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Pulmonary function and radiological features four months after COVID-19: first results from the national prospective observational Swiss COVID-19 lung study

Sabina A. Guler, Lukas Ebner, Catherine Beigelman, Pierre-Olivier Bridevaux, Martin Brutsche, Christian Clarenbach, Christian Garzoni, Thomas K. Geiser, Alexandra Lenoir, Marco Mancinetti, Bruno Naccini, Sebastian R. Ott, Lise Piquilloud, Maura Prella, Yok-Ai Que, Paula M. Soccal, Christophe von Garnier, Manuela Funke-Chambour
European Respiratory Journal 2021; DOI: 10.1183/13993003.03690-2020
Sabina A. Guler
1Department of Pulmonary Medicine, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
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Lukas Ebner
2Department of Diagnostic, Interventional and Pediatric Radiology, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
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Catherine Beigelman
3Radiodiagnostic and Interventional Radiology, CHUV-University Hospital, Lausanne, Switzerland
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Pierre-Olivier Bridevaux
4Service de Pneumologie, Hôpital du Valais, Sion, Switzerland
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Martin Brutsche
5Lung Center, Kantonsspital St. Gallen, St. Gallen, Switzerland
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Christian Clarenbach
6Pneumology, University Children Hospital Zurich, Zurich, Switzerland
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Christian Garzoni
7Clinic of Internal Medicine and Infectious Diseases, Clinica Luganese Moncucco, Lugano, Switzerland
8Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern, Switzerland
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Thomas K. Geiser
1Department of Pulmonary Medicine, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
9Department for BioMedical Research, University of Bern, Bern, Switzerland
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Alexandra Lenoir
10Division of Pulmonary Medicine, Lausanne University Hospital (CHUV), University of Lausanne, Lausanne, Switzerland
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Marco Mancinetti
11Department of Internal Medicine, University and Hospital of Fribourg, Fribourg, Switzerland
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Bruno Naccini
12Department of Pulmonary medicine, Clinica Luganese Moncucco, Lugano, Switzerland
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Sebastian R. Ott
13Department of Pulmonary Medicine, St. Claraspital AG, Basel, Switzerland
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Lise Piquilloud
14Adult Intensive care unit, University Hospital and University of Lausanne, Lausanne, Switzerland
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Maura Prella
10Division of Pulmonary Medicine, Lausanne University Hospital (CHUV), University of Lausanne, Lausanne, Switzerland
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Yok-Ai Que
15Department of Intensive Care Medicine, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
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Paula M. Soccal
16Division of Pulmonary Medicine, Geneva University Hospitals, Geneva
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Christophe von Garnier
10Division of Pulmonary Medicine, Lausanne University Hospital (CHUV), University of Lausanne, Lausanne, Switzerland
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Manuela Funke-Chambour
1Department of Pulmonary Medicine, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
9Department for BioMedical Research, University of Bern, Bern, Switzerland
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Figures

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  • FIGURE 1
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    FIGURE 1

    PRISMA flow diagram of the study.

  • FIGURE 2
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    FIGURE 2

    Variables associated with past COVID-19 disease severity. Association of demographic and functional parameters with mild/moderate and severe/critical COVID-19 disease. OR and corresponding 95%CI from unadjusted analysis (orange) and individual multivariable models for each parameter adjusting for confounding by age and sex (green).

  • FIGURE 3
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    FIGURE 3

    Characteristic radiological changes of a patient with severe sequelae 3 months after COVID-19 pneumonia. Extensive involvement of both lungs is present in a patient 3 months after a severe COVID-19 pneumonia. Diffuse mosaic attenuation pattern in all lung lobes seen on axial 1 mm-thick CT (a) and 10 mm-thick minimum intensity projection (mIP) slices, 1 mm-thick CT (c) and 10 mm-thick minimum intensity projection (mIP) sagittal reformats (d) in lung windowing. This combines classical features of lung fibrosis with architectural distortion, reticulations, honeycombing (arrowhead in A) and traction bronchiectasis (orange arrows in a−d), as well as sharply demarcated areas of low attenuation in both lungs (orange circles in a−d). Clusters of contiguous hypoattenuating lobules and traction bronchiectasis are better visualised on mIP images with narrow window settings (b and d). Note the bulging of the interlobular septae (b and d, blue curved arrows) as well as the subpleural pneumatocele in c and d.

Tables

  • Figures
  • TABLE 1

    Baseline characteristics and follow-up findings in patients with severe/critical and mild /moderate COVID-19

