Atrial fibrillation and associated comorbidities pose a risk factor for mortality, morbidity and development of complications in patients admitted for COVID-19.
ObjectivesTo describe the clinical, epidemiological, radiological and analytical characteristics of patients with AF admitted for COVID-19 in Spain. Secondarily, we aim to identify those variables associated with mortality and poor prognosis of COVID-19 in patients with AF.
MethodsRetrospective, observational, multicenter, nationwide, retrospective study of patients hospitalized for COVID-19 from March 1 to October 1, 2020. Data were obtained from the SEMI-COVID-19 Registry of the Spanish Society of Internal Medicine (SEMI) in which 150 Spanish hospitals participate.
ResultsBetween March 1 and October 1, 2020, data from a total of 16,461 patients were entered into the SEMI-COVID-19 registry. 1,816 (11%) had a history of AF and the number of deaths among AF patients amounted to 738 (41%). Regarding clinical characteristics, deceased patients were admitted with a higher heart rate (88.38 vs 84.95; p > 0.01), with a higher percentage of respiratory failure (67.2% vs 20.1%; p < 0.01) and high tachypnea (58% vs 30%; p < 0.01). The comorbidities that presented statistically significant differences in the deceased group were: age, hypertension and diabetes with target organ involvement. There was also a higher prevalence of a history of cardiovascular disease in the deceased. On multivariate analysis, DOACs treatment had a protective role for mortality (OR:0,597) IC (0,402-0,888 ; p = 0.011).
ConclusionsPrevious treatment with DOACs and DOACs treatment during admission seem to have a protective role in patients with AF, although this fact should be verified in prospective studies.
La fibrilación auricular y las comorbilidades asociadas a ella suponen un factor de riesgo de mortalidad, morbilidad y desarrollo de complicaciones en los pacientes ingresados por COVID-19.
ObjetivosDescribir las características clínicas, epidemiológicas, radiológicas y analíticas de los pacientes con FA ingresados por COVID-19 en España. De forma secundaria, se pretende identificar aquellas variables que se asocian con mortalidad y mal pronóstico de la COVID-19 en pacientes que presentan FA.
MétodosEstudio retrospectivo, observacional y multicéntrico de ámbito nacional de pacientes hospitalizados por COVID-19 desde el 1 de marzo al 1 de octubre de 2020. Los datos fueron obtenidos del Registro SEMI-COVID-19 de la Sociedad Española de Medicina Interna (SEMI) en el que participan 150 hospitales españoles.
ResultadosDe un total de 16.461 pacientes en el registro SEMI-COVID-19, 1.816 (11%) tenían antecedente de FA y el número de fallecidos entre los pacientes con FA ascendió a 738 (41%). En cuanto a la clínica, los pacientes fallecidos ingresaron con una frecuencia cardíaca mayor (88,38 vs 84,95; p > 0,01), con mayor porcentaje de insuficiencia respiratoria (67,2% vs 20,1%; p < 0,01) y mayor taquipnea (58% vs 30%; p < 0,09). En el análisis multivariante, el tratamiento con ACOD tuvo un papel protector para la mortalidad por infección por COVID 19 (OR:0,597; IC (0,402-0,888; p = 0.011)
ConclusionesEl tratamiento previo con ACOD como el tratamiento con ACOD durante el ingreso parecen tener un papel protector en los pacientes con FA, aunque este hecho debería ser comprobado con estudios prospectivos.
New coronavirus 2019 (COVID-19) disease, caused by SARS-CoV-2, has been and remains a challenge for health systems worldwide, given its high contagiousness and morbidity and mortality1. The pandemic caused by COVID-19 has affected more than 290 million people worldwide and has caused more than 5 million deaths as of January 20222. Spain is one of the most affected countries in the world3, with more than 7,164,906 million cases and more than 89,837 deaths since the start of the pandemic2. This has led the Spanish Society of Internal Medicine (SEMI) to create a registry with data on hospitalized patients throughout the country in which more than 150 hospitals have participated.
The magnitude of the pandemic has led to a truly scientific revolution, with studies to describe its clinical characteristics and risk factors, clinical trials to discover effective treatments and the development of vaccines in record time.
Among the risk factors described to date, cardiovascular disease has been associated with increased morbidity and mortality4–7. On the other hand, cardiovascular complications developed during admission in relation to COVID-19 are common and constitute a major cause of mortality8–12.
However, the role of atrial fibrillation (AF) and its management in relation to COVID-19 remains to be determined and not many studies have been published to date.
AF is the most common sustained arrhythmia in the Spanish population, with an overall prevalence of around 4% and over 15% in patients over 80 years of age13–15. It is a risk factor for the development of heart failure, cardioembolic stroke and dementia13,16, all of which have been independently associated with COVID-19 mortality. On the other hand, age, hypertension, diabetes mellitus, obesity and ischaemic heart disease are factors that increase the risk of developing AF and have all been described as poor prognostic factors in COVID-19. Bearing in mind all of the above, given the impact that both diseases independently have on global health and the evident relationship between them, this study aims to describe the clinical, epidemiological, radiological and laboratory characteristics of patients with AF admitted for COVID-19 in Spain.
A second aim is to identify those variables that are associated with mortality and poor prognosis of COVID-19 in patients with AF.
