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Changes in pulmonary function and patient-reported outcomes during COVID-19 recovery: a longitudinal, prospective cohort study

Aditi S. Shah, Min Hyung Ryu, Cameron J. Hague, Darra T. Murphy, James C. Johnston, Christopher J. Ryerson, Christopher Carlsten, Alyson W. Wong
ERJ Open Research 2021 7: 00243-2021; DOI: 10.1183/23120541.00243-2021
Aditi S. Shah
1Division of Respiratory Medicine, Dept of Medicine, University of British Columbia, Vancouver General Hospital, Vancouver, Canada
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Min Hyung Ryu
1Division of Respiratory Medicine, Dept of Medicine, University of British Columbia, Vancouver General Hospital, Vancouver, Canada
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Cameron J. Hague
2Dept of Radiology, University of British Columbia, St Paul's Hospital, Vancouver, Canada
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Darra T. Murphy
2Dept of Radiology, University of British Columbia, St Paul's Hospital, Vancouver, Canada
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James C. Johnston
3Division of Respiratory Medicine, Dept of Medicine, University of British Columbia, BC Centre for Disease Control, Vancouver, Canada
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Christopher J. Ryerson
4Division of Respiratory Medicine, Dept of Medicine, University of British Columbia, Centre for Heart Lung Innovation, St Paul's Hospital, Vancouver, Canada
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Christopher Carlsten
1Division of Respiratory Medicine, Dept of Medicine, University of British Columbia, Vancouver General Hospital, Vancouver, Canada
5These authors contributed equally
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  • For correspondence: carlsten@mail.ubc.ca
Alyson W. Wong
4Division of Respiratory Medicine, Dept of Medicine, University of British Columbia, Centre for Heart Lung Innovation, St Paul's Hospital, Vancouver, Canada
5These authors contributed equally
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  • FIGURE 1
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    FIGURE 1

    Flow diagram of study enrolment.

  • FIGURE 2
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    FIGURE 2

    Patient-reported outcomes and pulmonary function measurements at 3 and 6 months after coronavirus disease 2019 (COVID-19) symptom onset. Each circle represents a patient, and the box represents the median and interquartile range. The y-axis shows the complete range of possible scores, and areas shaded in grey represent the normal range based on population adjusted norms where available. DLCO: diffusing capacity of the lung for carbon monoxide; EQ-5D: EuroQol- 5 Dimension; FEV1: forced expiratory volume in 1 s; FVC: forced vital capacity; PHQ-9: Patient Health Questionnaire-9; PSQI: Pittsburgh Sleep Quality Index; QoL: quality of life; UCSD: University of California, San Diego shortness of breath questionnaire; VAS: visual analogue scale.

  • FIGURE 3
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    FIGURE 3

    The effect of time on the association between radiological abnormalities and diffusing capacity of the lung for carbon monoxide (DLCO) at 3 and 6 months after coronavirus disease 2019 (COVID-19) symptom onset. The x-axis represents the log of each radiological score. This figure demonstrates the association between 3-month computed tomography (CT) scores (ground glass, reticulation and total CT scores) and DLCO % predicted. In each case, there is a negative relationship between the radiological abnormalities and DLCO % predicted. However, this negative relationship is attenuated over time, as demonstrated by the shallower slopes at 6 months compared to 3 months.

Tables

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  • TABLE 1

    Clinical characteristics and pulmonary function tests of patients hospitalised with coronavirus disease 2019 (COVID-19), 6 months after symptom onset

