardo 55 ; Beltrán, Reyes 55 ; Sanmartino, Carolina 55 ; Maján, Concepción Tarancón 55 ; Gutiérrez, Alfredo Marcos 55 ; Valverde, Virginia Hidalgo 56 ; López, Caridad Martín 56 ; Badallo, Oihane 57 ; del Valle Ortiz, María 57 ; Arlanzón, Rebeca Vara 57 ; Posadilla, David Iglesias 57 ; Recio, María Teresa 58 ; Ballesteros, Juan Carlos 58 ; Laza, Enrique 59 ; Curto, Elena Gallego 60 ; García, Ma Car‐men Sánchez 60 ; Díaz‐Tavora, Miguel 61 ; Mancha, Rosa 61 ; Montes, Ana Ortega 62 ; Barbachano, Isabel Gallego 62 ; Mantiñán, Eva Sanmartín 62 ; Cordero, María Lourdes 63 ; García, Raquel María Rodríguez 63 ; Zapata, Jorge Gámez 63 ; Vázquez, María Gestal 63 ; Orjales, María José Castro 64 ; Diéguez, María Isabel Álvarez 64 ; Velasco, Carmen Rivero 65 ; Massa, Beatriz Lence 65 ; Martí, Ignacio 66 ; Tejedor, Alberto Hernández 67 ; Ramos, Esther Ma López 68 ; Elvira, Laura Alcázar Sánchez 68 ; Montero, Rocío Molina 68 ; Delgado, Ma Consuelo Pintado 68 ; de la Peña, María Trascasa Muñoz 68 ; de Zárate Ansotegui, Yaiza Betania Ortiz 68 ; Aranda, Alejandra Acha 68 ; Lucas, Juan Higuera 68 ; Giralt, Juan Antonio Sanchez 69 ; Llano, Marta Chicot 69 ; Fernández, Nuria Arevalillo 69 ; Galindo, Marta Sánchez 69 ; Ruiz, Ricardo Andino 69 ; Berlanga, Alfonso Canabal 69 ; Sánchez, Miguel 70 ; Nieto, Mercedes 70 ; Sarmiento, Eduardo Arias 71 ; Blázquez, Adoración Bueno 71 ; de la Casa, Rosa María 71 ; Martín, Fátima 71 ; González, Samuel 71 ; Quintana, Elena Martínez 72 ; Rueda, Bernardo Gil 72 ; Cañigral, Áurea Higon 72 ; Gómez, Laura López 72 ; Delis, Pablo Safwat Bayoumi 72 ; Muore, Augusto Montenegro 72 ; Luengas, Ángel Andrés Agamez 72 ; Soler, Enriqueta Andreu 73 ; Pérez, Ana Beatriz 73 ; de Gea García, José Higinio 73 ; Rubio, Rubén Jara 73 ; Cámara, Silvia Sánchez 73 ; Flores, Alba Moreno 73 ; Sánchez, José Moya 73 ; Martínez, Daniel Fran‐cisco Pérez 73 ; del Rey Carrión, Ma Desamparados 73 ; Lledó, María José Rico 74 ; Navarro, Juana María Serrano 74 ; Ruíz, Juan Fran‐cisco Martín 74 ; Hidalgo, Julián Triviño 74 ; Ferrer, África López 74 ; Navalón, Isabel Cremades 74 ; Payá, Josefa Murcia 75 ; Gallego, J. M. Allegre 75 ; del Carmen Lorente, María 76 ; Natera, Ruth González 77 ; de Murillo, Raquel Garrido López 77 ; Gros, Tania Ojuel 77 ; Viguera, Raquel Flecha 77 ; González, Isabel López 77 ; Herrera, Adriana García 78 ; Tello, Loreto Vidaur 79 ; Aseguinolaza, Maialen 79 ; Eguibar, Itziar 79 ; Parra, Asunción Marqués 80 ; Marti, Sergio García 80 ; Aguilar, Alberto Lorenzo 80 ; Bosch, Laura Bellver 80 ; Sanchez, Victor Gascón 80 ; De la Guía Ortega, Sonia 80 ; Montell, Martín Parejo 81 ; Muncharaz, Alberto Belenguer 81 ; Garces, Hector Hernández 81 ; Montero, Victor Ramírez 81 ; Gómez, Mónica Crespo 81 ; Algarra, Verónica Martí 81 ; Chinesta, Susana Sancho 82 ; Cervera, Joaquin Arguedas 82 ; Cebrian, Faustino Álvarez 82 ; Pérez, Begoña Balerdi 82 ; Fores, Rosa Jannone 82 ; de Maglia, Javier Botella 82 ; Monleón, Nieves Carbonell 83 ; Franco, Jose Ferreres 83 ; Lazaro, Ainhoa Serrano 83 ; Díaz, Mar Juan 83 ; Cortés, María Luisa Blasco 83 ; Fayos, Laura 84 ; Giménez, Julia 84 ; Soriano, Gaspar 84 ; Navarro, Ricardo 84 ; Mas, Sonia 85 ; Bisbal, Elena 85 ; Albert, Laura 85 ; Romero, Johncard 85 ; Cabreara, Juan Fernández 85 ; Ortíz, Andrea 86 ; Ribas, Antonio Margarit 87 ; Guasch, Neus 87