Material and methodsStudy designA nationwide retrospective, observational, multicenter study of patients hospitalized for COVID-19 was conducted from 1 March to 1 October 2020. The data were obtained from the SEMI-COVID-19 Registry, with the participation of 150 Spanish hospitals. The SEMI-COVID-19 registry has consecutively enrolled older patients with microbiologically confirmed COVID-19 disease using a reverse transcription polymerase chain reaction test obtained from a nasopharyngeal, sputum or bronchoalveolar lavage specimen.
For this study, we have selected patients with a history of AF during hospital admission for COVID-19.
VariablesClinical, epidemiological, radiological, laboratory and therapeutic variables were analysed, as well as mortality during admission or early readmission, defined as a new episode of hospital admission within 30 days after discharge. Data were collected retrospectively using an online data capture system. The comorbidity burden of patients was established with the age-adjusted Charlson comorbidity index17. To establish functional status prior to hospital admission, the Barthel index was used18 (independent or mild dependency: 100-91; moderate dependency: 90-61; severe dependency: ≤60). Patients were considered to have hypertension, diabetes mellitus or dyslipidaemia if they had a previous diagnosis in their medical history or were receiving medical treatment for them. Diabetes mellitus was classified into 2 subgroups: with target organ damage (brain, heart, kidney, or retina involvement) or without target organ damage. Chronic lung disease was defined as a previous diagnosis of chronic obstructive pulmonary disease or asthma. Atherosclerotic cardiovascular disease was defined by a previous history of ischemic heart disease (acute myocardial infarction, acute coronary syndrome, angina, or coronary revascularization). Neoplastic disease included all non-metastatic solid tumours (excluding non-melanoma skin tumours). Moderate-severe kidney disease was defined by a glomerular filtration rate below 45 ml/min/1.73 m2 according to the CKD-EPI equation10. Moderate-severe liver disease was defined as grade B or C in the Child-Pugh classification. Obesity was defined by a body mass index ≥ 30 kg/m2. Comorbidities were collected from the medical records of each hospital. Laboratory data (blood count, biochemistry, blood gases, coagulation) and imaging tests were collected on admission. Regarding anticoagulation, baseline anticoagulant treatment was classified into vitamin K antagonists (VKA) and direct oral anticoagulants (DOAC) since the frequency of low molecular weight heparin (LMWH) was negligible. However, 3 groups were differentiated in terms of anticoagulant treatment during admission: VKA, DOAC and LMWH. In-hospital complications included: admission to the intensive care unit, presence of acute respiratory distress syndrome, acute coronary syndrome, arrhythmia, shock, sepsis, acute renal failure, venous thromboembolism and acute arterial ischemia. Ventilatory support included invasive mechanical ventilation, non-invasive mechanical ventilation and high-flow oxygen.
Statistical analysisPatients were divided according to the categorical variable of mortality into deceased or non-deceased. Categorical and continuous variables were expressed as absolute values and percentages and as medians (ranges), respectively. Differences between groups were analysed using the Student's t test or the Mann-Whitney U test for continuous variables or with Pearson's χ2 for categorical variables. A value of p < 0.05 was considered statistically significant. The measure of association was presented as the odds ratio (OR) with a 95% confidence interval (95% CI). Subsequently, a multivariate analysis was performed expressed as adjusted OR, 95% CI. Logistic regression analysis was used to identify independent factors at admission for in-hospital mortality, including those variables with statistical significance in the bivariate analysis and with a percentage of missing values of less than 20%. The statistical analysis was done with the SPSS version 26.0 software (IBM SPSS Statistics ©).
Ethical aspectsAll patients gave their informed consent. This study was conducted in accordance with the Helsinki Declaration and was approved by the Malaga Ethics Committee (Code: SEMI-COVID-19 03-27-20). The STROBE initiative for the publication of observational studies was followed (available at www.strobe-statement.org).
ResultsA total of 16,461 patients were entered into the SEMI-COVID-19 registry between 1 March and 1 October 2020. Of these, 1816 (11%) had a history of AF. A total of 1,799 patients were finally analysed, as 17 were excluded due to lack of basic data for correct aetiology. The number of deaths among patients with AF was 738 (41%). The epidemiological, clinical, laboratory and radiological characteristics are shown in Table 1Table 1. A specific table has been developed for anticoagulation treatment both before and during admission (Table 2Table 2). Table 3Table 3 shows the treatments during admission and the complications. Table 4Table 4 shows the logistic regression.
Epidemiological, clinical, laboratory and radiological characteristics in patients with AF and COVID-19, classified into deceased and not deceased.
