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Detection and diagnosis of large airway collapse: a systematic review

Alexandros Mitropoulos, Woo-Jung Song, Fatma Almaghlouth, Samuel Kemp, Michael Polkey, James H. Hull
ERJ Open Research 2021 7: 00055-2021; DOI: 10.1183/23120541.00055-2021
Alexandros Mitropoulos
1Dept of Respiratory Medicine, Royal Brompton Hospital, London, UK
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Woo-Jung Song
2Dept of Allergy and Clinical Immunology, Asan Medical Centre, University of Ulsan College of Medicine, Seoul, Korea
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Fatma Almaghlouth
3National Heart and Lung Institute, Imperial College, London, UK
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Samuel Kemp
1Dept of Respiratory Medicine, Royal Brompton Hospital, London, UK
3National Heart and Lung Institute, Imperial College, London, UK
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Michael Polkey
1Dept of Respiratory Medicine, Royal Brompton Hospital, London, UK
3National Heart and Lung Institute, Imperial College, London, UK
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James H. Hull
1Dept of Respiratory Medicine, Royal Brompton Hospital, London, UK
3National Heart and Lung Institute, Imperial College, London, UK
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  • FIGURE 1
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    FIGURE 1

    PRISMA flow chart for study selection.

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    FIGURE 2

    Study cut-off thresholds reported for the diagnosis of large airway collapse, based on diagnostic modality. CSA: cross-sectional area; CT: computed tomography; MRI: magnetic resonance imaging.

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    FIGURE 3

    Forest plot of the prevalence of large airway collapse in healthy subjects. Random effects meta-analysis was done to estimate the pooled prevalence. Details of included studies, including population, diagnostic modality and threshold, are summarised in table 1.

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    FIGURE 4

    Forest plot of the prevalence of large airway collapse in patients with chronic obstructive airway diseases (either COPD or asthma). Random effects meta-analysis was done to estimate the pooled prevalence. Details of included studies, including population, diagnostic modality, and threshold, are summarised in table 2. AE: acute exacerbation.

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  • TABLE 1

    Bronchoscopic studies

    First author/yearStudy purpose and designPopulationDiagnostic modalityDiagnostic criteriaFindingsDiscussion
    Majid et al. 2014 [19]Prospective single-centre study
    Assessing inter- and intra-observer agreement in LAC
    10 patients (males (n=4), females (n=6); mean age: 65 years, age range: 43–74 years) with various conditionsDynamic flexible bronchoscopyTBM or EDAC ≥50% reduction in the anteroposterior diameterTBM was found in 70% of patientsThere is intra- and interobserver agreement among pulmonologists and trainees with various levels of experience in the evaluation of LAC
    Dal Negro et al. 2013 [7]Prospective single-centre study
    Assessing the prevalence of both TBM and EDAC
    202 asthmatics (males (n=91), females (n=111); age: 47.5±13.3 years), and 62 subjects without any obstructive disease (males (n=38), females (n=24); age: 38.9±10.4 years)Dynamic flexible bronchoscopyTBM or EDAC >50% of airway collapseTBM and particularly EDAC prevalence are related to asthma severityThe presence of TBM or EDAC should be considered when bronchial asthma persists despite appropriate pharmacological treatment
    Murgu & Colt, 2007 [18]Retrospective single-centre study
    Assessing a multidimensional classification system (FEMOS) for evaluating patients with expiratory LAC
    18 patients (males (n=13), females (n=5); 4 with EDAC and 14 with TBM)Rigid bronchoscopyLAC, normal <50%, mild, 50–75%; moderate, 75–100%; and severe, 100% and the airway walls make contactEDAC and TBM were found in 22.2% and 77.8%, respectivelyUsing FEMOS, the morphologies and aetiologies of LAC can be identified and stratified objectively based on the degree of functional impairment, extent of disease and severity of airway collapse

    LAC: large airway collapse; TBM: tracheobronchomalacia; EDAC: excessive dynamic airway collapse.