1 Universidad de La Sabana, Unisabana Center for Translational Science, Chía, Colombia (GRID:grid.412166.6) (ISNI:0000 0001 2111 4451); Clinica Universidad de La Sabana, Chía, Colombia (GRID:grid.412166.6) (ISNI:0000 0001 2111 4451); University of Oxford, Pandemic Sciences Institute, Oxford, UK (GRID:grid.4991.5) (ISNI:0000 0004 1936 8948)
2 Hospital Universitari Joan XXIII, Critical Care Department, URV/IISPV/CIBERES, Tarragona, Spain (GRID:grid.411435.6) (ISNI:0000 0004 1767 4677)
3 Universidad de La Sabana, Unisabana Center for Translational Science, Chía, Colombia (GRID:grid.412166.6) (ISNI:0000 0001 2111 4451); Clinica Universidad de La Sabana, Chía, Colombia (GRID:grid.412166.6) (ISNI:0000 0001 2111 4451)
4 Universidad de La Sabana, Unisabana Center for Translational Science, Chía, Colombia (GRID:grid.412166.6) (ISNI:0000 0001 2111 4451)
5 Fundación Valle del Lili, Cali, Colombia (GRID:grid.477264.4)
6 Pontificia Universidad Católica de Chile, Critical Care Department, Santiago, Chile (GRID:grid.7870.8) (ISNI:0000 0001 2157 0406)
7 Fundación Clínica Shaio, Bogotá, Colombia (GRID:grid.7870.8)
8 Eugenio Espejo Hospital of Specialties, Quito, Ecuador (GRID:grid.7870.8)
9 Universitat Autonoma Barcelona, Critical Care Department, Hospital Universitari Parc Taulí, Sabadell, Spain (GRID:grid.7080.f) (ISNI:0000 0001 2296 0625)
10 Hospital Universitario Dr Negrín, Las Palmas de Gran Canaria, Spain (GRID:grid.411250.3) (ISNI:0000 0004 0399 7109); Universidad Fernando Pessoa, Canarias, Spain (GRID:grid.512367.4)
11 Vall d’Hebron Hospital Universitari, Barcelona, Spain (GRID:grid.411083.f) (ISNI:0000 0001 0675 8654)
12 Guadalajara University Hospital, Guadalajara, Spain (GRID:grid.411098.5) (ISNI:0000 0004 1767 639X)
13 Son Llatzer University Hospital, Palma de Mallorca, Spain (GRID:grid.413457.0) (ISNI:0000 0004 1767 6285)
14 Fundación Clínica Shaio, Bogotá, Colombia (GRID:grid.412166.6)
15 La Cardio, Fundación Neumológica Colombiana, Bogotá, Colombia (GRID:grid.492703.b) (ISNI:0000 0004 0440 9989)
16 Jerez University Hospital, Jerez de la Frontera, Spain (GRID:grid.492703.b)
17 Hospital Universitario Virgen del Valme, Critical Care Department, Sevilla, Spain (GRID:grid.412800.f) (ISNI:0000 0004 1768 1690)
18 Hospital Providencial Nuestra Señora de Gracia, Zaragoza, Spain (GRID:grid.412800.f)
19 Hospital Universitario Miguel Servet, Critical Care Department, Zaragoza, Spain (GRID:grid.411106.3) (ISNI:0000 0000 9854 2756)
20 Royal Infirmary of Edinburgh, Intensive Care Unit, Edinburgh, UK (GRID:grid.418716.d) (ISNI:0000 0001 0709 1919); The University of Edinburgh, Centre for Inflammation Research, Edinburgh, Scotland, UK (GRID:grid.4305.2) (ISNI:0000 0004 1936 7988)
