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Focused lung ultrasound to predict respiratory failure in patients with symptoms of COVID-19: a multicentre prospective cohort study

Søren Helbo Skaarup, Rasmus Aagaard, Stig Holm Ovesen, Jesper Weile, Hans Kirkegaard, Caroline Espersen, Mats Christian Højbjerg Lassen, Kristoffer Grundtvig Skaarup, Stefan Posth, Christian B. Laursen, Ask Bock, Michael Dan Arvig, Tor Biering-Sørensen
ERJ Open Research 2022 8: 00128-2022; DOI: 10.1183/23120541.00128-2022
Søren Helbo Skaarup
1Department of Respiratory Diseases and Allergy, Aarhus University Hospital, Denmark
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  • For correspondence: soeska@rm.dk
Rasmus Aagaard
2Department of Anaesthesiology, Randers Regional Hospital, Denmark
3Research Center for Emergency Medicine, Aarhus University Hospital and Aarhus University, Denmark
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Stig Holm Ovesen
3Research Center for Emergency Medicine, Aarhus University Hospital and Aarhus University, Denmark
4Emergency Department, Horsens Regional Hospital, Denmark
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Jesper Weile
5Department of Emergency Medicine, Aarhus University Hospital, Denmark
6Research Center for Emergency Medicine, Aarhus University Hospital, Denmark
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Hans Kirkegaard
3Research Center for Emergency Medicine, Aarhus University Hospital and Aarhus University, Denmark
7Department of Emergency Medicine, Aarhus University Hospital, Denmark
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Caroline Espersen
8Department of Cardiology, Herlev & Gentofte University Hospital, Denmark
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Mats Christian Højbjerg Lassen
8Department of Cardiology, Herlev & Gentofte University Hospital, Denmark
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Kristoffer Grundtvig Skaarup
8Department of Cardiology, Herlev & Gentofte University Hospital, Denmark
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Stefan Posth
9Department of Emergency Medicine, Odense University Hospital, Denmark
10Department of Clinical Research, University of Southern Denmark, Denmark
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Christian B. Laursen
11Department of Respiratory Medicine, Odense University Hospital, Denmark
12Odense Respiratory Research Unit (ODIN), Department of Clinical Research, University of Southern Denmark, Denmark
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Ask Bock
13Copenhagen University Hospital – North Zealand, Hillerød, Denmark
14Department of Emergency Medicine, Odense University Hospital, Denmark
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Michael Dan Arvig
15Department of Emergency Medicine, Slagelse Hospital, Denmark
16Department of Clinical Medicine, University of Copenhagen, Denmark
17Department of Clinical Research, University of Southern Denmark, Denmark
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Tor Biering-Sørensen
8Department of Cardiology, Herlev & Gentofte University Hospital, Denmark
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Figures

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  • FIGURE 1
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    FIGURE 1

    Median focused lung ultrasound (FLUS) scores for the different end-points. Statistically significant higher FLUS score was found in patients who received mechanical ventilation (p<0.001), were admitted to intensive care (p<0.001), were treated with high-flow oxygen (p<0.001), who died of COVID-19 (p=0.004) and who died of any cause (p=0.01).

  • FIGURE 2
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    FIGURE 2

    Correlation and Bland–Altman plot of median focused lung ultrasound (FLUS) scores in randomly selected patients by two blinded observers. Little and clinically insignificant difference in scores is seen even though there is a trend (α: 0.36, p=0.01) with increasing difference as median FLUS score increases.

  • FIGURE 3
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    FIGURE 3

    Receiver operating characteristics of different scorings systems. The median focused lung ultrasound (FLUS) score and total sum from all zones and the median FLUS score from the anterior and lateral zones had higher area under the curve than other scoring systems.