| Deceased N = 738 | Not deceased N = 1,061 | p | |
|---|---|---|---|
| Comorbidities | |||
| Age | 83.30 ± 7.83 | 78.14 ± 10.63 | <0.01 |
| Male sex n (%) | 465 (63.2) | 600 (56.6) | <0.01 |
| HBP n (%) | 624 (84.7) | 806 (76.1) | <0.01 |
| Diabetes mellitus n (%) | |||
| Without TO lesion | 136 (18.5) | 207 (19.1) | 0.72 |
| With TO lesion | 113 (15.4) | 99 (9.1) | <0.01 |
| Dyslipidemia n (%) | 419 (56.9) | 565 (53.3) | 0.131 |
| BMI > 30n (%) | 142 (22.0) | 250 (25.6) | 0.103 |
| Charlson index | 2.98 ± 2.37 | 2.08 ± 2.03 | <0.01 |
| Heart failure n (%) | 277 (37.5) | 291 (27.4) | <0.01 |
| AMI n (%) | 115 (15.6) | 120 (11.3) | <0.01 |
| Angina n (%) | 74 (10.1) | 59 (5.6) | <0.01 |
| Stroke n (%) | 100 (13.6) | 105 (9.9) | 0.017 |
| PVD n (%) | 97 (13.2) | 77 (7.3) | <0.01 |
| COPD n (%) | 119 (16.2) | 150 (14.2) | 0.239 |
| Dementia n (%) | 200 (27.1) | 165 (15.6) | <0.01 |
| Clinical, laboratory and radiological characteristics | |||
| HR bpm | 88.38 ± 21.76 | 84.95 ± 18.93 | <0.01 |
| SBP mmHg | 126.5 ± 25.09 | 130.73 ± 23.50 | <0.01 |
| SpO2% | 90.07 ± 7.51 | 93.43 ± 4.64 | <0.01 |
| RR>20 rpm n (%) | 415 (58.0) | 313 (30.0) | <0.01 |
| Dyspnea n (%) | 540 (73.6) | 602 (56.8) | <0.01 |
| Confusion n (%) | 273 (37.1) | 140 (13.3) | <0.01 |
| Creatinine mg/dl | 1.66 ± 1.23 | 1.25 ± 0.93 | <0.01 |
| Glucose (mg/dl) | 150.01 ± 72.46 | 129.57 ± 61.91 | <0.01 |
| CRP (mg/L) | 110.34 ± 97.45 | 76.17 ± 77.02 | <0.01 |
| Ferritin (ng/dl) | 1.093.14 ± 1.386.62 | 691.01 ± 878.44 | <0.01 |
| INR | 2.51 ± 2.53 | 2.41 ± 2.72 | 0.56 |
| D-dimer (ng/dl) | 2.556.6 ± 8.546.71 | 1.409 ± 5.064.883 | <0.01 |
| Bilateral pneumonia n (%) | 385 (53.0) | 488 (46.8) | <0.01 |
| Pleural effusion n (%) | 47 (6.5) | 41 (3.9) | 0.01 |
| Usual treatment n (%) | |||
| ACEI | 219 (29.9) | 221 (20.9) | <0.01 |
| ARBs | 189 (25.9) | 309 (29.2) | 0.129 |
| ASA | 97 (13.3) | 116 (11.0) | 0.135 |
| Statins | 324 (44.6) | 490 (46.4) | 0.456 |
ASA: acetylsalicylic acid; ARBs: angiotensin receptor blockers; COPD: chronic obstructive pulmonary disease; CKD: chronic kidney disease; PVD: peripheral vascular disease; HR: heart rate; RR: respiratory rate; HBP: high blood pressure; AMI: acute myocardial infarction; HF: heart failure; ACEI: angiotensin converting enzyme inhibitors; BMI: body mass index; TO: target organ; CRP: C-reactive protein; SpO2: oxygen saturation; SBP: systolic blood pressure.
Anticoagulant treatment at baseline and during admission for patients with AF and COVID-19. Classified as deceased and not deceased
| Deceased N = 738 (%) | Not deceased N = 1061 (%) | p | |
|---|---|---|---|
| Baseline anticoagulant therapy | |||
| No treatment | 140 (19.1) | 252 (23.8) | <0.01 |
| VKA | 360 (49.2) | 384 (36.3) | <0.01 |
| DOAC | 212 (29.0) | 405 (38.3) | <0.01 |
| Anticoagulant treatment during admission | |||
| LMWH | 524 (72.1) | 788 (74.6) | 0.251 |
| VKA | 73 (10.1) | 109 (10.4) | |
| DOAC | 50 (6.9) | 200 (19) | <0.01 |
DOAC: direct oral anticoagulants; VKA: vitamin K antagonists; LMWH: low molecular weight heparin.
Treatments during admission and complications of patients with AF and COVID-19, classified as deceased and not deceased.
| Deceased N = 738 (%) | Not deceased N = 1061 (%) | p | |
|---|---|---|---|
| Treatments during admission | |||
| ACEI | 82 (11.2) | 124 (11.8) | 0.724 |
| ARBs | 91 (12.6) | 195 (18.6) | <0.01 |
| ASA | 75 (10.4) | 96 (9.2) | 0.396 |
| Statins | 109 (15.0) | 240 (2.9) | <0.01 |
| Ibuprofen | 1 (0.1) | 11 (1.0) | 0.04 |
| Other NSAIDs | 20 (2.8) | 37 (3.5) | 0.03 |
| Corticosteroids | 320 (43.8) | 387 (35.9) | <0.01 |
| Lopinavir/ritonavir | 302 (41.2) | 481 (44.5) | 0.17 |
| Remdesivir | 2 (0.3) | 15 (1.4) | <0.01 |
| Hydroxychloroquine | 500 (68.4) | 878 (81.1) | <0.01 |
| Chloroquine | 27 (3.7) | 33 (3.1) | 0.46 |
| Colchicine | 10 (1.4) | 9 (0.8) | 0.28 |
| Tocilizumab | 33 (4.5) | 46 (4.3) | 0.79 |
| Complications | |||
| Prone | 93 (12.7) | 58 (5.5) | <0.01 |
| NIMV | 58 (7.9) | 35 (3.3) | <0.01 |
| IMV | 47 (6.4) | 26 (2.5) | <0.01 |
| HFO | 85 (11.7) | 48 (4.6) | <0.01 |
| Bacterial pneum. | 149 (20.2) | 130 (12.3) | <0.01 |
| ARDS | 391 (53.4) | 49 (4.6) | <0.01 |
| HF | 208 (28.2) | 157 (14.8) | <0.01 |
| AMI | 23 (3.1) | 6 (0.6) | <0.01 |
| AKF | 279 (37.9) | 174 (16.4) | <0.01 |
| PTE | 4 (0.5) | 8 (0.8) | 0.578 |
ASA: acetylsalicylic acid; NSAIDs: nonsteroidal anti-inflammatory drugs; ARBs: angiotensin receptor blockers; AMI: acute myocardial infarction; HF: heart failure; ACEI: angiotensin converting enzyme inhibitors; AKF: acute kidney failure; HFO: high-flow oxygen therapy; ARDS: acute respiratory distress syndrome; PTE: pulmonary thromboembolism; IMV: invasive mechanical ventilation; NIMV: Non-invasive mechanical ventilation.