21 St. James’s Hospital, Department of Intensive Care Medicine, Multidisciplinary Intensive Care Research Organization (MICRO), Dublin, UK (GRID:grid.443984.6) (ISNI:0000 0000 8813 7132)
22 Hospital Juárez de México, Critical Care Unit, Mexico, Mexico (GRID:grid.414788.6)
23 Fundación Clínica Shaio, Bogotá, Colombia (GRID:grid.414788.6)
24 Hospital Interzonal de Agudos San Martín de La Plata, La Plata, Argentina (GRID:grid.414788.6)
25 Hospital Santa Clara, Bogota, Colombia (GRID:grid.414788.6)
26 Hospital Español, Intensive Care Unit, Montevideo, Uruguay (GRID:grid.414788.6)
27 UCI Hospital Universitario Virgen de Valme, Seville, Spain (GRID:grid.412800.f) (ISNI:0000 0004 1768 1690)
28 UCI Hospital Quirón, Huelva, Spain (GRID:grid.412800.f)
29 UCI Hospital Universitario Puerto Real, Cádiz, Spain (GRID:grid.411254.7)
30 UCI Hospital Universitario Virgen de la Macarena, Seville, Spain (GRID:grid.411375.5) (ISNI:0000 0004 1768 164X)
31 UCI Hospital Universitario Reina Sofía, Córdoba, Spain (GRID:grid.411349.a) (ISNI:0000 0004 1771 4667)
32 UCI Hospital Nuestra Señora de Gracia, Zaragoza, Spain (GRID:grid.411349.a)
33 UCI Hospital Clínico Universitario Lozano Blesa, Zaragoza, Spain (GRID:grid.411050.1) (ISNI:0000 0004 1767 4212)
34 UCI Hospital General San Jorge, Huesca, Spain (GRID:grid.415076.1) (ISNI:0000 0004 1765 5935)
35 UCI Hospital Obispo Polanco, Teruel, Spain (GRID:grid.414940.c) (ISNI:0000 0004 1794 9861)
36 UCI Hospital Universitario San Agustín, Avilés, Spain (GRID:grid.414940.c)
37 UCI Hospital Universitario Central de Asturias, Oviedo, Spain (GRID:grid.411052.3) (ISNI:0000 0001 2176 9028)
38 UCI Hospital Cabueñes, Gijón, Spain (GRID:grid.414440.1) (ISNI:0000 0000 9314 4177)
39 UCI Hospital Quirón Salud Palmaplanas, Palma de Mallorca, Spain (GRID:grid.413457.0)
40 UCI Hospital Universitario Son Espases, Palma de Mallorca, Spain (GRID:grid.411164.7) (ISNI:0000 0004 1796 5984)
41 UCI Hospital Comarcal d’Inca, Inca, Spain (GRID:grid.490114.9)
42 UCI Hospital Mateu Orfila, Mao, Spain (GRID:grid.490114.9)
43 UCI Complejo Hospitalario Universitario Insular—Materno Infantil, Las Palmas de Gran Canaria, Spain (GRID:grid.411322.7) (ISNI:0000 0004 1771 2848)
44 UCI Hospital General de la Palma, Tenerife, Spain (GRID:grid.411322.7)
45 UCI Hospital Universitari de Tarragona Joan XXIII, Tarragona, Spain (GRID:grid.411435.6) (ISNI:0000 0004 1767 4677)
46 UCI Hospital Universitari Arnau de Vilanova, Lleida, Spain (GRID:grid.411443.7) (ISNI:0000 0004 1765 7340)
47 UCI Hospital Verge de la Cinta, Tortosa, Spain (GRID:grid.490132.d)
48 UCI Hospital del Mar, Barcelona, Spain (GRID:grid.411142.3) (ISNI:0000 0004 1767 8811)
49 UCI Hospital Mutua de Terrasa, Terrasa, Spain (GRID:grid.411142.3)
50 UCI Hospital Sant Joan, Reus, Spain (GRID:grid.411136.0) (ISNI:0000 0004 1765 529X)
51 UCI Hospital Parc Tauli, Sabadell, Spain (GRID:grid.414560.2) (ISNI:0000 0004 0506 7757)
52 UCI Hospital Universitario Marqués de Valdecillas, Santander, Spain (GRID:grid.414560.2)
53 UCI Hospital Universitario de Guadalajara, Guadalajara, Spain (GRID:grid.411098.5) (ISNI:0000 0004 1767 639X)