    • TABLE 2

      Computed tomographic and magnetic resonance imaging studies

      First author/yearStudy purpose and designPopulationDiagnostic modalityDiagnostic criteriaFindingsDiscussion
      Bezuidenhout et al. 2019 [51]Retrospective single-centre study
      To evaluate patients with TBM after undergoing tracheobronchoplasty
      18 patients (males (n=5), females (n=13); mean age: 65±12 years) with COPD (n=7), GERD (n=14), OSA (n=8), cardiac disease (n=4)8-, 16- and 64-MDCT scanLAC ≥70% reduction in the CSAMean tracheal collapsibility improved by 34% in post-operative CTDynamic CT could play an important role in assessing response to tracheobronchoplasty
      Nygaard et al. 2019 [29]Retrospective/prospective single-centre study
      To assess TM over time (2 CT scans) in patients with excessive tracheal collapse
      20 patients with respiratory diseases (males (n=6), females (n=14); mean age: 68 years)high-resolution
      MDCT scan
      TM ≥50% reduction in the CSASeven patients showed a tracheal collapse progression (>10% difference) between the scansTracheal collapse regressed in half of the patients over a time period of 2 years
      Ciet et al. 2017 [31]Prospective single-centre study
      Comparison of MRI to MDCT in assessing TBM
      12 participants (males (n=5), females (n=7); 9 healthy adults and 3 patients with COPD; mean age: 64.5 years, age range: 45–77 years)1.5-T Signa MRI
      64-MDCT scan
      Criterion was not definedTM was 52% and 77% and BM was 55% and 63% during FVC for healthy and COPD patients, respectivelyMRI was found to be a technically feasible alternative to MDCT for assessing TBM
      Nygaard et al. 2017 [30]Retrospective single-centre study
      To compare four different image analysis methods for the diagnosis of tracheal collapse using MDCT
      353 patients (males (n=150), females (n=191), mean age: 60 years, age range: 18–88 years) with respiratory diseases (e.g. COPD, ILD, bronchiectasis)64-MDCT scanLAC >50% and >80% reduction in the CSALAC prevalence was ∼15.1% when using >50% as a thresholdThe different image analysis methods identified LAC in different patients. Thus, the diagnosis of LAC should not solely rely on MDCT images
      Leong et al. 2017 [6]Prospective single-centre study
      To explore the prevalence of ECAC in stable and acute exacerbations COPD (AECOPD) patients
      40 COPD patients (males (n=19), females (n=21); age: 70.1±8.2 years); 64 AECOPD (males (n=40), females (n=24); age: 70.2±11.6 years); 53 healthy volunteers (males (n=35), females (n=18); age: 56.6±16.9 years)320-slice dynamic MDCTLAC >50%, >75% and >80% reduction in the CSA were comparedECAC was observed in 35% of COPD, 39% of AECOPD and no healthy individuals when a >50% was used as a criterionECAC can be present in up to one third of patients with stable COPD, and the abnormality does not seem to be worsened during AECOPD
      Bhatt et al. 2016 [44]Retrospective multicentre study
      Assessing the association of ECAC to lung disease in smokers
      8820 ex- or active smokers (43.7% had COPD and 16.6% had asthma (males (n=4667), females (n=4153); mean age: 59.7 ±6.9 years))CT scanECAC ≥50% reduction in CSAECAC prevalence was 5% in ex- or active smokers and 5.9% in participants with COPD (n=229/3856)The presence of ECAC was associated with worse respiratory quality of life in current or former smokers
      Sindhwani et al. 2016 [34]Prospective single-centre study
      To assess expiratory wheeze in patients with obstructive airway disorders
      25 patients (males (n=14), females (n=11), mean age: 62.7±7.81 years) with COPDCT scanTBM/EDAC ≥50% reduction of the airway lumenTBM/EDAC was found in 40% of COPD patientsFindings indicate value of screening patients with obstructive airway disease for TBM/EDAC
      El Sorougi et al. 2016 [33]Prospective single-centre study
      To determine the prevalence of TM in COPD patients
      30 patients with COPD (demographics were not reported)64-MDCT scanTM ≥50% in the tracheal lumen CSA20% of COPD patients showed evidence of TMA significant proportion of patients with COPD had features consistent with TM on dynamic CT scanning
      Weinstein et al. 2016 [52]Prospective single-centre study
      To describe the imaging characteristics of people presenting exertional dyspnoea
      6 military personnel (males (n=5), females (n=1), mean age: 39.5 years, age range: 24 to 53 years) with no underlying lung diseaseCT scan
      Bronchoscopy at rest and during exercise (cycling; n=2).
      EDAC ≥75% reduction of the airway lumenEDAC was detected on expiratory images during dynamic CT (n=2)EDAC may explain “unexplained” exertional dyspnoea and wheeze in military recruits
      Represas-Represas et al. 2015 [43]Prospective single-centre study
