Procalcitonin and C-reactive protein to rule out early bacterial coinfection in COVID-19 critically ill patients

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Cited 14 times in Scopus logo

Cited 17 times in Web of Science logo

Cited 9 times in Europe PMC logo

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Financial support was provided by the Instituto de Salud Carlos III de Madrid (COV20/00110, ISCIII); Fondo Europeo de Desarrollo Regional (FEDER); Una manera de hacer Europa; Centro de Investigacion Biomedica En Red-Enfermedades Respiratorias (CIBERES); and Donation program estar preparados UNESPA, Madrid, Spain. DdGC has received financial support from the Instituto de Salud Carlos III (Miguel Servet 2020: CP20/00041), co-funded by European Social Fund (ESF)/ Investing in your future. Adrian Ceccato acknowledges receiving financial support from Instituto de Salud Carlos III (ISCIII; Sara Borrell 2021: CD21/00087).

Analysis of institutional authors

Badia Jobal, Joan RamonAuthorCastro Revollo, PedroAuthorKiarostami, KasraAuthorAndrea Riba, RutAuthorGracia Lopez, Maria Del CarmenAuthorCilloniz Campos, CatiaAuthorSanchez Sanchez, MiguelAuthorCastella Pericas, ManelAuthorMotos AAuthorFernández-Barat LCorresponding AuthorBarbeta EAuthorGabarrús AAuthorCeccato AAuthorPalomeque AAuthorDiaz EAuthorTorres Marti, AntoniCorresponding Author

July 31, 2023

Publications

Article

Publicated to:Intensive Care Medicine. 49 (8): 934-945 - 2023-08-01 49(8), DOI: 10.1007/s00134-023-07161-1

Authors: Galli, Flavia; Bindo, Francesco; Motos, Anna; Fernandez-Barat, Laia; Barbeta, Enric; Gabarrus, Albert; Ceccato, Adrian; Bermejo-Martin, Jesus F; Ferrer, Ricard; Riera, Jordi; Penuelas, Oscar; Lorente, Jose Angel; de Gonzalo-Calvo, David; Menendez, Rosario; Gonzalez, Jessica; Misuraca, Sofia; Palomeque, Andrea; Amaya-Villar, Rosario; Anon, Jose Manuel; Balan Marino, Ana; Barbera, Carme; Barberan, Jose; Blandino Ortiz, Aaron; Bustamante-Munguira, Elena; Caballero, Jesus; Canton-Bulnes, Maria Luisa; Carbajales Perez, Cristina; Carbonell, Nieves; Catalan-Gonzalez, Mercedes; de Frutos, Raul; Franco, Nieves; Galban, Cristobal; Lopez Lago, Ana; Gumucio-Sanguino, Victor D; de la Torre, Maria del Carmen; Diaz, Emilio; Estella, Angel; Gallego Curto, Elena; Garcia-Garmendia, Jose Luis; Gomez, Jose Manuel; Huerta, Arturo; Jorge Garcia, Ruth Noemi; Loza-Vazquez, Ana; Marin-Corral, Judith; Martin Delgado, Maria Cruz; Martinez de la Gandara, Amalia; Martinez Varela, Ignacio; Lopez Messa, Juan; M Albaiceta, Guillermo; Nieto, Maria Teresa; Novo, Mariana Andrea; Penasco, Yhivian; Perez-Garcia, Felipe; Pozo-Laderas, Juan Carlos; Ricart, Pilar; Sagredo, Victor; Sanchez-Miralles, Angel; Sancho Chinesta, Susana; Roche-Campo, Ferran; Socias, Lorenzo; Sole-Violan, Jordi; Suarez-Sipmann, Fernando; Tamayo Lomas, Luis; Trenado, Jose; Ubeda, Alejandro; Valdivia, Luis Jorge; Vidal, Pablo; Boado, Maria Victoria; Rodriguez, Alejandro; Antonelli, Massimo; Blasi, Francesco; Barbe, Ferran; Torres, Antoni