Tables

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  • TABLE 1

    Demographic, vital parameters, blood test results and end-points in the study population

    VariableObservations, NMean±sd, n (%) or %
    Study information
     Patients included in study415
     Patients excluded due to no lung ultrasound film clips available analysis17
     Patients analysed39896
      Site 120150.5
      Site 28220.6
      Site 36917.3
      Site 44611.6
    Demographics
     Age years38767.8±15.8
     Weight kg24278.4±19.7
     Height cm246171.6±10.1
     Sex, female398189 (47.5)
    Clinical data
     Systolic blood pressure mmHg386130.7±22.0
     Diastolic blood pressure mmHg38374.5±13.5
     Peripheral oxygen saturation %38795.3±3.3
     Heart rate beats·min−138185.1±18.4
     Respiratory frequency breaths·min−138620.3±5.1
     Supplementary oxygen doses L·min−13641.7±3.3
    Biochemical data
     Ferritin μg·L−1175986.0±1183.6
     Haemoglobin mmol·L−13847.7±1.4
     C-reactive protein mg·L−138164±66
     Leukocytes, count ×109 L−13859.0±5.1
     Lymphocytes, count ×109 L−13741.4±1.3
     Monocytes, count ×109 L−12990.6±0.4
     Neutrophils, count ×109 L−13796.7±4.6
     Estimated glomerular filtration rate mL·min−127269.6±23.3
     Carbamide mmol·L−12917.2±5.8
     Creatinine μmol·L−138598.0±92.3
     Natrium mmol·L−1385138.5±4.2
     Potassium mmol·L−13823.8±0.5
     Fibrin D-dimer mg·L−1 (FEU)2632.4±4.6
     Pro-brain natriuretic peptide ng·L−1155706.4±2418.1
     Troponin I (HS) ng·L−175211.0±1120.1
     Troponin T (HS) ng·L−19368.9±349.1
     Glucose mmol·L−12497.4±3.0
     Haemoglobin A1c mmol·mol−116044.5±13.2
     pH-arterial3017.5±0.1
     PaCO2 kPa2975.0±1.3
     PaO2 kPa13210.2±3.1
     Base excess mmol·L−11331.3±4.8
     Hydrogen carbonate mmol·L−130025.2±4.7
     Lactate-arterial mmol·L−12751.5±0.9
    Ultrasound equipment
     General Electric's Vivid S60398201 (51)
     General Electric's LogiQ S8398151 (38)
     Sonosite X-porte39846 (12)
     Phased array transducer with cardiography pre-set398201 (51)
     Curvilinear transducer with abdominal pre-set398197 (49)
    Outcome data
     COVID-19 positive PCR test398227 (57)
     Overall mortality 30 days after admission39847 (11.8)
     COVID-19-related mortality 30 days after admission39828 (7)
     Admission to intensive care39821 (5.3)
     COVID-19-positive admission to intensive care39819 (4.8)
     Ventilator treatment39818 (4.9)
     COVID-19-positive ventilator treatment care39817 (4.3)
     High-flow oxygen treatment39856 (14)
     COVID-19-positive, high-flow oxygen treatment39851 (12.8)
     Nasal oxygen treatment398159 (43.3)
     COVID-19-positive, nasal oxygen treatment398117 (29.4)

    FEU: fibrin-equivalent units; HS: high sensitivity; PaCO2: arterial carbon dioxide tension; PaO2: arterial oxygen tension.

    • TABLE 2

      Focused lung ultrasound (FLUS) scoring results from the thoracic scannings zones

      Scanning zoneFLUS score
      0. The pleural line is continuous and regular; horizontal artefacts are present1. The pleural line is indented; below the indent, vertical areas of white are visible2. The pleural line is broken; below the breaking point, small-to-large consolidated areas appear with associated areas of white below the consolidated area3. The scanned area shows dense and largely extended white lung with or without larger consolidationsMissing; no film recorded or ultrasound not performed in zone
      Right 1262 (65.8)59 (14.8)45 (11.3)29 (7.29)3 (0.75)
      Right 2250 (62.8)80 (20.1)43 (10.3)23 (4.8)2 (0.5)
      Right 3185 (45.5)67 (16.8)99 (24.9)22 (8.3)14 (3.5)
      Right 4197 (49.5)87 (21.9)69 (17.3)27 (6.7)18 (4.5)
      Right 570 (17.6)30 (7.5)27 (6.8)6 (1.5)265 (66.6)
      Right 698 (24.6)21 (5.3)11 (2.8)2 (0.5)266 (66.9)
      Right 7111 (27.9)15 (3.8)4 (1)2 (0.5)266 (66.8)
      Left 1276 (67.1)52 (13.1)50 (12.6)25 (6.3)4 (1)
      Left 2247 (62.1)60 (15.1)60 (15.1)23(5.8)8 (2)
      Left 3166 (41.7)74 (18.6)103 (25.9)42 (10.6)13 (3.3)
      Left 4200 (50.3)57 (14.3)81 (20.3)39 (9.8)21 (5.3)
      Left 582 (20.6)18 (4.5)23 (5.8)6 (1.5)269 (67.6)
      Left 699 (24.9)18 (4.5)14 (3.5)0 (0)267 (67.1)
      Left 7114 (28.6)11 (2.8)6 (1.5)0 (0)267 (67.1)

      Data presented as n (%).

