January 19, 2023
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Key factors associated with pulmonary sequelae in the follow-up of critically ill COVID-19 patients

Publicated to:Archivos De Bronconeumologia. 59 (4): 205-215 - 2023-04-01 59(4), DOI: 10.1016/j.arbres.2022.12.017

Authors: Gonzalez, Jessica; de Batlle, Jordi; Benitez, Ivan D; Torres, Gerard; Santisteve, Sally; Targa, Adriano D S; Gort-Paniello, Clara; Moncusi-Moix, Anna; Aguila, Maria; Seck, Fatty; Ceccato, Adrian; Ferrer, Ricard; Motos, Anna; Riera, Jordi; Fernandez, Laia; Menendez, Rosario; Lorente, Jose Angel; Penuelas, Oscar; Garcia-Gasulla, Dario; Penasco, Yhivian; Ricart, Pilar; Palomares, Elena Abril; Aguilera, Luciano; Rodriguez, Alejandro; Varela, Maria Victoria Boado; Betere, Belen; Pozo-Laderas, Juan Carlos; Sole-Violan, Jordi; Salvador-Adell, Inmaculada; Novo, Mariana Andrea; Villar, Rosario Amaya; Garnacho-Montero, Jose; Gomez, Jose M; Ortiz, Aaron Blandino; Lomas, Luis Tamayo; Ubeda, Alejandro; Catalan-Gonzalez, Mercedes; Sanchez-Miralles, Angel; Varela, Ignacio Martinez; Garcia, Ruth Noemi Jorge; Franco, Nieves; Gumucio-Sanguino, Victor D; Bustamante-Munguira, Elena; Valdivia, Luis Jorge; Caballero, Jesus; Gallego, Elena; Rodriguez, Covadonga; Castellanos-Ortega, Alvaro; Trenado, Josep; Marin-Corral, Judith; Albaiceta, Guillermo M; de la Torre, Maria del Carmen; Loza-Vazquez, Ana; Vidal, Pablo; Anon, Jose M; Perez, Cristina Carbajales; Sagredo, Victor; Carbonell, Nieves; Socias, Lorenzo; Barbera, Carme; Estella, Angel; Diaz, Emili; de Gonzalo-Calvo, David; Torres, Antoni; Barbe, Ferran