Affiliations

August Pi i Sunyer Biomedical Research Institute-IDIBAPS, University of Barcelona, Barcelona, Spain. - Author

August Pi i Sunyer Biomedical Research Institute-IDIBAPS, University of Barcelona, Barcelona, Spain. lfernan1@recerca.clinic.cat. - Author

CIBER de Enfermedades Respiratorias (CIBERes), Instituto de Salud Carlos III, Madrid, Spain. - Author

CIBER de Enfermedades Respiratorias (CIBERES), Instituto de Salud Carlos III, Madrid, Spain. lfernan1@recerca.clinic.cat. - Author

Clin Sagrada Familia, Pulm & Crit Care Div, Emergency Dept, Barcelona, Spain - Author

Complejo Asistencial Univ Palencia, Palencia 47, Spain - Author

Complejo Hosp Univ Santiago, Dept Crit Care Med, CHUS, Santiago, Spain - Author

Complexo Hosp Univ Ourense, Orense, Spain - Author

Critical Care Center, Institut d'Investigació i Innovació Parc Taulí I3PT, Parc Taulí Hospital Universitari, Sabadell, Spain. - Author

Critical Intensive Medicine Department, Hospital Universitari Arnau de Vilanova de Lleida, IRBLleida, Lleida, Spain. - Author

Department of Critical Care Medicine, CHUS, Complejo Hospitalario Universitario de Santiago, Santiago, Spain. - Author

Department of Intensive Care Medicine, Hospital Clínico Universitario Valladolid, Valladolid, Spain. - Author

Department of Intensive Care Medicine, Hospital Universitario 12 de Octubre, Madrid, Spain. - Author

Department of Intensive Care, Emergency Medicine and Anesthesia, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy. - Author

Department of Intensive Care, Hospital Universitari de Bellvitge, Bellvitge Biomedical Research Institute (IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain. - Author

Department of Medicine, Critical Care Department, Corporació Sanitària Parc Taulí, Universitat Autònoma de Barcelona (UAB), Sabadell, Barcelona, Spain. - Author

Department of Medicine, Intensive Care Unit University Hospital of Jerez, University of Cádiz, INIBiCA, Cádiz, Spain. - Author

Department of Pathophysiology and Transplantation, Università degli Studi di Milano, Milan, Italy. - Author

Department of Pneumology, Hospital Clinic of Barcelona - Author

Dept. of Bioengineering, Universidad Carlos III, Madrid, Spain. - Author

Fdn IRCCS Ca Granda Osped Maggiore Policlin, Resp Unit & Cyst Fibrosis Adult Ctr, Milan, Italy - Author

Fdn Policlin Univ A Gemelli IRCCS, Dept Intens Care Emergency Med & Anesthesia, Rome, Italy - Author

Group for Biomedical Research in Sepsis (BioSepsis), Instituto de Investigación Biomédica de Salamanca (IBSAL), Paseo de San Vicente, Salamanca, Spain. - Author

Hosp Alvaro Cunqueiro, Intens Care Unit, Vigo, Spain - Author

Hosp Clin Barcelona, Dept Pulm Med, C-Villarroel 170, Barcelona 08036, Spain - Author

Hosp Clin Univ, Intens Care Unit, Valencia, Spain - Author

Hosp Clinico Univ Valladolid, Dept Intens Care Med, Valladolid, Spain - Author

Hosp Gen Segovia, Segovia, Spain - Author

Hosp Gen Univ Gregorio Maranon, Madrid, Spain - Author

Hosp Mar IMIM, Crit Care Dept, Barcelona, Spain - Author

Hosp Mataro Barcelona, Barcelona, Spain - Author

Hosp Nuestra Senora Gracia, Dept Intens Care, Zaragoza, Spain - Author

Hosp Punta Europa, Serv Med Intens, Algeciras, Spain - Author

Hosp San Juan Dios Aljarafe, Intens Care Unit, Seville, Spain - Author

Hosp Santa Maria, IRBLleida, Lleida, Spain - Author

Hosp Son Llatzer, Intens Care Unit, Palma De Mallorca, Spain - Author

Hosp Univ 12 Octubre, Dept Intens Care Med, Madrid, Spain - Author

Hosp Univ Aranu Vilanova & Santa Maria, IRBLleida, Resp Dept, Translat Res Resp Med, Lleida, Spain - Author

