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Is asthma associated with COVID-19 infection? A UK Biobank analysis

Caroline J. Lodge, Alice Doherty, Dinh S. Bui, Raisa Cassim, Adrian J. Lowe, Alvar Agusti, Melissa A. Russell, Shyamali C. Dharmage
ERJ Open Research 2021 7: 00309-2021; DOI: 10.1183/23120541.00309-2021
Caroline J. Lodge
1Allergy and Lung Health Unit, Centre of Epidemiology and Biostatistics, Melbourne School of Population and Global Health, the University of Melbourne, Melbourne, VIC, Australia
6Equal first/senior
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  • For correspondence: clodge@unimelb.edu.au
Alice Doherty
1Allergy and Lung Health Unit, Centre of Epidemiology and Biostatistics, Melbourne School of Population and Global Health, the University of Melbourne, Melbourne, VIC, Australia
6Equal first/senior
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Dinh S. Bui
1Allergy and Lung Health Unit, Centre of Epidemiology and Biostatistics, Melbourne School of Population and Global Health, the University of Melbourne, Melbourne, VIC, Australia
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Raisa Cassim
1Allergy and Lung Health Unit, Centre of Epidemiology and Biostatistics, Melbourne School of Population and Global Health, the University of Melbourne, Melbourne, VIC, Australia
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Adrian J. Lowe
1Allergy and Lung Health Unit, Centre of Epidemiology and Biostatistics, Melbourne School of Population and Global Health, the University of Melbourne, Melbourne, VIC, Australia
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Alvar Agusti
2Centro de Investigation Biomédica en Red Enfermedades Respiratorias (CIBERES), Spain
3Institut d'Investigacions Biomediques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
4Respiratory Institute, Hospital Clinic, Barcelona, Spain
5University of Barcelona, Spain
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Melissa A. Russell
1Allergy and Lung Health Unit, Centre of Epidemiology and Biostatistics, Melbourne School of Population and Global Health, the University of Melbourne, Melbourne, VIC, Australia
6Equal first/senior
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Shyamali C. Dharmage
1Allergy and Lung Health Unit, Centre of Epidemiology and Biostatistics, Melbourne School of Population and Global Health, the University of Melbourne, Melbourne, VIC, Australia
6Equal first/senior
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    FIGURE 1

    Directed Acyclic Graph (DAG) identifying potential confounders for the relationship between asthma and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) positive test. An arrow from a factor to another means possible association. Red circles indicate variables that require adjustment to assess the relationship between exposure (asthma, green) and the outcome (SARS-CoV-2 test, blue).

Tables

  • Figures
  • TABLE 1

    Demographic characteristics amongst all UK Biobank individuals who attended an assessment centre and amongst UK Biobank individuals with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) test data