      To investigate the prevalence of EDAC in COPD
      53 patients (males (n=46), females (n=7), mean age: 65±9 years) with COPDHelicoidal MDCTEDAC >50% reduction in CSAPrevalence of EDAC was 9.4%EDAC in COPD patients is independent of disease severity and may not relate to symptoms
      O’Donnell et al. 2014 [25]¶Prospective single-centre study
      To determine the tracheal collapse in COPD patients
      67 patients (males (n=38), females (n=29); age: 65.1±6.5 years) with COPD64-detector row CT scanTracheal collapse ≥80% reduction in CSAAverage forced expiratory collapse (62±16%) was greater to end-expiratory collapse (17±18%)COPD patients display a wide range of tracheal collapse at end-expiration
      Wielpütz et al. 2014 [53]Prospective single-centre study
      To assess the feasibility of low-dose MDCT
      3 patients (3 males; mean age: 63.3 years) with COPD4D MDCT scanTM criterion was not reportedEDAC (n=1), sabre-sheath trachea and TBM (n=1), as well as tracheal stenosis (n=1) were demonstratedLow-dose MDCT may have equal diagnostic impact as bronchoscopy for tracheal instability
      Boiselle et al. 2013 [54]Prospective single-centre study
      To assess the tracheal collapse in morbidly obese, non-morbidly obese and normal weight COPD patients
      100 patients (males (n=52), females (n=48),
      mean age: 65±7 years) with COPD
      64-detector CT scanLAC criterion was not reportedExpiratory collapse was directly associated
      with BMI (p=0.002)
      Obesity is positively correlated with the degree of expiratory tracheal collapse
      among COPD patients
      O’Donnell et al. 2012 [40]#Prospective single-centre study
      To explore the association between forced expiratory tracheal collapse and age or sex
      81 healthy volunteers (males (n=41), females (n=40); age: 47±17 years)64-detector-row CT scanTracheal collapse≥80% reduction in CSAThe mean % collapse was similar for males (55±23%) and females (52±17%). The mean % collapse was correlated to age (r2 = 0.40, p< 0.001) in malesAge and sex should be considered when assessing forced expiratory airway collapse for suspected TM
      Boiselle et al. 2012 [24]¶Prospective single-centre study
      To determine the prevalence of tracheal collapse in COPD patients
      100 patients (males (n=52), females (n=48); age: 65±7 years) with COPD64-detector-row CT scanTracheal collapse ≥80% reduction in CSAPrevalence of TM was found in 20 participants (20%)TM is observed in a subset of patients with COPD, but the magnitude of collapse is independent of disease severity
      Boiselle et al. 2010 [32]Prospective single-centre study
      To assess the reproducibility of MDCT in measuring TM in healthy volunteers over time
      14 healthy volunteers (males (n=6), females (n=8), mean age: 48.7 ±13.8 years)64-MDCT scanTM criterion was not reported1st and 2nd year measures of tracheal collapse were strongly associated (r2=0.98, p<0.001)MDCT measurements of forced expiratory
      tracheal collapse in healthy volunteers is highly reproducible
      over time
      Litmanovich et al. 2010 [26]#Prospective single-centre study
      To assess the forced expiratory bronchial collapsibility in healthy volunteers
      51 healthy volunteers (males (n=25), females (n=26); age: 50±15 years)64-detector row MDCT scanExpiratory reduction in CSA of >50% and >80%, were both used73% of participants met the criterion (>50%) in one or both bronchiThe current data suggest the need for more rigorous criteria for the diagnosis of BM
      Wagnetz et al. 2010 [28]Prospective single-centre study
      To establish the use of a novel MDCT for the evaluation of TM
      6 patients (males (n=5), females (n=1); mean age: 53 years, age range: 37 to 70 years) with suspected TM (medical history was not reported)320-row MDCT scan and fibreoptic bronchoscopyTM/TBM≥50% reduction in CSAAll patients demonstrated TM/TBM with varying degrees of airway collapse (50% to >90% of the CSA)The 4D MDCT, isotropic, isovolumetric and isophasic, of the central airway is promising for the diagnosis of TM/TBM
      Boiselle et al. 2009 [14]#Prospective single-centre study
      To assess the tracheal collapsibility in healthy volunteers
      51 healthy volunteers (males (n=25), females (n=26); age: 50±15 years)64-detector row MDCT scanExpiratory reduction in CSA of >50%78% of healthy volunteers exceeded the current diagnostic criterion for TMThis study emphasises the need for a more rigorous diagnostic criterion to prevent overdiagnosis of TM
      McDermott et al. 2009 [39]Prospective single-centre study
      To determine the prevalence and severity of TM in adults with CF