Affiliations

Barcelona Supercomputing Center (BSC), Barcelona, Spain. - Author
BSC, Barcelona, Spain - Author
CIBER of Respiratory Diseases (CIBERES), Institute of Health Carlos III, Madrid, Spain - Author
CIBER of Respiratory Diseases (CIBERES), Institute of Health Carlos III, Madrid, Spain. - Author
Complexo Hosp Univ Ourense, Orense, Spain - Author
Critical Care Center, ParcTaulí Hospital Universitari, Institut d'Investigació i Innovació Parc Taulí I3PT, Sabadell, Spain. - Author
Critical Care Department, Hospital Joan XXIII, Tarragona, Spain. - Author
Critical Care Department, Hospital Universitari Arnau de Vilanova, IRBLleida, Lleida, Spain. - Author
Critical Care Department, Hospital Universitario Río Hortega de Valladolid, Valladolid, Spain. - Author
Department of Intensive Care Medicine, Hospital Clínico Universitario Valladolid, Valladolid, Spain. - Author
Hosp Alvaro Cunqueiro, Intens Care Unit, Vigo, Spain - Author
Hosp Arnau Vilanova, IRBLleida, Crit Care Dept, Lleida, Spain - Author
Hosp Clin & Univ Valencia, Intens Care Unit, Valencia, Spain - Author
Hosp Clin Univ Valladolid, Dept Intens Care Med, Valladolid, Spain - Author
Hosp Cruces, Serv Med Intens, Baracaldo, Vizcaya, Spain - Author
Hosp del Mar IMIM, Crit Care Dept, Barcelona, Spain - Author
Hosp Gen Univ Gregorio Maranon, Madrid, Spain - Author
Hosp Joan 23, Crit Care Dept, Tarragona, Spain - Author
Hosp Mataro Barcelona, Barcelona, Spain - Author
Hosp Nuestra Senora Gracia, Intens Care Dept, Zaragoza, Spain - Author
Hosp Punta Europa, Serv Med Intens, Algeciras, Spain - Author
Hosp Santa Maria, IRBLleida, Lleida, Spain - Author
Hosp Son Llatzer, Intens Care Unit, Palma De Mallorca, Illes Balears, Spain - Author
Hosp St Joan Alacant, Alacant, Spain - Author
Hosp Univ & Politecn La Fe, Serv Med Intens, Valencia, Spain - Author
Hosp Univ 12 Octubre, Dept Intens Care Med, Madrid, Spain - Author
Hosp Univ Basurto, Serv Anestesiol & Reanimac, Bilbao, Spain - Author
Hosp Univ Bellvitge, Dept Intens Care, Bellvitge Biomed Res Inst IDIBELL, Barcelona, Spain - Author
Hosp Univ Germans Trias, Serv Med Intens, Badalona, Spain - Author
Hosp Univ Getafe, Madrid, Spain - Author
Hosp Univ Infanta Leonor, Madrid, Spain - Author
Hosp Univ La Paz, Serv Med Intens, IdiPAZ, Madrid, Spain - Author
Hosp Univ Leon, Leon, Spain - Author
Hosp Univ Lucus Augusti, Crit Care Dept, Lugo, Spain - Author
Hosp Univ Marques Valdecilla, Serv Med Intens, Santander, Spain - Author
Hosp Univ Mostoles, Madrid, Spain - Author
Hosp Univ Mutua Terrassa, Serv Med Intens, Barcelona, Spain - Author
Hosp Univ Principe Asturias, Serv Anal Clin, Alcala De Henares, Spain - Author
Hosp Univ Ramon & Cajal, Serv Med Intens, Madrid, Spain - Author
Hosp Univ Reina Sofia, UGC Med Intens, Inst Maimonides IMIBIC, Cordoba, Spain - Author
Hosp Univ Rio Hortega Valladolid, Crit Care Dept, Valladolid, Spain - Author
Hosp Univ Salamanca, Salamanca, Spain - Author
Hosp Univ San Pedro Alcantara, Unidad Cuidados Intens, Caceres, Spain - Author
Hosp Univ Son Espases, Serv Med Intens, Palma De Mallorca, Illes Balears, Spain - Author
Hosp Univ Torrejon, Madrid, Spain - Author
Hosp Univ Virgen de Valme, Unidad Med Intens, Seville, Spain - Author
Hosp Univ Virgen del Rocio, Intens Care Clin Unit, Seville, Spain - Author
Hosp Univ Virgen Macarena, Intens Care Clin Unit, Seville, Spain - Author
Hosp Verge Cinta, Tarragona, Spain - Author
Hospital General Universitario Gregorio Maranon, Madrid, Spain. - Author
Hospital Universitario de Getafe, Madrid, Spain. - Author
Hospital Universitario de León, León, Spain. - Author
Hospital Universitario de Móstoles, Madrid, Spain. - Author
Hospital Universitario HM Montepríncipe, Universidad San Pablo-CEU, Madrid, Spain. - Author
Inst Hlth Carlos III, CIBER Resp Dis CIBERES, Madrid, Spain - Author
Intensive Care Clinical Unit, Hospital Universitario Virgen de Rocío, Sevilla, Spain. - Author
Intensive Care Department, Vall d'Hebron Hospital Universitari, SODIR Research Group, Vall d'Hebron Institut de Recerca (VHIR), Barcelona, Spain. - Author
Malalties metabòliques hereditàries i malalties musculars. Institut d'Investigacions Biomèdiques August Pi i Sunyer - Author
Mecanismes fisiopatològics de les malalties respiratòries. Institut d'Investigacions Biomèdiques August Pi i Sunyer - Author
ParcTauli Hosp Univ, I3PT, Crit Care Ctr, Sabadell, Spain - Author
Pulmonology Service, University and Polytechnic Hospital La Fe, Valencia, Spain. - Author
Servei de Medicina Intensiva, Hospital Universitari Germans Trias, Badalona, Spain. - Author
Servei de Medicina Intensiva, Hospital Universitari Son Espases, Palma de Mallorca, Illes Balears, Spain. - Author
Servicio de Medicina Intensiva, Hospital Universitario Marqués de Valdecilla, Santander, Spain. - Author
Servicio de Medicina Intensiva, Hospital Universitario Ramón y Cajal, Madrid, Spain. - Author
Translational Research in Respiratory Medicine, University Hospital Arnau de Vilanova and Santa Maria, IRBLleida, Lleida, Spain - Author
Translational Research in Respiratory Medicine, University Hospital Arnau de Vilanova and Santa Maria, IRBLleida, Lleida, Spain. - Author
UAB, Dept Med, Crit Care Dept, Corp Sanitaria Parc Tauli, Barcelona, Spain - Author
Univ & Polytech Hosp La Fe, Pulmonol Serv, Valencia, Spain - Author
Univ Barcelona, Hosp Clin Barcelona, August Pi & Sunyer Biomed Res Inst IDIBAPS, Dept Pneumol, Barcelona, Spain - Author
Univ Cadiz, Univ Hosp Jerez, Intens Care Unit, INiBICA,Med Dept, Cadiz, Spain - Author
Univ Fernando Pessoa, Hosp Dr Negrin Gran Canaria, Crit Care Dept, Gran Canaria, Canarias, Spain - Author
Univ Hosp Arnau de Vilanova & Santa Maria, IRBLleida, Translat Res Resp Med, Lleida, Spain - Author
Univ Oviedo, Inst Univ Oncol Principado Asturias, Inst Invest Sanitaria Principado Asturias, Dept Biol Func,Hosp Cent Asturias, Oviedo, Spain - Author
Univ San Pablo CEU, Hosp Univ HM Monteprincipe, Madrid, Spain - Author
Vall dHebron Hosp Univ, Vall dHebron Inst Recerca VHIR, Intens Care Dept, SODIR Res Grp, Barcelona, Spain - Author
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Abstract