    All UK BiobankUK Biobank with SARS-CoV-2 test data
    Whole sampleWhole sample#PositiveNegative
    Subjects n502 505107 41217 979 (17%)89 433 (83%)
    Age at recruitment¶ (mean±sd)56.53±8.1056.70±8.2553.52±8.5857.33±8.03
    Age at SARS-CoV-2 test¶ (mean±sd)68.23±8.2364.69±8.5869.00±7.94
    Sex¶
     Female54.054.052.954.3
     Male45.645.947.145.7
    Ethnicity¶
     White94.193.689.594.5
     Mixed0.60.60.80.6
     Asian2.32.44.62.0
     Black1.61.82.91.5
     Other ethnic background1.31.31.91.2
    Ever asthma
     Yes12.613.914.113.9
     No87.085.685.485.7
    Asthma age of onset (if asthma yes)¶ (mean±sd)31.16±18.6931.67±18.8130.02±17.7132.02±19.02
    Asthma onset (if asthma yes)
     Early-onset (<13 years)36.936.534.936.8
     Late onset (≥13 years)63.163.565.163.2
    COPD diagnosis
     Yes0.30.40.30.5
     No23.823.118.324.0
    COPD age of onset59.52±9.2858.82±10.1858.39±9.6458.89±10.26
    Hay fever or eczema diagnosis (mean±sd)
     Yes23.624.023.624.1
     No75.975.675.975.5
    Hay fever or eczema age of onset¶25.21±16.1325.68±16.3924.46±15.1425.91±16.61
    Asthma medication (if asthma yes) (mean±sd)
     No asthma/COPD medications47.045.645.845.6
     Only non-steroidal medications15.414.814.714.8
     Steroid medications37.639.539.539.5
    Hay fever medication (if hay fever yes)
     No hay fever medication82.681.582.381.4
     Medication; no antihistamines7.27.57.37.6
    Antihistamines10.110.810.310.9
    Lung function+
     FEV1 at baseline, z-score¶0.37 (−0.32–1.08)0.41−0.29–1.12)0.44−0.27–1.16)0.40−0.30–1.11)
     FVC at baseline, z-score¶0.18 (−0.48–0.84)0.21 (−0.46–0.88)0.24 (−0.44–0.92)0.21 (−0.46–0.87)
     FEV1/FVC at baseline, z-score0.34 (−0.16–0.90)0.35 (−0.16–0.90)0.34 (−0.16–0.92)0.35 (−0.16–0.90)
    Household income GBP
      <18 00018.919.720.119.6
     18 000 to 30 99921.521.220.221.4
     31 000 to 51 99922.322.123.621.8
     52 000 to 100 00017.817.217.317.2
      >100 0004.95.14.45.3
    Education¶
     None of the following0.90.90.81.0
     College or University degree32.430.625.131.7
     A levels/AS levels or equivalent10.910.49.910.5
     O levels/GCSEs or equivalent20.821.022.420.7
     CSEs or equivalent5.35.58.84.8
     NVQ or HND or HNC or equivalent6.67.07.86.8
     Other professional qualifications5.25.34.85.5
    Smoking history¶
     Never54.452.252.952.0
     Past34.436.335.036.6
     Current10.510.811.510.7
    Smoking pack-years19.00 (10.00–32.00)19.88 (10.13–33.00)20.00 (10.50–33.00)19.88 (10.00–33.00)
    BMI¶ (mean±sd)27.43±4.8027.83±4.9628.29±5.1027.74±4.93
    White blood cell count¶6.65 (5.63–7.86)6.70 (5.69–7.90)6.73 (5.70–7.99)6.70 (5.69–7.90)
    Eosinophil count0.14 (0.10–0.21)0.14 (0.10–0.21)0.14 (0.10–0.22)0.14 (0.10–0.21)
    Close to major road
     Yes7.07.27.47.1
     No91.591.591.491.5
    Greenspace percentage, buffer 300 m¶29.53 (17.22–48.41)29.53 (17.17–48.21)27.44 (16.37–44.02)29.97 (17.35–49.11)

    Values are % of participants, mean±sd or median (interquartile range) unless stated otherwise. FEV1: forced expiratory volume in 1 s; FVC: forced vital capacity; BMI: body mass index. #: sample of UK Biobank with SAR-CoV-2 test data differs from whole UK Biobank cohort (p<0.05) in all parameters except greenspace percentage, buffer 300 m. ¶: all p-values are <0.001, except for FVC at baseline, z-score (p=0.002) and white blood cell count (p=0.008). p-values are comparing positive and negative test result: chi-square for categorical exposures, ANOVA for parametric and Mann–Whitney U-test (Wilcoxon rank sum test) for non-parametric analysis of variance for continuous variables. +: z-score means represent the mean standard deviation of lung function parameters compared with values for age-, sex- and race-matched individuals.

    • TABLE 2

      Adjusted association between asthma and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) positive test

      Percentage of positive tests (n/N)OR (95% CI) for a positive testp-value
      Ever asthma
       No16.6 (15 347/91 977)Ref
       Yes16.9 (2539/14 988)0.97 (0.92–1.02)0.28
      Asthma onset
       No asthma16.6 (15 347/91 977)Ref
       Early-onset (<13 years)16.2 (887/5469)0.91 (0.84–0.99)0.03
       Late onset (≥13 years)17.3 (1652/9519)1.00 (0.94–1.07)0.87

      Adjusted for age at recruitment, sex and baseline measures of: education, average household income, smoking history, BMI, ethnicity, white blood cell count, eosinophil count, close to major road and greenspaces buffer. Bold values indicate p-value <0.05.