Logistic regression analysis of factors associated with mortality in patients with AF admitted for COVID-19, including oral anticoagulation
| OR CI | p | |
|---|---|---|
| Age | 1.069 1.048–1.090 | 0.000 |
| Sex (female) | 0.726 0.518–1.018 | 0.63 |
| Oxygen saturation>93% | 0.956 0.929–0.985 | 0.003 |
| Charlson index | 1.112 1.035–1.194 | 0.004 |
| D-dimer (ng/dl) | 1.000 1.000–1.000 | 0.693 |
| Serum creatine at admission (mg/dL) | 1.354 1.157–1.584 | 0.001 |
| C-reactive protein at admission (mg/L) | 1.003 1.001–1.005 | 0.002 |
| Direct oral anticoagulant | 0.597 0.402–0.888 | 0.011 |
Numerous variables showed statistically significant differences in the deceased group. These were older and had a higher proportion of hypertensive and diabetic patients with target organ involvement. However, no statistically significant differences were found for dyslipidaemia and obesity, although there was a greater trend in the deceased group. A higher prevalence of cardiovascular history was also observed in the deceased: heart failure, acute myocardial infarction, angina pectoris, stroke, and peripheral vascular disease.
Clinically, deceased patients were admitted with a higher heart rate (88.38 vs. 84.95; p < 0.01), with higher percentage of respiratory failure (67.2 vs. 20.1%; p < 0.01), higher tachypnoea (58.0 vs. 30.0%; p < 0.01) and greater dyspnoea and confusion on admission (73.6 vs. 56.8%; p < 0.01 and 37.1 vs. 13.3%; p < 0.01, respectively). On the other hand, deceased patients had statistically significantly higher levels of creatinine, glucose, C-reactive protein (CRP), ferritin and D-dimer, as well as a higher percentage of bilateral pneumonia and pleural effusion. No differences were found in INR values (2.51 vs. 2.41; p = 0.56). Deceased patients showed higher rates of complications, except for pulmonary embolism (0.5 vs. 0.8; p = 0.578).
With regard to anticoagulant treatment, it is noteworthy that deceased patients had a lower frequency of treatment with DOACs, both at baseline (29 vs. 38.3%; p < 0.01) and during admission (6.9 vs. 19%; p < 0.01).
Finally, in the multivariate analysis, the following were independent factors for mortality: age, hypertension, Charlson index, and elevated heart rate, creatinine, CRP, ferritin and D-dimer values. Treatment with DOACs had a protective role for mortality (Appendix C Supplementary table of Annex B).
DiscussionThe results of our research show that patients with COVID-19 infection with a history of AF may have a high mortality rate during hospital admission. In our series, the mortality observed in this patient population exceeded 40% during the first waves of the COVID-19 pandemic. These findings have also been observed in other international multicenter registries such as HOPE, in which the researchers also observed a mortality rate of 43% for subjects with a history of AF19.
AF associates a series of comorbidities that have been described as poor prognostic factors in COVID-1919. Our series showed a higher proportion of hypertensive, diabetic and patients with a history of cardiovascular disease (heart failure, acute myocardial infarction, angina, stroke and peripheral vascular disease) among the deceased. In terms of clinical characteristics at admission, the following were associated with worse prognosis: elevated heart rate, baseline oxygen saturation below 94%, tachypnoea and the presence of dyspnoea and confusion. These results are similar to those described in the literature in patients without AF3. Likewise, patients who had a significant inflammatory response on admission with increased lymphopenia and higher CRP, D-dimer, ferritin and creatinine levels had higher mortality3,7.
Our research allows, at the time of admission, to identify a profile of patients with a history of AF and a high risk of mortality and complications. Given the high mortality rate in patients with AF, the mere fact of having AF poses a risk, which is increased in the case of advanced age, hypertension, previously established cardiovascular diseases, and a state of instability with respiratory failure and tachycardia with a high inflammatory response. The number of complications developed by AF patients was also quite high, all of them higher in the deceased group, as expected.
AF is the most common arrhythmia in patients with COVID-19 for two reasons: on the one hand, it is the most common arrhythmia in the general population and, on the other hand, COVID-19 favours its occurrence8,10. The mechanisms by which COVID-19 increases the frequency of AF are beginning to be understood, although they are not yet fully clear. Among the hypotheses proposed, the following have been postulated: reduced availability of ACE-II receptors, cytokine storm, endothelial damage, electrolyte disturbances, hypoxaemia and increased activity of the sympathetic nervous system as mechanisms favouring the onset of AF due to its effects on cardiac remodelling11. Recent studies show that patients with COVID-19 infection with a greater inflammatory reaction have a higher risk of developing AF, as occurs with influenza infection20.