Critical COVID-19 survivors have a high risk of respiratory sequelae. Therefore, we aimed to identify key factors associated with altered lung function and CT scan abnormalities at a follow-up visit in a cohort of critical COVID-19 survivors.Multicenter ambispective observational study in 52 Spanish intensive care units. Up to 1327 PCR-confirmed critical COVID-19 patients had sociodemographic, anthropometric, comorbidity and lifestyle characteristics collected at hospital admission; clinical and biological parameters throughout hospital stay; and, lung function and CT scan at a follow-up visit.The median [p25-p75] time from discharge to follow-up was 3.57 [2.77-4.92] months. Median age was 60 [53-67] years, 27.8% women. The mean (SD) percentage of predicted diffusing lung capacity for carbon monoxide (DLCO) at follow-up was 72.02 (18.33)% predicted, with 66% of patients having DLCO<80% and 24% having DLCO<60%. CT scan showed persistent pulmonary infiltrates, fibrotic lesions, and emphysema in 33%, 25% and 6% of patients, respectively. Key variables associated with DLCO<60% were chronic lung disease (CLD) (OR: 1.86 (1.18-2.92)), duration of invasive mechanical ventilation (IMV) (OR: 1.56 (1.37-1.77)), age (OR [per-1-SD] (95%CI): 1.39 (1.18-1.63)), urea (OR: 1.16 (0.97-1.39)) and estimated glomerular filtration rate at ICU admission (OR: 0.88 (0.73-1.06)). Bacterial pneumonia (1.62 (1.11-2.35)) and duration of ventilation (NIMV (1.23 (1.06-1.42), IMV (1.21 (1.01-1.45)) and prone positioning (1.17 (0.98-1.39)) were associated with fibrotic lesions.Age and CLD, reflecting patients' baseline vulnerability, and markers of COVID-19 severity, such as duration of IMV and renal failure, were key factors associated with impaired DLCO and CT abnormalities.Published by Elsevier España, S.L.U.

Keywords

AdultAgedArticleArtificial ventilationBacterial pneumoniaBlood gas analysisCarbon monoxideChronic lung diseaseChronic obstructive lung diseaseComputed tomographic angiographyCoronavirus disease 2019Covid-19CreatinineCritical illnessCritically ill patientCt abnormalitiesDiffusing capacity for carbon monoxideDisease progressionEmphysemaEstimated glomerular filtration rateFemaleFollow-up studiesForced expiratory volumeGastrointestinal hemorrhageGlomerulus filtration rateHospital admissionHospitalizationHumanHumansHydroxychloroquineHypertensionIcuImmune responseIntensive care unitInvasive ventilationKidney failureLungLung complicationLung diffusion capacityLung functionLung function testLung infiltrateMajor clinical studyMaleMiddle agedMulticenter studyNoninvasive ventilationObesityObservational studyPalliative therapyPlatelet countPolymerase chain reactionPulmonary emphysemaSensitivity analysisSequelaeSpirometrySurvivorUreaVulnerabilityX-ray computed tomography

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal Archivos De Bronconeumologia due to its progression and the good impact it has achieved in recent years, according to the agency WoS (JCR), it has become a reference in its field. In the year of publication of the work, 2023, it was in position 9/101, thus managing to position itself as a Q1 (Primer Cuartil), in the category Respiratory System. Notably, the journal is positioned above the 90th percentile.

From a relative perspective, and based on the normalized impact indicator calculated from the Field Citation Ratio (FCR) of the Dimensions source, it yields a value of: 4.83, which indicates that, compared to works in the same discipline and in the same year of publication, it ranks as a work cited above average. (source consulted: Dimensions Jul 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-07-07, the following number of citations:

  • WoS: 4
  • Scopus: 4
  • Europe PMC: 2

Impact and social visibility

From the perspective of influence or social adoption, and based on metrics associated with mentions and interactions provided by agencies specializing in calculating the so-called "Alternative or Social Metrics," we can highlight as of 2025-07-07:

  • The use, from an academic perspective evidenced by the Altmetric agency indicator referring to aggregations made by the personal bibliographic manager Mendeley, gives us a total of: 41.
  • The use of this contribution in bookmarks, code forks, additions to favorite lists for recurrent reading, as well as general views, indicates that someone is using the publication as a basis for their current work. This may be a notable indicator of future more formal and academic citations. This claim is supported by the result of the "Capture" indicator, which yields a total of: 44 (PlumX).

With a more dissemination-oriented intent and targeting more general audiences, we can observe other more global scores such as:

  • The Total Score from Altmetric: 9.
  • The number of mentions on the social network Facebook: 1 (Altmetric).
  • The number of mentions on the social network X (formerly Twitter): 5 (Altmetric).