54 UCI Hospital Nuestra Señora del Prado, Toledo, Spain (GRID:grid.477416.7)
55 UCI Hospital Virgen de la Concha, Zamora, Spain (GRID:grid.413506.5) (ISNI:0000 0000 9961 7465)
56 UCI Complejo Asistencial de Segovia, Segovia, Spain (GRID:grid.413506.5)
57 UCI Hospital universitario de Burgos, Burgos, Spain (GRID:grid.459669.1) (ISNI:0000 0004 1771 1036)
58 UCI Hospital Clínica de Salamanca, Salamanca, Spain (GRID:grid.459669.1)
59 UCI Hospital Universitario de Ceuta, Ceuta, Spain (GRID:grid.459669.1)
60 UCI Hospital San Pedro de Alcántara, Cáceres, Spain (GRID:grid.413393.f) (ISNI:0000 0004 1771 1124)
61 UCI Hospital de Mérida, Mérida, Spain (GRID:grid.413393.f)
62 UCI Hospital Montecelo, Pontevedra, Spain (GRID:grid.414863.c) (ISNI:0000 0000 9921 6370)
63 UCI CHUAC A Coruña, A Coruña, Spain (GRID:grid.414863.c)
64 UCI Centro Hospital Universitario de Ferrol, Ferrol, Spain (GRID:grid.414863.c)
65 UCI Hospitalario Clínico Universitario de Santiago, Santiago de Compostela, Spain (GRID:grid.11794.3a) (ISNI:0000000109410645)
66 UCI Hospital Lucus Augusti, Lugo, Spain (GRID:grid.414792.d) (ISNI:0000 0004 0579 2350)
67 UCI IFEMA, Madrid, Spain (GRID:grid.414792.d)
68 UCI Hospital Príncipe de Asturias, Madrid, Spain (GRID:grid.411336.2) (ISNI:0000 0004 1765 5855)
69 UCI Hospital de la Princesa, Madrid, Spain (GRID:grid.411251.2) (ISNI:0000 0004 1767 647X)
70 UCI Hospital Clinico San Carlos, Madrid, Spain (GRID:grid.411068.a) (ISNI:0000 0001 0671 5785)
71 UCI Hospital HLA la Moncloa, Madrid, Spain (GRID:grid.411068.a)
72 UCI Hospital Morales Meseguer, Murcia, Spain (GRID:grid.411101.4) (ISNI:0000 0004 1765 5898)
73 UCI Hospital Clínico Universitario Virgen de la Arrixaca, Murcia, Spain (GRID:grid.411372.2) (ISNI:0000 0001 0534 3000)
74 UCI Hospital Reina Sofía, Murcia, Spain (GRID:grid.411089.5) (ISNI:0000 0004 1768 5165)
75 UCI Hospital Santa Lucía, Cartagena, Spain (GRID:grid.411089.5)
76 UCI Hospital Rafael Méndez, Lorca, Spain (GRID:grid.490171.a) (ISNI:0000 0004 1793 8687)
77 UCI Hospital Reina Sofía, Tudela, Spain (GRID:grid.411349.a) (ISNI:0000 0004 1771 4667)
78 UCI Hospital García Orcoyen, Estella‐Lizarra, Spain (GRID:grid.411349.a)
79 UCI Hospital Universitario de Donostia, Donostia, Spain (GRID:grid.414651.3) (ISNI:0000 0000 9920 5292)
80 UCI Hospital Universitario de La Ribera, Alzira, Spain (GRID:grid.440284.e) (ISNI:0000 0005 0602 4350)
81 UCI Hospital Dr. Peset, Valencia, Spain (GRID:grid.411289.7) (ISNI:0000 0004 1770 9825)
82 UCI Hospital Universitari i Politècnic La Fe, Valencia, Spain (GRID:grid.84393.35) (ISNI:0000 0001 0360 9602)
83 UCI Hospital Clínico Universitario de Valencia, Valencia, Spain (GRID:grid.411308.f)
84 UCI Hospital Virgen de los Lirios de Alcoy, Alicante, Spain (GRID:grid.413522.3) (ISNI:0000 0000 9189 6148)
85 UCI Hospital Arnau de Vilanova, Valencia, Spain (GRID:grid.413937.b) (ISNI:0000 0004 1770 9606)
86 UCI Hospital Comarcal de Vinarós, Vinarós, Spain (GRID:grid.413937.b)
87 ICU Hospital nostra Señyora de Meritxell, Les Esclades, Spain (GRID:grid.413937.b)