The role of anticoagulation in the treatment of COVID-19 is yet to be determined. Several studies have demonstrated the benefit of anticoagulation at prophylactic doses in relation to the prothrombotic state resulting from the massive inflammatory response occurring in COVID-1911. Recent published evidence in non-critically ill patients with COVID-19 shows that an initial strategy of therapeutic dose anticoagulation with heparin increased the likelihood of survival to hospital discharge compared to routine thromboprophylaxis21.
One of the most relevant findings of our study is the observation of a higher proportion of patients treated with DOACs among the survivors, both at baseline and during admission. In fact, it behaves as a protective factor in the multivariate analysis. This finding is probably influenced by the fact that patients on baseline DOAC therapy are younger and in a better cardiorespiratory status, which allows them to tolerate the oral route well. However, maintaining the DOAC during admission was not associated with increased mortality. In this sense, some authors have also observed these findings of benefit from the use of DOACs in patients with COVID-19 infection who required hospital admission22.
The indication to maintain DOAC therapy in patients with AF already taking it at baseline and DOAC therapy in the prevention of thromboembolic events in COVID-19 is an attractive option to consider in outpatient management or hospitalised COVID patients with good cardiopulmonary function. The main limitation would be its potential interaction with some of the treatments used at the beginning of the pandemic for COVID-19 such as lopinavir/ritonavir, although these treatments are currently out of use and no interactions have been described with corticosteroids, remdesivir or anti-inflammatory biologics (tocilizumab, baricitinib, etc.), which are the current reference treatments.
We believe that our study meets the objective of describing a clinical profile of patients with AF admitted for COVID-19 in Spain and identifying poor prognostic factors associated with morbidity and mortality: it is the first of its kind in Spain and one of the few worldwide. Despite this, it has several limitations. Firstly, this is a retrospective and observational study so, despite a multivariate analysis and a logistic regression, bias cannot be ruled out. On the other hand, the SEMI-COVID registry has involved a large number of investigators at different levels of care, which means heterogeneity in the inclusion of data, which, moreover, have been obtained from discharge reports and clinical records. Analysing only hospitalised patients gives a profile of greater severity and the data may not be fully translatable to the rest of AF patients. Despite these limitations, a large number of AF patients from all over the country have been analysed, as it is a multicentre registry, which has made it possible to draw up a risk profile in patients hospitalised for COVID-19. Future prospective studies are needed to confirm these initial data, given that only retrospective studies have been published to date.
ConclusionsAF and its associated comorbidities are a risk factor for mortality, morbidity, and the development of complications in patients hospitalized for COVID-19. Given the magnitude and importance of the pandemic, this has meant that COVID-19 has become the leading cause of death in patients with AF, replacing cardiovascular causes. On the other hand, the clinical, laboratory and radiological data associated with a worse outcome in AF patients are similar to those previously described in the overall population.
Both pre-treatment with DOACs and treatment with DOACs during admission seem to have a protective role in patients with AF, although this fact should be confirmed in prospective studies. In any case, with these findings, there is no indication to modify the treatment with DOACs for LMWH in hospitalized patients and the door is opened to carry out clinical trials with DOACs as prevention of thromboembolic events occurring in COVID-19.
Conflict of interestsThe authors state that they have no conflict of interest in relation to this publication.
AcknowledgementsWe thank all participants and investigators of the SEMI-COVID-19 Registry.
Annex A. List of investigators of the SEMI-COVID-19 RegistrySEMI-COVID-19 Registry Coordinator: Jose Manuel Casas Rojo.
Members of the Scientific Committee of the SEMI-COVID-19 Registry: José Manuel Casas Rojo, José Manuel Ramos Rincón, Carlos Lumbreras Bermejo, Jesús Millán Núñez-Cortés, Juan Miguel Antón Santos, Ricardo Gómez Huelgas.
Members of the SEMI-COVID-19 Group
Bellvitge University Hospital (L'Hospitalet de Llobregat, Barcelona)V
Xavier Corbella, Francesc Formiga Pérez, Narcís Homs, Abelardo Montero, José María Mora-Luján, Manuel Rubio-Rivas
de Octubre University Hospital (Madrid)
Paloma Agudo de Blas, Coral Arévalo Cañas, Blanca Ayuso, José Bascuñana Morejón, Samara Campos Escudero, María Carnevali Frías, Santiago Cossío Tejido, Borja de Miguel Campo, Carmen Díaz Pedroche, Raquel Díaz Simón, Ana García Reyne, Laura Ibarra Veganzones, Lucía Jorge Huerta, Antonio Lalueza Blanco, Jaime Laureiro Gonzalo, Jaime Lora-Tamayo, Carlos Lumbreras Bermejo, Guillermo Maestro de la Calle, Rodrigo Miranda Godoy, Bárbara Otero Perpiña, Diana Paredes Ruiz, Marcos Sánchez Fernández, Javier Tejada Montes
Costa del Sol Hospital (Marbella, Malaga)
Victoria Augustín Bandera, Javier García Alegría, Nicolás Jiménez-García, Jairo Luque del Pino, María Dolores Martín Escalante, Francisco Navarro Romero, Victoria Núñez Rodríguez, Julián Olalla Sierra
Gregorio Marañón University Hospital (Madrid)
Laura Abarca Casas, Álvaro Alejandre de Oña, Rubén Alonso Beato, Leyre Alonso Gonzalo, Jaime Alonso Muñoz, Christian Mario Amodeo Oblitas, Cristina Ausín García, Marta Bacete Cebrián, Jesús Baltasar Corral, María Barrientos Guerrero, Alejandro D. Bendala Estrada, María Calderón Moreno, Paula Carrascosa Fernández, Raquel Carrillo, Sabela Castañeda Pérez, Eva Cervilla Muñoz, Agustín Diego Chacón Moreno, María Carmen Cuenca Carvajal, Sergio de Santos, Andrés Enríquez Gómez, Eduardo Fernández Carracedo, María Mercedes Ferreiro-Mazón Jenaro, Francisco Galeano Valle, Alejandra García, Irene García Fernandez-Bravo, María Eugenia García Leoni, María Gómez Antúnez, Candela González San Narciso, Anthony Alexander Gurjian, Lorena Jiménez Ibáñez, Cristina Lavilla Olleros, Cristina Llamazares Mendo, Sara Luis García, Víctor Mato Jimeno, Clara Millán Nohales, Jesús Millán Núñez-Cortés, Sergio Moragón Ledesma, Antonio Muiño Míguez, Cecilia Muñoz Delgado, Lucía Ordieres Ortega, Susana Pardo Sánchez, Alejandro Parra Virto, María Teresa Pérez Sanz, Blanca Pinilla Llorente, Sandra Piqueras Ruiz, Guillermo Soria Fernández-Llamazares, María Toledano Macías, Neera Toledo Samaniego, Ana Torres do Rego, María Victoria Villalba García, Gracia Villarreal, María Zurita Etayo.
