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Add-on inhaled budesonide in the treatment of hospitalised patients with COVID-19: a randomised clinical trial

Alvar Agustí, Gaston De Stefano, Alberto Levi, Xavier Muñoz, Christian Romero-Mesones, Oriol Sibila, Alejandra Lopez-Giraldo, Vicente Plaza Moral, Elena Curto, Andrés L. Echazarreta, Silvana E. Márquez, Sergi Pascual-Guàrdia, Salud Santos, Alicia Marin, Luis Valdés, Fernando Saldarini, Clara Salgado, Georgina Casanovas, Sara Varea, José Ríos, Rosa Faner
European Respiratory Journal 2022; DOI: 10.1183/13993003.03036-2021
Alvar Agustí
1Hospital Clinic, Barcelona, Spain
2Universitat Barcelona, Spain
3Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
4CIBER Enfermedades Respiratorias, Spain
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  • For correspondence: aagusti@clinic.cat
Gaston De Stefano
5Servicio de Neumotisiologia, Hospital Francisco Muñiz, Buenos Aires, Argentina
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Alberto Levi
5Servicio de Neumotisiologia, Hospital Francisco Muñiz, Buenos Aires, Argentina
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Xavier Muñoz
4CIBER Enfermedades Respiratorias, Spain
6Servei Pneumologia H. Vall d'Hebron, Barcelona Spain
7Biostatistics Unit, Faculty of Medicine, Universitat Autònoma de Barcelona
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Christian Romero-Mesones
4CIBER Enfermedades Respiratorias, Spain
6Servei Pneumologia H. Vall d'Hebron, Barcelona Spain
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Oriol Sibila
1Hospital Clinic, Barcelona, Spain
2Universitat Barcelona, Spain
3Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
4CIBER Enfermedades Respiratorias, Spain
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Alejandra Lopez-Giraldo
2Universitat Barcelona, Spain
3Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
4CIBER Enfermedades Respiratorias, Spain
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Vicente Plaza Moral
4CIBER Enfermedades Respiratorias, Spain
8Department of Respiratory Medicine, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain
9Institut d'Investigació Biomédica Sant Pau (IIB Sant Pau), Barcelona, Spain
10Department of Medicine, Universitat Autònoma de Barcelona, Barcelona, Spain
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Elena Curto
4CIBER Enfermedades Respiratorias, Spain
8Department of Respiratory Medicine, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain
9Institut d'Investigació Biomédica Sant Pau (IIB Sant Pau), Barcelona, Spain
10Department of Medicine, Universitat Autònoma de Barcelona, Barcelona, Spain
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Andrés L. Echazarreta
11Servicio de Neumonología, Hospital San Juan de Dios de La Plata, Buenos Aires, Argentina
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  • ORCID record for Andrés L. Echazarreta
Silvana E. Márquez
11Servicio de Neumonología, Hospital San Juan de Dios de La Plata, Buenos Aires, Argentina
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Sergi Pascual-Guàrdia
4CIBER Enfermedades Respiratorias, Spain
12Servei de Pneumologia, Hospital del Mar – IMIM, Barcelona, Spain
13Universitat Pompeu Fabra Barcelona, Spain
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Salud Santos
2Universitat Barcelona, Spain
4CIBER Enfermedades Respiratorias, Spain
14Department of Pulmonary Medicine, Bellvitge University Hospital, L'Hospitalet de Llobregat, Barcelona, Spain
15Institut d'Investigació Biomèdica de Bellvitge – IDIBELL, Spain
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Alicia Marin
4CIBER Enfermedades Respiratorias, Spain
16Hospital Universitari Germans Trias i Pujol, Badalona, Spain
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Luis Valdés
17Servicio de Neumología, Complejo Hospitalario Universitario de Santiago, Santiago de Compostela, Spain
18Instituto de Investigaciones Sanitarias (IDIS), Santiago de Compostela, Spain
19Universidad de Santiago de Compostela, Spain
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Fernando Saldarini
20Sección de Neumotisiologia, Hospital Donación Francisco Santojanni, Buenos Aires, Argentina
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Clara Salgado
21Centro de Educación Médica e Investigaciones Clínicas Norberto Quirno
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Georgina Casanovas
1Hospital Clinic, Barcelona, Spain
3Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
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Sara Varea
1Hospital Clinic, Barcelona, Spain
3Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
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José Ríos
1Hospital Clinic, Barcelona, Spain
3Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
7Biostatistics Unit, Faculty of Medicine, Universitat Autònoma de Barcelona
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Rosa Faner
2Universitat Barcelona, Spain
3Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
4CIBER Enfermedades Respiratorias, Spain
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SARS-CoV-2 vaccines have been extremely effective to reduce the incidence of severe COVID19 [1–3], but effective and safe treatments of the acute infection are still limited [4, 5]. An uncontrolled pulmonary inflammatory response to SARS-CoV-2 is considered a key pathogenic mechanism of COVID19 progression [6], so systemic dexamethasone is recommended in severe cases [5, 7]. On the other hand, in very mild patients at home inhaled corticosteroids (ICS) may prevent disease progression [8–11]. Whether ICS prevent disease progression too in patients hospitalised because of COVID19 has not been explored before. Accordingly, we designed an investigator-initiated, open-label, randomised clinical trial (RCT) to explore the efficacy of adding inhaled budesonide to usual care to prevent disease progression in patients hospitalised because of COVID19 pneumonia. We also monitored carefully the safety of this intervention since there are concerns about the use of systemic corticosteroids in other viral (influenza) lung infections [12].