1 Universidad de La Sabana, Unisabana Center for Translational Science, Chía, Colombia (GRID:grid.412166.6) (ISNI:0000 0001 2111 4451); Clinica Universidad de La Sabana, Chía, Colombia (GRID:grid.412166.6) (ISNI:0000 0001 2111 4451); University of Oxford, Pandemic Sciences Institute, Oxford, UK (GRID:grid.4991.5) (ISNI:0000 0004 1936 8948)
2 Hospital Universitari Joan XXIII, Critical Care Department, URV/IISPV/CIBERES, Tarragona, Spain (GRID:grid.411435.6) (ISNI:0000 0004 1767 4677)
3 Universidad de La Sabana, Unisabana Center for Translational Science, Chía, Colombia (GRID:grid.412166.6) (ISNI:0000 0001 2111 4451); Clinica Universidad de La Sabana, Chía, Colombia (GRID:grid.412166.6) (ISNI:0000 0001 2111 4451)
4 Universidad de La Sabana, Unisabana Center for Translational Science, Chía, Colombia (GRID:grid.412166.6) (ISNI:0000 0001 2111 4451)
5 Fundación Valle del Lili, Cali, Colombia (GRID:grid.477264.4)
6 Pontificia Universidad Católica de Chile, Critical Care Department, Santiago, Chile (GRID:grid.7870.8) (ISNI:0000 0001 2157 0406)
7 Fundación Clínica Shaio, Bogotá, Colombia (GRID:grid.7870.8)
8 Eugenio Espejo Hospital of Specialties, Quito, Ecuador (GRID:grid.7870.8)
9 Universitat Autonoma Barcelona, Critical Care Department, Hospital Universitari Parc Taulí, Sabadell, Spain (GRID:grid.7080.f) (ISNI:0000 0001 2296 0625)
10 Hospital Universitario Dr Negrín, Las Palmas de Gran Canaria, Spain (GRID:grid.411250.3) (ISNI:0000 0004 0399 7109); Universidad Fernando Pessoa, Canarias, Spain (GRID:grid.512367.4)
11 Vall d’Hebron Hospital Universitari, Barcelona, Spain (GRID:grid.411083.f) (ISNI:0000 0001 0675 8654)
12 Guadalajara University Hospital, Guadalajara, Spain (GRID:grid.411098.5) (ISNI:0000 0004 1767 639X)
13 Son Llatzer University Hospital, Palma de Mallorca, Spain (GRID:grid.413457.0) (ISNI:0000 0004 1767 6285)
14 Fundación Clínica Shaio, Bogotá, Colombia (GRID:grid.412166.6)
15 La Cardio, Fundación Neumológica Colombiana, Bogotá, Colombia (GRID:grid.492703.b) (ISNI:0000 0004 0440 9989)
16 Jerez University Hospital, Jerez de la Frontera, Spain (GRID:grid.492703.b)
17 Hospital Universitario Virgen del Valme, Critical Care Department, Sevilla, Spain (GRID:grid.412800.f) (ISNI:0000 0004 1768 1690)
18 Hospital Providencial Nuestra Señora de Gracia, Zaragoza, Spain (GRID:grid.412800.f)
19 Hospital Universitario Miguel Servet, Critical Care Department, Zaragoza, Spain (GRID:grid.411106.3) (ISNI:0000 0000 9854 2756)
20 Royal Infirmary of Edinburgh, Intensive Care Unit, Edinburgh, UK (GRID:grid.418716.d) (ISNI:0000 0001 0709 1919); The University of Edinburgh, Centre for Inflammation Research, Edinburgh, Scotland, UK (GRID:grid.4305.2) (ISNI:0000 0004 1936 7988)
21 St. James’s Hospital, Department of Intensive Care Medicine, Multidisciplinary Intensive Care Research Organization (MICRO), Dublin, UK (GRID:grid.443984.6) (ISNI:0000 0000 8813 7132)
22 Hospital Juárez de México, Critical Care Unit, Mexico, Mexico (GRID:grid.414788.6)
23 Fundación Clínica Shaio, Bogotá, Colombia (GRID:grid.414788.6)