    COVID-19 survivorsSevere/critical disease (n=66)Mild/moderate disease (n=47)
    Number (%), mean (sd), median (IQR)p-value#
    CHARACTERSTICS AT BASELINE
    Gender, men/women40/2627/200.89
    Age, years60.3 (12.0)52.9 (10.9)<0.001
    Ever smokers %¶56%37%0.16
    Body mass index, kg/m229.8 (5.7)25.5 (4.7)0.02
    D-Dimers, µg/L+1011 (366–1989)387 (1–658)0.26
    Mechanical ventilation#71%––
    Duration of mechanical ventilation, days#11.9 (9.5–18)––
    COMORBIDITIES
    Interstitial lung disease6%3%0.58
    COPD12%3%0.18
    Asthma9%19%0.32
    Arterial hypertension55%8%0.003
    Diabetes35%0%0.04
    GERD10%9%1
    Sleep apnea16%3%0.09
    Chronic heart failure10%9%1
    Chronic renal failure19%0%0.009
    Cancer6%5%1
    Depression or antiety12%7%0.66
    PULMONARY FUNCTION AT FOLLOW-UP (n=72)
    FEV/FVC, %94.7 (13.7)84.2 (14.3)<0.001
    TLC, L5.22 (1.5)6.5 (1.6)0.050
    TLC, % predicted86.0 (20.0)102.0 (19.3)0.047
    FVC, L3.28 (1.01)4.12 (1.2)<0.001
    FVC, % predicted86.6 (20.1)95.6 (17.9)0.02
    FEV1, L2.64 (0.8)3.34 (1.1)<0.001
    FEV1, % predicted89.4 (20.7)94.0 (15.6)0.19
    DLCO, % predicted73.2 (18.4)95.3 (20.6)0.003
    PImax, kPa10.3 (8.8)8.1 (2.6)0.14
    PEmax, kPa8.7 (3.3)10.3 (4.1)0.20
    OXYGENATION AT FOLLOW-UP (n=72)
    paO2, mmHg79.0 (12.2)87.5 (9.0)0.0002
    6-MWD, meters456 (105)576 (78)0.001
    O2 nadir on 6MWT90 (4.5)93 (3.1)0.001
    O2 desaturation 6MWT5.6 (3.8)2.6 (3.1)0.02

    #p-values from two-sample t-tests, Wilcoxon Rank Sum test, chi square test, or Fisher's Exact Test.

    ¶38 missing,.

    +59 missing, *11 missing.

    Abbreviations: COPD: chronic obstructive pulmonary disease; CT: computed tomography DLCO: diffusing capacity of the lung for carbon monoxide; FEV1: forced vital capacity in 1 min; FVC: forced vital capacity; GERD: gastroesophageal reflux disease; paO2: arterial partial pressure of oxygen; PImax: maximal inspiratory pressure; PEmax: maximal expiratory pressure; TLC: total lung capacity; 6MWD: 6-min walk distance; 6MWT: 6-min walk test.

    • TABLE 2

      Complete clinical multivariable model for severe/critical disease

      OR (95% CI)p-value*
      DLCO, 10%-pred.0.59 (0.37–0.87)0.01
      Age, year0.98 (0.92–1.05)0.62
      Sex, men1.98 (0.50–8.56)0.34
      BMI, kg/m21.19 (1.03–1.41)0.02
      6MWD, 10 m0.88 (0.67–0.95)0.01
      Min. SpO2, %0.80 (0.44–0.95)0.07

      Effect estimates indicate the associations of the variables with severe/critical disease in the context of the complete multivariable model. E.g. for every 10 meters increase in 6MWD the odds for severe/critical disease decreases by 12% adjusting for age, sex, BMI, DLCO, and minimal SpO2. The overall area under the receiver operating curve (AUC) of the multivariable model including DLCO, age, sex, BMI, 6MWD, and minimal SpO2 was 0.95 (95% CI 0.88–1.00).

      Abbreviations: AUC: area under the receiver operating curve; BMI: body mass index; CI: confidence interval; DLCO: diffusing capacity of the lung for carbon monoxide; OR: odds ratio; 6MWD: 6-min walk distance; min. SpO2: minimal oxygen saturation on 6-min walk test.

      • TABLE 3

        Unadjusted and adjusted association of radiological features with previous severe/critical COVID-19

        Radiological signUnadjustedAdjusted for age and sex
        OR (95% CI)p#OR (95% CI)p#
        Hypoattenuation13.5 (2.1–265)0.0211.7 (1.7–239)0.03
        Reticulations10.1 (1.6–198)0.048.73 (1.3–174)0.06

        #p-value for the radiological sign.

        Odds ratios indicate the associations of the radiological variables at follow-up with severe/critical disease. E.g. the odds of severe/critical disease is 11.7 times higher for a patient with than for a patient without hypoattenuation, adjusting for age and sex.

        Abbreviations: CI: confidence interval; COVID-19: coronavirus disease 2019; DLCO: diffusing capacity of the lung for carbon monoxide, OR: odds ratio.

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        Pulmonary function and radiological features four months after COVID-19: first results from the national prospective observational Swiss COVID-19 lung study
        Sabina A. Guler, Lukas Ebner, Catherine Beigelman, Pierre-Olivier Bridevaux, Martin Brutsche, Christian Clarenbach, Christian Garzoni, Thomas K. Geiser, Alexandra Lenoir, Marco Mancinetti, Bruno Naccini, Sebastian R. Ott, Lise Piquilloud, Maura Prella, Yok-Ai Que, Paula M. Soccal, Christophe von Garnier, Manuela Funke-Chambour
        European Respiratory Journal Jan 2021, 2003690; DOI: 10.1183/13993003.03690-2020

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        Pulmonary function and radiological features four months after COVID-19: first results from the national prospective observational Swiss COVID-19 lung study
        Sabina A. Guler, Lukas Ebner, Catherine Beigelman, Pierre-Olivier Bridevaux, Martin Brutsche, Christian Clarenbach, Christian Garzoni, Thomas K. Geiser, Alexandra Lenoir, Marco Mancinetti, Bruno Naccini, Sebastian R. Ott, Lise Piquilloud, Maura Prella, Yok-Ai Que, Paula M. Soccal, Christophe von Garnier, Manuela Funke-Chambour
        European Respiratory Journal Jan 2021, 2003690; DOI: 10.1183/13993003.03690-2020
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