Methods

The “Inhaled Corticosteroid Treatment of COVID19 Patients With Pneumonia” (TACTIC) was a multicentre, international (Spain and Argentina), randomised (1:1), open label RCT (NCT04355637) whose primary objective was to investigate if the addition of inhaled budesonide (400 µg/12 h via Pulmicort Turbuhaler®) to usual care (as dynamically established by the institutional protocol of each participating centre during the course of the pandemic) prevents disease progression, defined by a composite outcome that included treatment with non-invasive ventilation of high flow oxygen devices (WHO stage 5), invasive ventilation (WHO stage 6) and/or death from any cause (WHO stage 7) [13] during the first 15 days after randomisation.

We studied males and females between 18–80 years of age hospitalised because of PCR confirmed SARS-CoV-2 infection, with radiological evidence (plain chest x-ray) of pneumonia, without any contraindication to the study drug, who provided informed consent. Exclusion criteria included previous treatment with inhaled or systemic steroids (e.g., dexamethasone) and/or other immunomodulator drugs (e.g., anti-interleukins), high flow-oxygen or mechanical ventilation, and pregnancy. This RCT was approved by the Institutional Review Boards of participating institutions and was supported by AstraZeneca, who generously provided the study medication for free and economic support for logistics costs but did not participate in the design of the study, data analysis and/or writing of the manuscript. The Clinical Trial Unit of Fundació Clinic per la Recerca Biomedica-Hospital Clinic (Barcelona, Spain) monitored the trial in coordination with Klixar (in participating centres in Argentina), centralised all investigational information, and assured the quality control of results.

Based on available knowledge at the time of trial design (March 2020), we hypothesised that this would occur in 15% of patients randomised to the usual care arm and 5% of those included in the intervention arm. Then, for a two-sided type I error of 5% and power of 80% and 5% estimated losses during follow-up, with three prespecified interim analyses designed using the Rho family spending functions with rho=7 and a recalculation of sample size at 75% of expected events, we estimated that 300 patients (150 per arm) would be needed to be randomised, (East v6.5 Cytel Inc., Cambridge, MA). Randomisation (1:1) was made by a permuted-block method with a block size of multiple of 2 elements and was stratified by centre with an interactive web service. The primary endpoint of the study was estimated by comparing the proportion of patients with disease progression (defined as above) in both arms using a binomial regression model, adjusted for centre (grouped by country) as covariate [14, 15]. Time-to-event analyses was described by means of the Kaplan-Meier method and inferential analyses was made by means log-rank test. All analyses were carried out by the Medical Statistics Core Facility of IDIBAPS-Hospital Clinic Barcelona (Spain) and performed using SAS v9.4 (SAS Institute Inc Cary, NC, USA)

Results

From April 21, 2020 until March 16 2021, we randomised 120 patients (Full Analysis Set (FAS)). Because the progressive and generalised use of dexamethasone to treat hospitalised patients with COVID-19 [5] limited greatly our capacity to continue recruiting patients who had not received it before randomisation, the steering committee of the study decided to stop the study prematurely in April 2021.