    FeaturesOverall cohortPatients with dyspnoea at 6 monthsp-value
    Unexplained dyspnoeaDyspnoea
    Subjects n731315
    Demographics
     Age years65 (53–72)49 (34–67)66 (59–76)0.02
     Male sex n (%)44 (60)4 (31)9 (60)0.12
     Ever-smoker n (%)23 (32)2 (15)8 (53)0.06
    Comorbidities n (%)
     Hypertension27 (37)5 (39)8 (53)0.43
     Diabetes19 (26)3 (23)5 (33)0.69
     Chronic pulmonary disease#10 (14)04 (27)0.10
     Coronary heart disease7 (10)03 (20)0.23
     Malignancy8 (11)1 (8)1 (7)1.00
     Chronic kidney disease6 (8)1 (8)2 (13)1.00
    Respiratory symptoms
     UCSD dyspnoea score9 (3–31)31 (17–40)35 (23–46)0.27
     Cough VAS mm20 (10–37)10 (9–10)30 (16–44)0.07
    Patient-reported outcome measures
     EQ-5D health utility0.9 (0.8–0.9)0.83 (0.77–0.87)0.83 (0.76–0.87)0.79
     EQ-5D VAS80 (75–90)75 (70–90)75 (65–85)0.50
     PSQI5 (2–9)
    (n=72)
    9 (6–12)
    (n=12)
    7 (5–9)0.28
     PHQ-91 (0–6)6 (2–10)5 (1–7)0.39
    Pulmonary function tests
     FEV1 % predicted91±15
    (n=72)
    88±1483±140.31
     FVC % predicted93±16
    (n=72)
    93±1181±150.03
     FEV1/FVC %84±12
    (n=72)
    84±1384±110.88
     TLC % predicted87±13
    (n=64)
    86±11
    (n=12)
    77±13
    (n=14)
    0.09
      DLCO % predicted79±18
    (n=70)
    88±963±14<0.001
    Transthoracic echocardiogram (n=72)
     LVEF %60 (60–65)60 (60–64)65 (60–65)0.29
     PASP mmHg27 (23–30)19 (23–34)27 (23–30)0.77

    Data are shown as mean±sd or median (IQR) unless otherwise stated. Data denoted in bold indicate p-value <0.05. Patients with dyspnoea (n=31) have been categorised into those with unexplained dyspnoea (i.e. UCSD >10 with DLCO ≥80% predicted) and those with dyspnoea (i.e. UCSD >10 with DLCO <80% predicted). There were three patients who did not have DLCO measurements and could not be categorised. Echocardiogram data are from 3 months after symptom onset. UCSD: University of California, San Diego shortness of breath questionnaire; VAS: visual analogue scale; EQ-5D: EuroQol- 5 Dimension; PSQI: Pittsburgh Sleep Quality Index; PHQ-9: Patient Health Questionnaire-9; FEV1: forced expiratory volume in 1 s; FVC: forced vital capacity; TLC: total lung capacity; DLCO: diffusing capacity of the lung for carbon monoxide; LVEF: left ventricular ejection fraction; PASP: pulmonary artery systolic pressure. #: asthma (n=3), COPD (n=4), interstitial lung disease (n=2) or previous pulmonary embolism (n=1).

    • TABLE 2

      Respiratory symptoms, patient-reported outcome measures and pulmonary function at 3 and 6 months after coronavirus disease 2019 (COVID-19) symptom onset

      3 months6 monthsMean or median difference95% CIp-value
      Respiratory symptoms
       UCSD dyspnoea score11 (3–26)9 (3–31)−1.0−4.0–2.00.53
       Cough VAS28 (8–60)20 (10–35)−4.6−18.7–8.40.41
      Patient-reported outcome measures
       PHQ-92 (1–6)1 (0–6)0.50–1.50.16
       PSQI5 (3–8)5 (2–9)0−1.0–1.50.81
       EQ-5D utility0.87 (0.79–0.95)0.90 (0.81–0.95)−0.022−0.1–0.0030.12
       EQ-5D VAS75 (68–90)80 (75–90)6.35.0–9.5<0.001
      Pulmonary function, % predicted
       FEV189±1691±161.3−0.8–3.40.21
       FVC90±1793±173.31.3–5.20.001
       FEV1/FVC87±1284±12−2.9−4.5–  −1.30.001
       TLC83±1487±133.82.2–5.5<0.001
        DLCO74±1780±175.73.6–7.8<0.001

      Data for 3 and 6 months are shown as mean±sd or median (IQR). Data denoted in bold indicate p-value <0.05. A paired t-test or Wilcoxon signed rank test were used to compare values between 3 and 6 months. UCSD: University of California, San Diego shortness of breath questionnaire; VAS: visual analogue scale; PHQ-9: Patient Health Questionnaire-9; PSQI: Pittsburgh Sleep Quality Index; EQ-5D: EuroQol- 5 Dimension; FEV1: forced expiratory volume in 1 s; FVC: forced vital capacity; TLC: total lung capacity; DLCO: diffusing capacity of the lung for carbon monoxide.