Hosp Univ Arnau Vilanova Lleida, Crit Intens Med Dept, IRBLleida, Lleida, Spain - Author

Hosp Univ Basurto, Serv Anestesiol Reanimac, Bilbao, Spain - Author

Hosp Univ Bellvitge, Bellvitge Biomed Res Inst IDIBELL, Dept Intens Care, Lhospitalet De Llobregat, Spain - Author

Hosp Univ Cruces, Baracaldo, Spain - Author

Hosp Univ Germans Trias, Serv Med Intens, Badalona, Spain - Author

Hosp Univ Infanta Leonor, Dept Intens Med, Madrid, Spain - Author

Hosp Univ La Paz, Serv Med Intensiva, 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 Politecn La Fe, Serv Med Intens, Valencia, Spain - Author

Hosp Univ Princesa, Intens Care Unit, Madrid, Spain - Author

Hosp Univ Ramon & Cajal, Serv Med Intens, Madrid, Spain - Author

Hosp Univ Rio Hortega Valladolid, Crit Care Dept, Valladolid, Spain - Author

Hosp Univ Rio Hortega Valladolid, Valladolid, Spain - Author

Hosp Univ Sagrat Cor, Intens Care Unit, Grp Quironsalud, Barcelona, Spain - Author

Hosp Univ Salamanca, Salamanca, Spain - Author

Hosp Univ San Pedro Alcantara, Unidad Cuidados Intensivos, Caceres, Spain - Author

Hosp Univ Sant Joan dAlacant, Intens Care Unit, Alicante, Spain - Author

Hosp Univ Son Espases, Serv Med Intens, Palma De Mallorca, Spain - Author

Hosp Univ Vall Hebron, Vall Hebron Inst Recerca, Dept Intens Care, Barcelona, Spain - Author

Hosp Univ Virgen Macarena, Intens Care Clin Unit, Seville, Spain - Author

Hosp Univ Virgen Rocio, Intens Care Clin Unit, Seville, Spain - Author

Hosp Univ Virgen Valme, Unidad Med Intens, Seville, Spain - Author

Hosp Verge Cinta, Inst Invest Sanitaria Pere Virgili IISPV, Tarragona, Spain - Author

Hospital de Mataró de Barcelona, Barcelona, Spain. - Author

Hospital Santa Maria, IRBLleida, Lleida, Spain. - Author

Hospital Universitario de Getafe, Universidad Europea, Madrid, Spain. - Author

Hospital Universitario de Móstoles, Madrid, Spain. - Author

Hospital Universitario HM Montepríncipe, Facultad HM Hospitales de Ciencias de la Salud, Universidad Camilo Jose Cela, Madrid, Spain. - Author

Hospital Universitario Río Hortega de Valladolid, Valladolid, Spain. - Author

Hospital Universitario San Agustín, Asturias, Spain. - Author

Inst Invest Biomed Salamanca IBSAL, Grp Biomed Res Sepsis BioSepsis, Salamanca, Spain - Author

Inst Salud Carlos III, CIBER Enfermedades Respiratorias CIBERES, Madrid, Spain - Author

Inst Salud Carlos III, Ctr Invest Biomed Red Enfermedades Infecciosas CI, Madrid, Spain - Author

Intensive Care Clinical Unit, Hospital Universitario Virgen de Rocío, Seville, Spain. - Author