      40 patients (males (n=22), females (n=18); mean age: 28±8, age range: 18–54) with CF and 10 controlsDynamic cine MDCT with 64-detector rowTM >50% or >75% reduction in CSA during coughTM was found in 69% of patients with CF during forced expiration and in 29% during coughingTM depicted at dynamic cine MDCT is a highly prevalent finding in patients with CF
      Inoue et al. 2009 [45]Retrospective single-centre study
      To evaluate the frequency of TBM associated with PE
      56 patients (males (n=55), females (n=1); mean age: 68.9 years, age range: 49–87 years) with PEMDCT scanner with two-detector rowTBM ≥50% decrease in CSAFour (7.1%) patients were diagnosed as having TM or BMTBM might be under- diagnosed in some patients with PE when using the standard criterion (e.g. ≥50%)
      Ochs et al. 2009 [46]Retrospective multicentre study
      To investigate the prevalence of TM in an emphysema cohort
      431 patients (males (n=267, mean age: 64 years, range: 41 to 76), females (n=164, mean age: 62 years, range: 41 to 76))CT scanLAC ≥50%, and >70% in the CSAPrevalence of TM was found in 13.4% participants based on ≥50% criterionA large degree of tracheal collapse can be found at end-expiration in patients with emphysema
      Ferretti et al. 2008 [27]Prospective single-centre study
      To compare dynamic and end-expiratory imaging to assess LAC in patients with suspected TBM
      70 patients (males (n=43), females (n=27); mean age: 57 years, age range: 12–79 years) with respiratory conditions (e.g. COPD)16-detector row helical CT scanTBM was not definedTBM was not found at the end of expiration, but its prevalence was 13% during dynamic expirationDynamic expiratory CT demonstrates a greater degree of LAC than the end-expiratory acquisition in patients with suspected TBM
      Lee et al. 2007 [50]Retrospective single-centre study
      To compare the dynamic expiratory CT against bronchoscopy for detecting airway malacia
      29 patients (males (n=12), females (n=17), mean age: 60 years, age range: 36 to 79 years) with COPD and relapsing polychondritisMDCT helical scanLAC >50% reduction in CSACT findings were concordant with bronchoscopy in 97% of patientsCT is a highly sensitive method for detecting airway malacia and could serve as an effective, noninvasive test for diagnosing LAC
      Boiselle et al. 2006 [20]Prospective single-centre study
      To describe the technical aspects of using 64-MDCT during coughing
      17 patients (males (n=6), females (n=11), age range: 62.4 years) with suspected TM64-MDCT scanTM >50% reduction in CSA during coughing64-MDCT during a coughing protocol was technically successful in 94% of patients64-MDCT is technically feasible and has the potential to make significant contributions to the noninvasive diagnosis of TM
      Lee et al. 2006 [55]Retrospective single-centre study
      To assess the prevalence of expiratory CT abnormalities, including malacia
      18 patients (males (n=3), females (n=15), mean age: 47 years; age range: 20–71 years) with relapsing polychondritisHelical MDCTLAC >50% reduction in CSACT abnormalities were present in 94% and airway malacia in 72% of patientsDynamic expiratory CT should be considered a standard component of airway evaluation in patients with relapsing polychondritis
      Nishino et al. 2006 [36]Prospective single-centre study
      To evaluate the frequency and severity of BM
      46 patients (males (n=10), females (n=36), mean age: 64 years, age range: 44–84 years) with bronchiectasisVolumetric high-resolution 4- or 8-detector CTLAC ≥50% reduction in the CSAPrevalence of BM was found in 70% of patients at end-expirationAir trapping in bronchiectasis might be greater in bronchiectasis patients with BM compared to those without
      Baroni et al. 2005 [38]Retrospective single-centre study
      To compare the dynamic- and end-expiratory CT in assessing LAC
      14 patients (males (n=11), females (n=3), mean age 53 years old and age range: 19–79 years) with various conditionsEight-detector row helical CT scanLAC ≥50% reduction in the CSACollapse was greater in dynamic expiration than in end-expiration (p<0.004)The reliance on end-expiratory imaging alone might result in a high level of false-negative results
      Baroni et al. 2005 [37]Prospective single-centre study
      To describe the role of pre- and post-operative dynamic CT in patients undergoing tracheoplasty
      5 patients (males (n=4), woman (n=1); mean age: 62, age range: 56–78)8-MDCT helical scanTBM ≥50% reduction in the CSATracheal collapse was found to be 58.9% pre- and 26.9% post-operatively during dynamic expirationDynamic expiratory CT is a potentially valuable tool in the pre- and post-operative evaluations of patients undergoing tracheoplasty
      Nishino et al. 2005 [35]Prospective single-centre study
      To investigate the frequency of BM associated with sarcoidosis