Cabueñes Hospital (Gijon, Asturias)
Ana María Álvarez Suárez, Carlos Delgado Vergés, Rosa Fernández-Madera Martínez, Eva M.ª Fonseca Aizpuru, Alejandro Gómez Carrasco, Cristina Helguera Amezúa, Juan Francisco López Caleya, Diego López Martínez, María del Mar Martínez López, Aleida Martínez Zapico, Carmen Olabuenaga Íscar, Lucía Pérez Casado, María Luisa Taboada Martínez, Lara María Tamargo Chamorro.
Regional University Hospital of Malaga (Malaga)
M.ª Mar Ayala-Gutiérrez, Rosa Bernal López, José Bueno Fonseca, Verónica Andrea Buonaiuto, Luis Francisco Caballero Martínez, Lidia Cobos Palacios, Clara Costo Muriel, Francis de Windt, Ana Teresa Fernández-Truchaud Christophel, Paula García Ocaña, Ricardo Gómez Huelgas, Javier Gorospe García, José Antonio Hurtado Oliver, Sergio Jansen-Chaparro, María Dolores López-Carmona, Pablo López Quirantes, Almudena López Sampalo, Elizabeth Lorenzo-Hernández, Juan José Mancebo Sevilla, Jesica Martín Carmona, Luis Miguel Pérez-Belmonte, Iván Pérez de Pedro, Araceli Pineda-Cantero, Carlos Romero Gómez, Michele Ricci, Jaime Sanz Cánovas.
La Paz University Hospital (Madrid)
Jorge Álvarez Troncoso, Francisco Arnalich Fernández, Francisco Blanco Quintana, Carmen Busca Arenzana, Sergio Carrasco Molina, Aránzazu Castellano Candalija, Germán Daroca Bengoa, Alejandro de Gea Grela, Alicia de Lorenzo Hernández, Alejandro Díez Vidal, Carmen Fernández Capitán, María Francisca García Iglesias, Borja González Muñoz, Carmen Rosario Herrero Gil, Juan María Herrero Martínez, Víctor Hontañón, María Jesús Jaras Hernández, Carlos Lahoz, Cristina Marcelo Calvo, Juan Carlos Martín Gutiérrez, Mónica Martínez Prieto, Elena Martínez Robles, Araceli Menéndez Saldaña, Alberto Moreno Fernández, José María Mostaza Prieto, Ana Noblejas Mozo, Carlos Manuel Oñoro López, Esmeralda Palmier Peláez, Marina Palomar Pampyn, María Angustias Quesada Simón, Juan Carlos Ramos, Luis Ramos Ruperto, Aquilino Sánchez Purificación, Teresa Sancho Bueso, Raquel Sorriguieta Torre, Clara Itziar Soto Abanedes, Yeray Untoria Tabares, Marta Varas Mayoral, Julia Vásquez Manau.
Royo Villanova Hospital (Zaragoza)
Nicolás Alcalá Rivera, Anxela Crestelo Vieitez, Esther del Corral Beamonte, Jesús Díez Manglano, Isabel Fiteni Mera, María del Mar García Andreu, Martín Gericó Aseguinolaza, Cristina Gallego Lezaun, Claudia Josa Laorden, Raúl Martínez Murgui, Marta Teresa Matía Sanz.
Reina Sofia University Hospital (Cordoba)
Antonio Pablo Arenas de Larriva, Pilar Calero Espinal, Javier Delgado Lista, Francisco Fuentes-Jiménez, María del Carmen Guerrero Martínez, María Jesús Gómez Vázquez, José Jiménez Torres, Laura Limia Pérez, José López-Miranda, Laura Martín Piedra, Marta Millán Orge, Javier Pascual Vinagre, Pablo Pérez-Martinez, María Elena Revelles Vílchez, Ángela Rodrigo Martínez, Juan Luis Romero Cabrera, José David Torres-Peña.
Hospital Clínico of Santiago de Compostela (La Coruña)
María del Carmen Beceiro Abad, María Aurora Freire Romero, Sonia Molinos Castro, Emilio Manuel Paez Guillán, María Pazo Núñez, Paula María Pesqueira Fontán.