24 Hospital Interzonal de Agudos San Martín de La Plata, La Plata, Argentina (GRID:grid.414788.6)
25 Hospital Santa Clara, Bogota, Colombia (GRID:grid.414788.6)
26 Hospital Español, Intensive Care Unit, Montevideo, Uruguay (GRID:grid.414788.6)
27 UCI Hospital Universitario Virgen de Valme, Seville, Spain (GRID:grid.412800.f) (ISNI:0000 0004 1768 1690)
28 UCI Hospital Quirón, Huelva, Spain (GRID:grid.412800.f)
29 UCI Hospital Universitario Puerto Real, Cádiz, Spain (GRID:grid.411254.7)
30 UCI Hospital Universitario Virgen de la Macarena, Seville, Spain (GRID:grid.411375.5) (ISNI:0000 0004 1768 164X)
31 UCI Hospital Universitario Reina Sofía, Córdoba, Spain (GRID:grid.411349.a) (ISNI:0000 0004 1771 4667)
32 UCI Hospital Nuestra Señora de Gracia, Zaragoza, Spain (GRID:grid.411349.a)
33 UCI Hospital Clínico Universitario Lozano Blesa, Zaragoza, Spain (GRID:grid.411050.1) (ISNI:0000 0004 1767 4212)
34 UCI Hospital General San Jorge, Huesca, Spain (GRID:grid.415076.1) (ISNI:0000 0004 1765 5935)
35 UCI Hospital Obispo Polanco, Teruel, Spain (GRID:grid.414940.c) (ISNI:0000 0004 1794 9861)
36 UCI Hospital Universitario San Agustín, Avilés, Spain (GRID:grid.414940.c)
37 UCI Hospital Universitario Central de Asturias, Oviedo, Spain (GRID:grid.411052.3) (ISNI:0000 0001 2176 9028)
38 UCI Hospital Cabueñes, Gijón, Spain (GRID:grid.414440.1) (ISNI:0000 0000 9314 4177)
39 UCI Hospital Quirón Salud Palmaplanas, Palma de Mallorca, Spain (GRID:grid.413457.0)
40 UCI Hospital Universitario Son Espases, Palma de Mallorca, Spain (GRID:grid.411164.7) (ISNI:0000 0004 1796 5984)
41 UCI Hospital Comarcal d’Inca, Inca, Spain (GRID:grid.490114.9)
42 UCI Hospital Mateu Orfila, Mao, Spain (GRID:grid.490114.9)
43 UCI Complejo Hospitalario Universitario Insular—Materno Infantil, Las Palmas de Gran Canaria, Spain (GRID:grid.411322.7) (ISNI:0000 0004 1771 2848)
44 UCI Hospital General de la Palma, Tenerife, Spain (GRID:grid.411322.7)
45 UCI Hospital Universitari de Tarragona Joan XXIII, Tarragona, Spain (GRID:grid.411435.6) (ISNI:0000 0004 1767 4677)
46 UCI Hospital Universitari Arnau de Vilanova, Lleida, Spain (GRID:grid.411443.7) (ISNI:0000 0004 1765 7340)
47 UCI Hospital Verge de la Cinta, Tortosa, Spain (GRID:grid.490132.d)
48 UCI Hospital del Mar, Barcelona, Spain (GRID:grid.411142.3) (ISNI:0000 0004 1767 8811)
49 UCI Hospital Mutua de Terrasa, Terrasa, Spain (GRID:grid.411142.3)
50 UCI Hospital Sant Joan, Reus, Spain (GRID:grid.411136.0) (ISNI:0000 0004 1765 529X)
51 UCI Hospital Parc Tauli, Sabadell, Spain (GRID:grid.414560.2) (ISNI:0000 0004 0506 7757)
52 UCI Hospital Universitario Marqués de Valdecillas, Santander, Spain (GRID:grid.414560.2)
53 UCI Hospital Universitario de Guadalajara, Guadalajara, Spain (GRID:grid.411098.5) (ISNI:0000 0004 1767 639X)
54 UCI Hospital Nuestra Señora del Prado, Toledo, Spain (GRID:grid.477416.7)
55 UCI Hospital Virgen de la Concha, Zamora, Spain (GRID:grid.413506.5) (ISNI:0000 0000 9961 7465)
56 UCI Complejo Asistencial de Segovia, Segovia, Spain (GRID:grid.413506.5)