      18 patients (males (n=6), females (n=12); mean age: 47 years, age range: 29–64 years) with pulmonary sarcoidosisHigh-Resolution CTLAC >50% reduction in CSABM was found in 61% of patientsBM is frequently associated with sarcoidosis
      Heussel et al. 2004 [42]Prospective single-centre study
      To assess the respiratory lumen diameter, change in the tracheal level during continuous respiration
      38 subjects, 23 patients with COPD (age: 59 years, age range: 41–68 years) and 15 healthy adults (age: 62 years, age range: 48 to 74 years)Cine-MRILAC >50% reduction in CSAA pathological collapse occurred in 33% of volunteers and in 69.6% of patients with COPDThe airway collapse is significantly larger in patients with COPD compared to volunteers
      Hasegawa et al. 2003 [21]Retrospective single-centre study
      To determine the frequency of TM incidentally detected on CT pulmonary angiography (CTPA)
      163 (73
      males (n=73), females (n=90); mean age: 60 years) with suspected pulmonary embolism
      Single detector CT and MDCT (with 4 and 8 detectors)TM ≥50% decrease in tracheal lumenPrevalence of TM was found in 10% of the participants with suspected pulmonary embolismTM is a relatively common finding in CTPA when assessing patients with suspected pulmonary embolism
      Zhang et al. 2003 [3]Prospective single-centre study
      To compare standard- and low-dose CT images assessing tracheal lumen
      10 patients (males (n=5), females (n=5), mean age: 56 ±11 years) with bronchoscopically proved TBMMulti-section helical MDCT scanLAC >50% reduction in the CSATBM was found in all 10 patientsPaired inspiratory and dynamic expiratory CT images is a promising method for diagnosing TBM
      Aquino et al. 2001 [56]Retrospective and prospective single-centre study
      To explore the measurements of the trachea between inspiration and end-expiration on CT
      10 TM patients (males (n=6), females (n=4); mean age: 60 years, age range: 42 to 84 years) and 23 normal control patients (males (n=15), females (n=8); mean age: 40 years, age range: 27 to 57 years)CT scanDiagnostic criterion for TM was not reportedCollapsibility in tracheal CSA was significantly greater in patients with TM (1.9±0.9 cm2) compared to controls (2.4±0.6 cm2) during end-expirationPatients with TM demonstrate a higher airway collapse compared to controls
      Gilkeson et al. 2001 [4]Prospective single-centre study
      To examine the role of dynamic inspiratory-expiratory imaging with MDCT in patients with suspected TBM
      13 patients (males (n=7), females (n=6); mean age: 49 years and age range: 14–88 years) with respiratory conditions (e.g. asthma, chronic cough, smoking)MDCT scan, bronchoscopyLAC >50% reduction in the CSAAll patients showed evidence of TBM of different degrees, 50–75% (n=3) 75–100% (n=7), and 100% (n=3)MDCT with inspiratory-expiratory imaging is a promising method in the evaluation of patients with suspected TBM
      Heussel et al. 2001 [22]Prospective (including retrospective analysis) single-centre study
      To compare CT, MRI bronchoscopy, in the diagnosis of LAC
      29 patients (males (n=10), females (n=19); mean age: 61 years, age range: 27–82 years) with suspicion of or previously bronchoscopically verified tracheal collapseCT scans (spiral and cine), cine-MRI, bronchoscopy≥50% collapse of the CSABronchoscopy correlated with cine CT. MRI demonstrated similar time curves of tracheal CSA to cine CTCine CT is able to obtain significantly improved evaluation of respiratory collapse. Cine-MRI promises functional information due to free choice of imaging plane
      Suto & Tanabe, 1998 [41]Prospective single-centre study
      To evaluate tracheal collapsibility during coughing in patients with TM who underwent MRI
      6 patients (males (n=4), females (n=2); mean age: 40 years, age range: 44 to 68 years) with suspected TBM and 13 healthy volunteers (males (n=10), females (n=3); mean age: 40 years, age range: 17 to 63 years)1.5-T superconducting MRI systemDiagnostic criterion for TM was not reportedCollapse was 30±13% and 50±15% in forced expiration, and 38±16% and 75±12% during coughing in healthy and patients with TM, respectivelyCollapsibility during forced expiration-inspiration and collapsibility during coughing was not significant in patients with TM during MRI
      Stern et al. 1993 [57]Prospective single-centre study
      To define the range of intrathoracic tracheal diameters and CSA during forced respiration
      10 healthy volunteers (males (n=10), age range: 24–31 years)CT using the model C-100 scannerTM >70% reduction in the CSATrachea significantly decreased (p<0.001) from end-inspiration (280 mm2) to end-expiration (178 mm2)Intrathoracic tracheal shape, sagittal and coronal diameters, and CSA can vary greatly during a forced respiration