      • TABLE 3

        Predictors of change in respiratory outcomes and QoL between 3 and 6 months after coronavirus disease 2019 (COVID-19) symptom onset

        ModelOutcomePredictor (at 3 months)Coefficient95% CIp-valuePrespecified covariates
        1aDLCO % predictedGround glass score−2.2−5.9–1.40.23Sex, age, smoking pack-years
        Time0.8−0.5–2.00.21
        Ground glass score*Time0.60.05–1.20.03
        1bDLCO % predictedReticulation score−8.7−12.1–  −5.4<0.001Sex, age, smoking pack-years
        Time1.20.1–2.20.03
        Reticulation score*Time0.6−0.01–1.250.05
        1cDLCO % predictedTotal CT score−5.3−8.7–  −1.80.003Sex, age, smoking pack-years
        Time0.8−0.5–2.20.23
        Total CT score*Time0.5−0.04–1.050.07
        2aUCSDGround glass score0.8−3.4–5.00.69Sex, age, smoking pack-years
        Time−0.2−2.9–2.50.88
        Ground glass score*Time−0.1−1.4–1.10.87
        2bQoLGround glass score−0.003−0.05–0.040.89Sex, age, smoking pack-years
        Time−0.003−0.02–0.020.77
        Ground glass score*Time0.01−0.002–0.020.15
        3aUCSDUnexplained dyspnoea5.16−7.95–18.30.43Sex, age, smoking pack-years
        Time−0.45−1.98–1.080.56
        Unexplained dyspnoea*Time1.01−2.98–5.010.61
        3bQoLUnexplained dyspnoea0.01−0.11–0.130.88Sex, age, smoking pack-years
        Time0.01−0.001–0.020.07
        Unexplained Dyspnoea*Time−0.01−0.04–0.010.33

        Time was categorised as 3 months (reference) and 6 months from symptom onset. Ground glass, reticulation and total CT scores were continuous variables that were log-transformed to make them normally distributed and to meet model assumptions. Unexplained dyspnoea at 3 months (defined as the presence of a UCSD dyspnoea score >10 with DLCO % predicted ≥80%) was categorical (present or absent). Time was included as an interaction term to evaluate whether time modified the effect of the primary predictor on the outcome. The primary predictor variables are denoted in bold. Example of Model 1a interpretation: the coefficient of −2.2 for ground glass score indicates that each 1% increase in ground glass score is associated with a 2.2% decrease in DLCO % predicted. This association is modified by time. At 6 months, for each 1% increase in ground glass, the coefficient will increase by 1.4 (0.8+0.6), which means there will be a 0.8% (−2.2+1.4) decrease in DLCO % predicted at 6 months compared to a 2.2% decrease at 3 months. DLCO : diffusing capacity of the lung for carbon monoxide; UCSD: University of California, San Diego shortness of breath questionnaire; QoL: quality of life. Asterisks (*) signify interaction terms.

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        Changes in pulmonary function and patient-reported outcomes during COVID-19 recovery: a longitudinal, prospective cohort study
        Aditi S. Shah, Min Hyung Ryu, Cameron J. Hague, Darra T. Murphy, James C. Johnston, Christopher J. Ryerson, Christopher Carlsten, Alyson W. Wong
        ERJ Open Research Jul 2021, 7 (3) 00243-2021; DOI: 10.1183/23120541.00243-2021

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        Changes in pulmonary function and patient-reported outcomes during COVID-19 recovery: a longitudinal, prospective cohort study
        Aditi S. Shah, Min Hyung Ryu, Cameron J. Hague, Darra T. Murphy, James C. Johnston, Christopher J. Ryerson, Christopher Carlsten, Alyson W. Wong
        ERJ Open Research Jul 2021, 7 (3) 00243-2021; DOI: 10.1183/23120541.00243-2021
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