Puerta de Hierro University Hospital (Madrid)
Ane Andrés Eisenhofer, Ana Arias Milla, Isolina Baños Pérez, Laura Benítez Gutiérrez, Javier Bilbao Garay, Jorge Calderón Parra, Alejandro Callejas Díaz, Erika Camacho Da Silva, M.ª Cruz Carreño Hernández, Raquel Castejón Díaz, María Jesús Citores Sánchez, Carmen Cubero Gozalo, Valentín Cuervas-Mons Martínez, Laura Dorado Doblado, Sara de la Fuente Moral, Alberto Díaz de Santiago, Itziar Diego Yagüe, Ignacio Donate Velasco, Ana María Duca, Pedro Durán del Campo, Gabriela Escudero López, Esther Expósito Palomo, Ana Fernández Cruz, Amy Galán Gómez, Sonia García Prieto, Beatriz García Revilla, Miguel Ángel García Viejo, Javier Gómez Irusta, Patricia González Merino, Edith Vanessa Gutiérrez Abreu, Isabel Gutiérrez Martín, Ángela Gutiérrez Rojas, Andrea Gutiérrez Villanueva, Jesús Herráiz Jiménez, Fátima Ibáñez Estéllez, Pedro Laguna del Estal, M.ª Carmen Máinez Sáiz, Carmen de Mendoza Fernández, María Martínez Urbistondo, Fernando Martínez Vera, María Mateos Seirullo, Susana Mellor Pita, Patricia A. Mills Sánchez, Esther Montero Hernández, Alberto Mora Vargas, Víctor Moreno-Torres Concha, Ignacio Morrás de la Torre, Elena Múñez Rubio, Rosa Muñoz de Benito, Alejandro Muñoz Serrano, Pablo Navarro Palomo, Ilduara Pintos Pascual, Arturo José Ramos Martín-Vegue, Antonio Ramos Martínez, Celia Rodríguez Olleros, Alberto Roldán Montaud, Yolanda Romero Pizarro, Silvia Rosado García, Diana Ruiz de Domingo, David Sánchez Ortiz, Enrique Sánchez Chica, Irene Solano Almena, Elena Suanzes Martín, Yale Tung Chen, Pablo Tutor de Ureta, Ángela Valencia Alijo, José Manuel Vázquez Comendador, Juan Antonio Vargas Núñez.
Dr. Peset University Hospital (Valencia)
Juan Alberto Aguilera Ayllón, Arturo Artero, María del Mar Carmona Martín, María José Fabiá Valls, María de Mar Fernández Garcés, Ana Belén Gómez Belda, Ian López Cruz, Manuel Madrazo López, Elisabeth Mateo Sanchís, Jaume Micó Gandía, Laura Piles Roger, Adela María Pina Belmonte, Alba Viana García.
Hospital Clínico San Carlos (Madrid)
Inés Armenteros Yeguas, Javier Azaña Gómez, Julia Barrado Cuchillo, Irene Burruezo López, Noemí Cabello Clotet, Alberto E. Calvo Elías, Elpidio Calvo Manuel, Carmen María Cano de Luque, Cynthia Chocron Benbunan, Laura Dans Vilan, Claudia Dorta Hernández, Ester Emilia Dubon Peralta, Vicente Estrada Pérez, Santiago Fernández-Castelao, Marcos Oliver Fragiel Saavedra, José Luis García Klepzig, María del Rosario Iguarán Bermúdez, Esther Jaén Ferrer, Alejandro Maceín Rodríguez, Alejandro Marcelles de Pedro, Rubén Ángel Martín Sánchez, Manuel Méndez Bailón, Sara Miguel Álvarez, María José Núñez Orantos, Carolina Olmos Mata, Eva Orviz García, David Oteo Mata, Cristina Outon González, Juncal Pérez-Somarriba, Pablo Pérez Mateos, María Esther Ramos Muñoz, Xabier Rivas Regaira, Laura M.ª Rodríguez Gallardo, Íñigo Sagastagoitia Fornie, Alejandro Salinas Botrán, Miguel Suárez Robles, Maddalena Elena Urbano, Andrea María Vellisca González, Miguel Villar Martínez, Borja Sainz Rodríguez.
Badajoz University Hospital Complex (Badajoz)
Rafael Aragón Lara, Inmaculada Cimadevilla Fernández, Juan Carlos Cira García, Gema María García, Julia González Granados, Beatriz Guerrero Sánchez, Francisco Javier Monreal Periáñez, María Josefa Pascual Pérez.
University Hospital San Juan de Alicante (Alicante)
Marisa Asensio Tomás, David Balaz, David Bonet Tur, Ruth Cañizares Navarro, Paloma Chazarra Pérez, Jesús Corbacho Redondo, Eliana Damonte White, María Escamilla Espínola, Leticia Espinosa del Barrio, Pedro Jesús Esteve Atiénzar, Carles García Cervera, David Francisco García Núñez, Francisco Garrido Navarro, Vicente Giner Galvañ, Angie Gómez Uranga, Javier Guzmán Martínez, Isidro Hernández Isasi, Lourdes Lajara Villar, Verónica Martínez Sempere, Juan Manuel Núñez Cruz, Sergio Palacios Fernández, Juan Jorge Peris García, Rafael Piñol Pleguezuelos, Andrea Riaño Pérez, José Miguel Seguí Ripoll, Azucena Sempere Mira, Philip Wikman-Jorgensen.