Intensive Care Clinical Unit, Hospital Universitario Virgen Macarena, Seville, Spain. - Author

Intensive Care Department, Hospital Universitari Vall d'Hebron, Vall d'Hebron Institut de Recerca, Barcelona, Spain. - Author

Intensive Care Unit, and Emergency Medicine, Universidad de Alcalá, Madrid, Spain. - Author

Intensive Care Unit, Grupo Quironsalud, Hospital Universitari Sagrat Cor, Barcelona, Spain. - Author

Intensive Care Unit, Hospital Álvaro Cunqueiro, Vigo, Spain. - Author

Intensive Care Unit, Hospital Clínico Universitario, Valencia, Spain. - Author

Malalties metabòliques hereditàries i malalties musculars. Institut d'Investigacions Biomèdiques August Pi i Sunyer - Author

Parc Tauli Hosp Univ, Inst Invest Innovacio Parc Tauli I3PT, Crit Care Ctr, Sabadell, Spain - Author

Pulmonary Department, University and Polytechnic Hospital La Fe, Valencia, Spain. - Author

Respiratory Unit and Cystic Fibrosis Adult Center, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy. - Author

Rovira & Virgili Univ, CIBERES, Crit Care Dept, Hosp Univ Joan 23, Tarragona, Spain - Author

Servicio de Anestesiología y Reanimación, Hospital Universitario Basurto, Bilbao, Spain. - Author

Servicio de Medicina Intensiva, Hospital Universitario La Paz, IdiPAZ, Madrid, Spain. - Author

Servicio de Medicina Intensiva, Hospital Universitario Ramón y Cajal, Madrid, Spain. - Author

Spain Hosp Univ San Agustin, Asturias, Spain - Author

Translational Research in Respiratory Medicine, Respiratory Department, Hospital Universitari Aranu de Vilanova and Santa Maria, IRBLleida, Lleida, Spain. - Author

UGC Med Intens, Inst Maimonides IMIBIC, Hosp Univ Reina Sofia, Cordoba, Spain - Author

Unidad de Cuidados Intensivos, Hospital Universitario San Pedro de Alcántara, Cáceres, Spain. - Author

Univ & Polytechn Hosp La Fe, Dept Pulm, Valencia, Spain - Author

Univ Alcala, Fac Med, Dept Biomed Biotecnol, Serv Microbiol Clin,Hosp Univ Principe Asturias, Alcala De Henares, Spain - Author

Univ Alcala, Intens Care Unit & Emergency Med, Madrid, Spain - Author

Univ Autonoma Barcelona UAB, Corporacio Sanitaria Parc Tauli, Crit Care Dept, Dept Med, Barcelona, Spain - Author

Univ Barcelona, Hosp Clin Barcelona August Pi Sunyer Biomed Res I, Dept Pneumol, Barcelona, Spain - Author

Univ Cadiz, Dept Med, Intens Care Unit, INIBiCA,Univ Hosp Jerez, Cadiz, Spain - Author

Univ Camilo Jose Cela, Hosp Univ HM Monteprincipe, Fac HM Hosp Ciencias Salud, Madrid, Spain - Author

Univ Carlos III, Dept Bioengn, Madrid, Spain - Author

Univ Cattolica Sacro Cuore, Rome, Italy - Author

Univ Europea, Hosp Univ Getafe, Madrid, Spain - Author

Univ Fernando Pessoa Canarias, Hosp Univ GC Dr Negrin, Crit Care Dept, Gran Canaria, Spain - Author

Univ Francisco Vitoria, Hosp Univ Torrejon, Madrid, Spain - Author

Univ Milan, Dept Pathophysiol & Transplantat, Milan, Italy - Author

Univ Oviedo, Inst Univ Oncol Principado Asturias, Inst Invest Sanitaria Principado Asturias, Hosp Cent Asturias,Dept Biol Func, Oviedo, Spain - Author