As shown in table 1, both groups were comparable in terms of demographics and main clinical and radiological characteristics at randomisation, albeit the proportion of patients without supplemental oxygen at entry was nominally higher in the usual care group (n=49 (79.0%) versus n=40 (69.0%)). Disease progression occurred in 4 patients (6.62%; 95% CI 0.45% to 12.79%) in the usual care group and 2 patients (3.74%; 95%CI −1.23% to 8.72%] in the usual care+budesonide one, difference being non-significant (−2.88% [95%CI −10.48% to 4.72%], p=0.458). Of note, 13 patients (21%) in the usual care arm were treated with dexamethasone after randomisation at the discretion of the attending physician, whereas only 6 patients (10.7%) in the intervention group were. Importantly, adverse events were similar in both groups and there were no treatment-related adverse events (table 1). Two patients died during follow-up, both beyond day 30, 1 in the control group (due to liver cirrhosis) and 1 in the intervention group (due to COVID19) (log-rank p value=0.9564).

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TABLE 1

Demographics and main clinical variables (n (%) or mean±sd) at randomisation (FAS), concomitant medications received and adverse events (Safety population)

Discussion

This RCTs lacks statistical power because it had to be terminated prematurely. However, results suggest that the addition of inhaled budesonide to usual care in patients hospitalised because of COVID19 pneumonia is safe and showed an encouraging trend towards a reduction in disease progression. The fact that the proportion of patients not requiring oxygen supplementation at randomisation was larger in the usual care group (hence, better pulmonary gas exchange at baseline), and that, despite this, a higher proportion of them received systemic dexamethasone at the discretion of the attending physician, provides additional indirect evidence of a beneficial clinical effect of inhaled budesonide to prevent disease progression. Finally, it is important to highlight that the use of an inhaled corticosteroid in these patients was safe. These results may open the door for larger RCT in the near future, now that a new pandemic wave seems to be emerging again in several countries around the world. Dexamethasone reduces mortality in patients requiring supplementary oxygen in hospital and is recommended by ERS guideline [5, 7], but is not recommended for patients not requiring supplementary oxygen, which accounted for 74% of our cohort. A safe treatment that could reduce disease progression in this patient group would still be desirable. In fact, three very recent reports have shown that the use of inhaled steroids can reduce disease progression in mostly asymptomatic COVID-19 patients treated at home [8–11]. The results of the current RCT extend these previous observations on the use of inhaled steroids in the community to patients hospitalised because of COVID-19 pneumonia. Future studies may also need to explore the efficacy and safety of higher doses of inhaled budesonide (800 µg/12 h), as previously investigated in milder patients at home [8].

In conclusion, the results of this RCT suggest that the addition of inhaled budesonide (400 µg/12 h) on top of usual care in patients hospitalised because of COVID-19 pneumonia is safe and may reduce the risk of disease progression.

Acknowledgments

Acknowledgments: Authors thank all participants in the study for their willingness to contribute to medical research, and the Barcelona Respiratory Network (www.brn.cat) to facilitate collaborative research. We also acknowledge the support of the Clinical Trial Unit (L. Aparicio, JA Arnaiz), the Medical Statistics Core Facility (F. Torres, G. Domenech) of IDIBAPS-Hospital Clinic Barcelona in Spain, the members of the DSMB (Drs. B. Cosio, JM. Miro, F. Barbe, F. Torres) as well as Klixar in Argentina (F. Licastro), for their support during the conduct of the trial and analysis of results. Finally, we acknowledge the economic and logistic support of AstraZeneca (Dra. Ana Perez and Dr. Gonzalo de Miquel).

Footnotes

  • Support statement: TACTIC was an investigator-initiated trial supported by AstraZeneca. AstraZeneca; DOI: http://dx.doi.org/10.13039/100004325.

  • Data availability: This trial complies with all the requirements of the ICMJE guidelines.

  • Conflict of interest: Dr. Agustí declares grant support from AstraZeneca, GlaxoSmithKline and Menarini; consulting fees and payment or honoraria from AstraZeneca, Chiesi and GlaxoSmithKline; and payment or honoraria from Menarini, all in the 36 months prior to manuscript submission.