57 UCI Hospital universitario de Burgos, Burgos, Spain (GRID:grid.459669.1) (ISNI:0000 0004 1771 1036)
58 UCI Hospital Clínica de Salamanca, Salamanca, Spain (GRID:grid.459669.1)
59 UCI Hospital Universitario de Ceuta, Ceuta, Spain (GRID:grid.459669.1)
60 UCI Hospital San Pedro de Alcántara, Cáceres, Spain (GRID:grid.413393.f) (ISNI:0000 0004 1771 1124)
61 UCI Hospital de Mérida, Mérida, Spain (GRID:grid.413393.f)
62 UCI Hospital Montecelo, Pontevedra, Spain (GRID:grid.414863.c) (ISNI:0000 0000 9921 6370)
63 UCI CHUAC A Coruña, A Coruña, Spain (GRID:grid.414863.c)
64 UCI Centro Hospital Universitario de Ferrol, Ferrol, Spain (GRID:grid.414863.c)
65 UCI Hospitalario Clínico Universitario de Santiago, Santiago de Compostela, Spain (GRID:grid.11794.3a) (ISNI:0000000109410645)
66 UCI Hospital Lucus Augusti, Lugo, Spain (GRID:grid.414792.d) (ISNI:0000 0004 0579 2350)
67 UCI IFEMA, Madrid, Spain (GRID:grid.414792.d)
68 UCI Hospital Príncipe de Asturias, Madrid, Spain (GRID:grid.411336.2) (ISNI:0000 0004 1765 5855)
69 UCI Hospital de la Princesa, Madrid, Spain (GRID:grid.411251.2) (ISNI:0000 0004 1767 647X)
70 UCI Hospital Clinico San Carlos, Madrid, Spain (GRID:grid.411068.a) (ISNI:0000 0001 0671 5785)
71 UCI Hospital HLA la Moncloa, Madrid, Spain (GRID:grid.411068.a)
72 UCI Hospital Morales Meseguer, Murcia, Spain (GRID:grid.411101.4) (ISNI:0000 0004 1765 5898)
73 UCI Hospital Clínico Universitario Virgen de la Arrixaca, Murcia, Spain (GRID:grid.411372.2) (ISNI:0000 0001 0534 3000)
74 UCI Hospital Reina Sofía, Murcia, Spain (GRID:grid.411089.5) (ISNI:0000 0004 1768 5165)
75 UCI Hospital Santa Lucía, Cartagena, Spain (GRID:grid.411089.5)
76 UCI Hospital Rafael Méndez, Lorca, Spain (GRID:grid.490171.a) (ISNI:0000 0004 1793 8687)
77 UCI Hospital Reina Sofía, Tudela, Spain (GRID:grid.411349.a) (ISNI:0000 0004 1771 4667)
78 UCI Hospital García Orcoyen, Estella‐Lizarra, Spain (GRID:grid.411349.a)
79 UCI Hospital Universitario de Donostia, Donostia, Spain (GRID:grid.414651.3) (ISNI:0000 0000 9920 5292)
80 UCI Hospital Universitario de La Ribera, Alzira, Spain (GRID:grid.440284.e) (ISNI:0000 0005 0602 4350)
81 UCI Hospital Dr. Peset, Valencia, Spain (GRID:grid.411289.7) (ISNI:0000 0004 1770 9825)
82 UCI Hospital Universitari i Politècnic La Fe, Valencia, Spain (GRID:grid.84393.35) (ISNI:0000 0001 0360 9602)
83 UCI Hospital Clínico Universitario de Valencia, Valencia, Spain (GRID:grid.411308.f)
84 UCI Hospital Virgen de los Lirios de Alcoy, Alicante, Spain (GRID:grid.413522.3) (ISNI:0000 0000 9189 6148)
85 UCI Hospital Arnau de Vilanova, Valencia, Spain (GRID:grid.413937.b) (ISNI:0000 0004 1770 9606)
86 UCI Hospital Comarcal de Vinarós, Vinarós, Spain (GRID:grid.413937.b)
87 ICU Hospital nostra Señyora de Meritxell, Les Esclades, Spain (GRID:grid.413937.b)
Pages
6553
Publication year
2023
Publication date
2023
e-ISSN
20452322
Source type
Scholarly Journal
Language of publication
English
ProQuest document ID
2804153187
Copyright
© The Author(s) 2023. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.