Università Cattolica del Sacro Cuore, Rome, Italy. - Author

Abstract

Although the prevalence of community-acquired respiratory bacterial coinfection upon hospital admission in patients with coronavirus disease 2019 (COVID-19) has been reported to be < 5%, almost three-quarters of patients received antibiotics. We aim to investigate whether procalcitonin (PCT) or C-reactive protein (CRP) upon admission could be helpful biomarkers to identify bacterial coinfection among patients with COVID-19 pneumonia.We carried out a multicentre, observational cohort study including consecutive COVID-19 patients admitted to 55 Spanish intensive care units (ICUs). The primary outcome was to explore whether PCT or CRP serum levels upon hospital admission could predict bacterial coinfection among patients with COVID-19 pneumonia. The secondary outcome was the evaluation of their association with mortality. We also conducted subgroups analyses in higher risk profile populations.Between 5 February 2020 and 21 December 2021, 4076 patients were included, 133 (3%) of whom presented bacterial coinfection. PCT and CRP had low area under curve (AUC) scores at the receiver operating characteristic (ROC) curve analysis [0.57 (95% confidence interval (CI) 0.51-0.61) and 0.6 (95% CI, 0.55-0.64), respectively], but high negative predictive values (NPV) [97.5% (95% CI 96.5-98.5) and 98.2% (95% CI 97.5-98.9) for PCT and CRP, respectively]. CRP alone was associated with bacterial coinfection (OR 2, 95% CI 1.25-3.19; p = 0.004). The overall 15, 30 and 90 days mortality had a higher trend in the bacterial coinfection group, but without significant difference. PCT ≥ 0.12 ng/mL was associated with higher 90 days mortality.Our study suggests that measurements of PCT and CRP, alone and at a single time point, are not useful for ruling in or out bacterial coinfection in viral pneumonia by COVID-19.© 2023. The Author(s).

Keywords

adultsbacterial coinfectionc-reactive proteincovid-19critically illdecisiondiagnosisetiologyinfectionintensive caremortalitysepsisserum procalcitoninstatistics notesAdultAgedAntibiotic agentArea under the curveArticleBacterial coinfectionBacterial infectionBiological markerBiomarkersC reactive proteinC-reactive proteinCalcitoninCohort analysisCoinfectionCommunity-acquired pneumoniaComplicationControlled studyCoronavirus disease 2019CorticosteroidCovid-19Critical illnessCritically illCritically ill patientDiagnostic test accuracy studyFemaleHospital admissionHumanHumansIntensive careMajor clinical studyMaleMetabolismMortalityMortality rateObservational studyPredictive valueProcalcitoninProtein blood levelReceiver operating characteristicRetrospective studiesRetrospective studyRoc curveSensitivity and specificity

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal Intensive Care Medicine 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 2/55, thus managing to position itself as a Q1 (Primer Cuartil), in the category Critical Care Medicine. Notably, the journal is positioned above the 90th percentile.

From a relative perspective, and based on the normalized impact indicator calculated from World Citations provided by WoS (ESI, Clarivate), it yields a value for the citation normalization relative to the expected citation rate of: 3.4. This 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: ESI Nov 14, 2024)

This information is reinforced by other indicators of the same type, which, although dynamic over time and dependent on the set of average global citations at the time of their calculation, consistently position the work at some point among the top 50% most cited in its field:

Weighted Average of Normalized Impact by the Scopus agency: 3.11 (source consulted: FECYT Feb 2024)
Field Citation Ratio (FCR) from Dimensions: 18.67 (source consulted: Dimensions Jul 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-07-04, the following number of citations:

WoS: 17
Scopus: 14
Europe PMC: 9

Impact and social visibility

Leadership analysis of institutional authors

This work has been carried out with international collaboration, specifically with researchers from: Italy.

There is a significant leadership presence as some of the institution’s authors appear as the first or last signer, detailed as follows: Last Author (Torres Martí, Antoni).