  • Conflict of interest: Dr. De Stefano declares no additional competing interests.

  • Conflict of interest: Dr. Levi declares no additional competing interests.

  • Conflict of interest: Dr. Muñoz declares grant support from AstraZeneca, GlaxoSmithKline and Sanofi; consulting fees and support for attending meetings and/or travel from AstraZeneca, GlaxoSmithKline and Novartis; payment or honoraria from AstraZeneca, GlaxoSmithKline, Boehringer Ingelheim and Sanofi; and participation on a Data Safety Monitoring Board or Advisory Board for GlaxoSmithKline and Chiesi, all in the 36 months prior to manuscript submission.

  • Conflict of interest: Dr. Romero-Mesones declares no additional competing interests.

  • Conflict of interest: Dr. Sibila declares no additional competing interests.

  • Conflict of interest: Dr. Lopez-Giraldo declares no additional competing interests.

  • Conflict of interest: Dr. Moral declares grant support from AstraZeneca, GlaxoSmithKline and Sanofi; consulting fees from AstraZeneca, GlaxoSmithKline and Novartis; payment or honoraria from AstraZeneca, GlaxoSmithKline, Boehringer Ingelheim and Chiesi; payment for expert testimony from AstraZeneca and Chiesi; support for attending meetings and/or travel from AstraZeneca and Chiesi; and participation on a Data Safety Monitoring Board or Advisory Board for GlaxoSmithKline, Chiesi and AstraZeneca, all in the 36 months prior to manuscript submission.

  • Conflict of interest: Dr. Curto declares no additional competing interests.

  • Conflict of interest: Dr. Echazarreta declares no additional competing interests.

  • Conflict of interest: Dr. Márquez declares no additional competing interests.

  • Conflict of interest: Dr. Pascual-Guàrdia declares no additional competing interests.

  • Conflict of interest: Dr. Santos declares no additional competing interests.

  • Conflict of interest: Dr. Marin declares no additional competing interests.

  • Conflict of interest: Dr. Valdés declares no additional competing interests.

  • Conflict of interest: Dr. Saldarini declares no additional competing interests.

  • Conflict of interest: Dr. Salgado declares no additional competing interests.

  • Conflict of interest: Dr. Casanovas declares no additional competing interests.

  • Conflict of interest: Dr. Varea declares no additional competing interests.

  • Conflict of interest: Dr. Ríos declares no additional competing interests.

  • Conflict of interest: Dr. Faner declares grant support from AstraZeneca, GlaxoSmithKline and Menarini, in the 36 months prior to manuscript submission.

  • Received November 30, 2021.
  • Accepted December 28, 2021.
  • Copyright ©The authors 2022.
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Add-on inhaled budesonide in the treatment of hospitalised patients with COVID-19: a randomised clinical trial
Alvar Agustí, Gaston De Stefano, Alberto Levi, Xavier Muñoz, Christian Romero-Mesones, Oriol Sibila, Alejandra Lopez-Giraldo, Vicente Plaza Moral, Elena Curto, Andrés L. Echazarreta, Silvana E. Márquez, Sergi Pascual-Guàrdia, Salud Santos, Alicia Marin, Luis Valdés, Fernando Saldarini, Clara Salgado, Georgina Casanovas, Sara Varea, José Ríos, Rosa Faner
European Respiratory Journal Jan 2022, 2103036; DOI: 10.1183/13993003.03036-2021

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Add-on inhaled budesonide in the treatment of hospitalised patients with COVID-19: a randomised clinical trial
Alvar Agustí, Gaston De Stefano, Alberto Levi, Xavier Muñoz, Christian Romero-Mesones, Oriol Sibila, Alejandra Lopez-Giraldo, Vicente Plaza Moral, Elena Curto, Andrés L. Echazarreta, Silvana E. Márquez, Sergi Pascual-Guàrdia, Salud Santos, Alicia Marin, Luis Valdés, Fernando Saldarini, Clara Salgado, Georgina Casanovas, Sara Varea, José Ríos, Rosa Faner
European Respiratory Journal Jan 2022, 2103036; DOI: 10.1183/13993003.03036-2021
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