      • TABLE 3

        The associations between asthma age-of-onset phenotypes and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) positive test by treatment and lung function

        Early onsetLate onset
        Percentage of positive tests (n/N)OR (95% CI) for a positive testPercentage of positive tests (n/N)OR (95% CI) for a positive test
        Asthma treatment
         No15.8 (491/3114)Ref18 (672/3727)Ref
         Treated with non-steroid17.3 (112/645)1.05 (0.81–1.36), p=0.6716.5 (261/1576)0.90 (0.75–1.08), p=0.26
         Treated with steroids16.6 (284/1710)1.18 (0.98–1.42), p=0.0717.1 (719/4216)1.04 (0.91–1.19), p=0.55
        Quartiles of baseline FEV1
         Q1 of FEV1 (lowest quartile)12.4 (70/562)Ref18.3 (190/1035)Ref
         Q2 of FEV116.7 (120/715)1.25 (0.88–1.79), p=0.2015.2 (203/1332)0.81 (0.64–1.03), p=0.09
         Q3 of FEV114.8 (145/976)1.22 (0.87–1.72), p=0.2316.9 (280/1653)0.92 (0.73–1.15), p=0.48
         Q4 of FEV116.7 (310/1851)1.44 (1.05–1.72), p=0.0217.4 (516/2962)0.90 (0.73–1.15), p=0.36

        FEV1: forced expiratory volume in 1 s.

        • TABLE 4

          The associations between asthma onset phenotypes and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) positive test stratified by sex, baseline smoking, obesity and ethnicity (NEW)

          Percentage of positive tests (n/N)OR (95% CI) for a positive testPercentage of positive tests (n/N)OR (95% CI) for a positive testp-value for interaction
          MaleFemaleSex
          Asthma onset0.53
           No asthma17.2 (7374/42 981)Ref16.3 (7973/48 996)Ref
           Early-onset (<13 years)15.5 (417/2684)0.86 (0.76–0.97), p=0.0116.8 (470/2785)0.94 (0.83–1.06), p=0.330.29
           Late onset (≥13 years)18.1 (626/3464)1.00 (0.91–1.11), p=0.8816.9 (1023/6055)0.99 (0.92–1.08), p=0.950.75
          Never smokedEver smokedSmoking
          Asthma onset0.71
           No asthma16.9 (8156/48 191)Ref16.4 (7152/43 479)Ref
           Early-onset (<13 years)16.5 (495/3003)0.87 (0.78–0.98), p=0.0216.0 (399/2497)0.94 (0.84–1.07), p=0.400.45
           Late onset (≥13 years)17.4 (819/4711)1.00 (0.91–1.09), p=0.8617.2 (793/4589)1.00 (0.91–1.09), p=0.970.79
          Normal weightOverweight/ObeseBMI
          Asthma onset0.03
           No asthma14.8 (4202/28 226)Ref17.4 (11 036/63 271)Ref
           Early-onset (<13 years)16.1 (264/1634)1.09 (0.94–1.27), p=0.2216.2 (625/3854)0.85 (0.77–0.93), p=0.0010.01
           Late onset (≥13 years)14.4 (330/2280)0.94 (0.82–1.08), p=0.4318.2 (1293/7070)1.02 (0.94–1.09), p=0.590.41
          Non-blackBlackEthnicity
          Asthma onset0.32
           No asthma16.5 (14 900/90 327)Ref27.1 (444/1637)Ref
           Early-onset (<13 years)15.9 (859/5389)0.90 (0.82–0.98), p=0.0134.6 (27/78)1.54 (0.90–2.6), p=0.110.14
           Late onset (≥13 years)17.1 (1601/9355)0.99 (0.93–1.06), p=0.8931.1 (51/164)1.18 (0.79–1.7), p=0.400.67

          Adjusted for age at recruitment, sex, and baseline measures of: education, average household income, smoking history, BMI, ethnicity, white blood cell count, eosinophil count, close to major road and greenspaces buffer. Bold values indicate p-value <0.05.

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          Is asthma associated with COVID-19 infection? A UK Biobank analysis
          Caroline J. Lodge, Alice Doherty, Dinh S. Bui, Raisa Cassim, Adrian J. Lowe, Alvar Agusti, Melissa A. Russell, Shyamali C. Dharmage
          ERJ Open Research Oct 2021, 7 (4) 00309-2021; DOI: 10.1183/23120541.00309-2021

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          Is asthma associated with COVID-19 infection? A UK Biobank analysis
          Caroline J. Lodge, Alice Doherty, Dinh S. Bui, Raisa Cassim, Adrian J. Lowe, Alvar Agusti, Melissa A. Russell, Shyamali C. Dharmage
          ERJ Open Research Oct 2021, 7 (4) 00309-2021; DOI: 10.1183/23120541.00309-2021
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