      • TABLE 3

        Uni- and multivariate logistic regression analysis of capability to predict primary outcome and secondary outcomes of median focused lung ultrasound (FLUS) score

        Univariate logistic regressionMultivariate logistic regression
        Relative riskSE95% CIp-valueRelative riskSE95% CIp-value
        Mechanical ventilation2.840.751.69–4.77<0.0012.440.771.31–4.520.005
        Intensive care unit2.850.731.73–4.71<0.0012.550.761.42–4.60.002
        High-flow oxygen treatment2.060.271.59–2.66<0.0011.950.261.5–2.53<0.001
        30-day mortality due to COVID-191.770.371.17–2.670.0071.140.290.7–1.880.601
        30-day all-cause mortality1.510.241.10–2.060.010.950.220.61–1.510.853

        Age, sex, comorbidity and non-high-flow oxygen treatment are included as covariates in the multivariate analysis. In this analysis FLUS was the only variable that predicted need for mechanical ventilation, admission to intensive care unit and high-flow oxygen treatment. FLUS did not predict 30-day mortality or 30-day mortality due to COVID-19. Age was the only positive predictor for these in a multivariable logistic regression.

        • TABLE 4

          Uni- and multivariate logistic regression analysis of different focused lung ultrasound (FLUS) scoring systems’ capability to predict need for mechanical ventilation

          Univariate logistic regressionMultivariate logistic regression
          Relative riskSE95% CIp-valueRelative riskSE95% CIp-value
          Median FLUS score2.840.751.69–4.77<0.0012.440.771.31–4.520.005
          Highest FLUS score in any zone2.971.031.5–5.90.0022.220.81.1–4.510.028
          FLUS score >3 in any of the zones5.422.672.06–14.25<0.0013.541.841.27–9.830.015
          Count of FLUS zones scoring 31.480.041.4–1.58<0.0011.460.091.29–1.66<0.001
          Count of FLUS zones scoring 21.310.091.14–1.5<0.0011.380.111.18–1.61<0.001
          Median FLUS score, anterior and lateral zones only2.960.761.79–4.89<0.0012.630.771.47–4.690.001
          Total sum of FLUS1.120.021.09–1.17<0.0011.120.031.08–1.18<0.001

        Supplementary Materials

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          Please note: supplementary material is not edited by the Editorial Office, and is uploaded as it has been supplied by the author.

          Supplementary material 00128-2022.SUPPLEMENT

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        Focused lung ultrasound to predict respiratory failure in patients with symptoms of COVID-19: a multicentre prospective cohort study
        Søren Helbo Skaarup, Rasmus Aagaard, Stig Holm Ovesen, Jesper Weile, Hans Kirkegaard, Caroline Espersen, Mats Christian Højbjerg Lassen, Kristoffer Grundtvig Skaarup, Stefan Posth, Christian B. Laursen, Ask Bock, Michael Dan Arvig, Tor Biering-Sørensen
        ERJ Open Research Oct 2022, 8 (4) 00128-2022; DOI: 10.1183/23120541.00128-2022

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        Focused lung ultrasound to predict respiratory failure in patients with symptoms of COVID-19: a multicentre prospective cohort study
        Søren Helbo Skaarup, Rasmus Aagaard, Stig Holm Ovesen, Jesper Weile, Hans Kirkegaard, Caroline Espersen, Mats Christian Højbjerg Lassen, Kristoffer Grundtvig Skaarup, Stefan Posth, Christian B. Laursen, Ask Bock, Michael Dan Arvig, Tor Biering-Sørensen
        ERJ Open Research Oct 2022, 8 (4) 00128-2022; DOI: 10.1183/23120541.00128-2022
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