      #The studies by Litmanovich et al. 2010 and Boiselle et al. 2009 were not analysed as part of the main results as the participants of both studies were included in O'Donnell et al. 2012. ¶The study by Boiselle et al. 2013 was not analysed as part of the main results as the participants were included in O'Donnell et al. 2014. TBM: tracheobronchomalacia; GERD: gastro-oesophageal reflux disease; OSA: obstructive sleep apnoea; MDCT: multi-detector CT; LAC: large airway collapse; CSA: cross-sectional area; EDAC: excessive dynamic airway collapse; CT: computed tomography; TM: tracheomalacia; MRI: magnetic resonance imaging; BM: bronchomalacia; FVC: forced vital capacity; ILD: interstitial lung disease; ECAC: excessive central airway collapse; CF: cystic fibrosis; PE: pulmonary emphysema; CTPA: pulmonary angiography.

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      Detection and diagnosis of large airway collapse: a systematic review
      Alexandros Mitropoulos, Woo-Jung Song, Fatma Almaghlouth, Samuel Kemp, Michael Polkey, James H. Hull
      ERJ Open Research Jul 2021, 7 (3) 00055-2021; DOI: 10.1183/23120541.00055-2021

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      Detection and diagnosis of large airway collapse: a systematic review
      Alexandros Mitropoulos, Woo-Jung Song, Fatma Almaghlouth, Samuel Kemp, Michael Polkey, James H. Hull
      ERJ Open Research Jul 2021, 7 (3) 00055-2021; DOI: 10.1183/23120541.00055-2021
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      Online ISSN: 2312-0541

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