General University Hospital of Elda (Alicante)
Carmen Cortés Saavedra, Jennifer Fernández Gómez, Borja González López, María Soledad Hernández Garrido, Ana Isabel López Amorós, Santiago López Gil, María de los Reyes Pascual Pérez, Nuria Ramírez Perea, Andrea Torregrosa García.
Infanta Cristina University Hospital (Parla, Madrid)
Juan Miguel Antón Santos, Ana Belén Barbero Barrera, Blanca Beamonte Vela, Coralia Bueno Muiño, Charo Burón Fernández, Ruth Calderón Hernáiz, Irene Casado López, José Manuel Casas Rojo, Andrés Cortés Troncoso, Pilar Cubo Romano, Francesco Deodati, Alejandro Estrada Santiago, Gonzalo García Casasola Sánchez, Elena García Guijarro, Francisco Javier García Sánchez, Pilar García de la Torre, Mayte de Guzmán García-Monge, Davide Luordo, María Mateos González, José A. Melero Bermejo, Cruz Pastor Valverde, José Luis Pérez Quero, Fernando Roque Rojas, Lorea Roteta García, Elena Sierra Gonzalo, Francisco Javier Teigell Muñoz, Juan Vicente de la Sota, Javier Villanueva Martínez.
Pozoblanco Hospital (Cordoba)
José Nicolás Alcalá Pedrajas, Antonia Márquez García, Inés Vargas.
Santa Marina Hospital (Bilbao)
María Areses Manrique, Ainara Coduras Erdozain, Ane Labirua-Iturburu Ruiz.
Son Llàtzer University Hospital (Palma de Mallorca)
Andrés de la Peña Fernández, Almudena Hernández Milián.
San Pedro Hospital (Logroño, La Rioja)
Diana Alegre González, Irene Ariño Pérez de Zabalza, Sergio Arnedo Hernández, Jorge Collado Sáenz, Beatriz Dendariena, Marta Gómez del Mazo, Iratxe Martínez de Narvajas Urra, Sara Martínez Hernández, Estela Menéndez Fernández, José Luis Peña Somovilla, Elisa Rabadán Pejenaute.
Mataró Hospital (Barcelona)
Raquel Aranega González, Ramón Boixeda, Javier Fernández, Carlos Lopera Mármol, Marta Parra Navarro, Ainhoa Rex Guzmán, Aleix Serrallonga Fustier.
Ferrol University Hospital Complex (La Coruña)
Hortensia Álvarez Díaz, Tamara Dalama López, Estefanía Martul Pego, Carmen Mella Pérez, Ana Pazos Ferro, Sabela Sánchez Trigo, Dolores Suárez Sambade, María Trigas Ferrín, María del Carmen Vázquez Friol, Laura Vilariño Maneiro.
Infanta Margarita Hospital (Cabra, Cordoba)
María Esther Guisado Espartero, Lorena Montero Rivas, María de la Sierra Navas Alcántara, Raimundo Tirado-Miranda.
University Healthcare Complex of Salamanca (Salamanca)
Gloria María Alonso Claudio, Víctor Barreales Rodríguez, Cristina Carbonell Muñoz, Adela Carpio Pérez, María Victoria Coral Orbes, Daniel Encinas Sánchez, Sandra Inés Revuelta, Miguel Marcos Martín, José Ignacio Martín González, José Ángel Martín Oterino, Leticia Moralejo Alonso, Sonia Peña Balbuena, María Luisa Pérez García, Ana Ramón Prados, Beatriz Rodríguez-Alonso, Ángela Romero Alegría, María Sánchez Ledesma, Rosa Juana Tejera Pérez.
Virgen del Rocío University Hospital (Seville)
Reyes Aparicio Santos, Máximo Bernabeu-Wittel, Santiago Rodríguez Suárez, María Nieto, Luis Giménez Miranda, Rosa María Gámez Mancera, Fátima Espinosa Torre, Carlos Hernández Quiles, Concepción Conde Guzmán, Juan Delgado de la Cuesta, Jara Eloísa Ternero Vega, María del Carmen López Ríos, Pablo Díaz Jiménez, Bosco Barón Franco, Carlos Jiménez de Juan, Sonia Gutiérrez Rivero, Julia Lanseros Tenllado, Verónica Alfaro Lara, Aurora González Estrada.
Public Hospital of Monforte de Lemos (Lugo)
José López Castro, Manuel Lorenzo López Reboiro, Cristina Sardiña González.
Marina Baixa Hospital (Villajoyosa, Alicante)Javier Ena, José Enrique Gómez Segado.
Defense General Hospital (Zaragoza)
Anyuli Gracia Gutiérrez, Leticia Esther Royo Trallero.
Quironsalud Madrid U. Hospital (Madrid)
Pablo Guisado Vasco, Ana Roda Santacruz, Ana Valverde Muñoz.
Blanes Regional Hospital (Girona)
Oriol Alonso Gisbert, Mercé Blázquez Llistosella, Pere Comas Casanova, Angels García Flores, Anna García Hinojo, Ana Inés Méndez Martínez, María del Carmen Nogales Nieves, Agnés Rivera Austrui, Alberto Zamora Cervantes.
Salnes Hospital (Villagarcia de Arosa, Pontevedra)
Vanesa Alende Castro, Ana María Baz Lomba, Ruth Brea Aparicio, Marta Fernández Morales, Jesús Manuel Fernández Villar, María Teresa López Monteagudo, Cristina Pérez García, Lorena Rodríguez Ferreira, Diana Sande Llovo, María Begoña Valle Feijoo.
The following is Supplementary data to this article:
