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The importance of central airway dilatation in patients with bronchiolitis obliterans

Mariko Kogo, Hisako Matsumoto, Naoya Tanabe, Toyofumi F. Chen-Yoshikawa, Naoki Nakajima, Akihiko Yoshizawa, Tsuyoshi Oguma, Susumu Sato, Natsuko Nomura, Chie Morimoto, Hironobu Sunadome, Shimpei Gotoh, Akihiro Ohsumi, Hiroshi Date, Toyohiro Hirai
ERJ Open Research 2021 7: 00123-2021; DOI: 10.1183/23120541.00123-2021
Mariko Kogo
1Dept of Respiratory Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan
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Hisako Matsumoto
1Dept of Respiratory Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan
5These authors contributed equally to this work
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  • For correspondence: matsumoto.hisako.v92@kyoto-u.jp
Naoya Tanabe
1Dept of Respiratory Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan
5These authors contributed equally to this work
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  • ORCID record for Naoya Tanabe
Toyofumi F. Chen-Yoshikawa
2Dept of Thoracic Surgery, Graduate School of Medicine, Nagoya University, Nagoya, Japan
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Naoki Nakajima
3Dept of Diagnostic Pathology, Graduate School of Medicine, Kyoto University, Kyoto, Japan
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Akihiko Yoshizawa
3Dept of Diagnostic Pathology, Graduate School of Medicine, Kyoto University, Kyoto, Japan
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Tsuyoshi Oguma
1Dept of Respiratory Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan
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Susumu Sato
1Dept of Respiratory Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan
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Natsuko Nomura
1Dept of Respiratory Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan
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Chie Morimoto
1Dept of Respiratory Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan
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Hironobu Sunadome
1Dept of Respiratory Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan
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Shimpei Gotoh
1Dept of Respiratory Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan
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Akihiro Ohsumi
4Dept of Thoracic Surgery, Graduate School of Medicine, Kyoto University, Kyoto, Japan
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Hiroshi Date
4Dept of Thoracic Surgery, Graduate School of Medicine, Kyoto University, Kyoto, Japan
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Toyohiro Hirai
1Dept of Respiratory Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan
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Figures

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  • FIGURE 1
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    FIGURE 1

    Patient flow chart. Thirty-eight patients were included, of which 22 had airway dilatation on CT. Twenty-four and 17 patients were quantitatively analysed for inspiratory CT and paired inspiratory–expiratory CT, respectively. BO: bronchiolitis obliterans; CT: computed tomography; HRCT: high-resolution computed tomography.

  • FIGURE 2
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    FIGURE 2

    Associations between the Reiff score and variables on inspiratory CT. a) CT-TLV/pred TLC and b) LAV−950%. The extent of airway dilatation was expressed by the Reiff score, which assessed the number of lobes involved (with the lingula considered to be a separate lobe) and the degree of dilatation (tubular=1, varicose=2 and cystic=3). The maximum score is 18, and the minimum score is 1 for a patient with airway dilatation. Patients without airway dilatation were scored as 0. CT: computed tomography; pred TLC: predicted total lung capacity; LAV−950%: percentage of low attenuation volume <−950 Hounsfield units.

  • FIGURE 3
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    FIGURE 3

    Longitudinal data of patients with (a–d) and without (e–h) airway dilatation. a) and e) show HRCT of each patient. The airways with a white arrow were measured for lumen. The longitudinal changes in pulmonary function test (unavailable from the middle due to repeating pneumothorax in both patients) and indices on HRCT are presented in (b) and (f). c) and g) show representative lung histology of the patients. The small airways <2 mm in diameter are shown with arrows (white arrow: normal airway, black arrow: narrowing or obstructive airway). [c) elastica Masson stain, g) elastica van Gieson stain]. d) and h) show one of the narrowing and normal airways, respectively, at high magnification of circled airways in (c) and (g) [d) elastica Masson stain, h) elastica van Gieson stain]. BO: bronchiolitis obliterans; FEV1: forced expiratory volume in 1 s; HRCT: high-resolution computed tomography; LAV−950%: percentage of low attenuation volume <−950 Hounsfield units; fSAD: functional small airway disease; RV: residual volume; TLC: total lung capacity.

  • FIGURE 4
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    FIGURE 4

    Pathological measurements related to BO of relatively circular bronchioles. a) The percentage of narrowing or obstructive bronchioles due to BO among the total number of assessed bronchioles per patient and b) thickness of airway wall compartments adjusted by Pbm. c) and d) show the associations between Reiff score and the extent of BO and thickness of subepithelium. The Reiff score assesses the number of lobes involved (with the lingula considered to be a separate lobe) and the degree of dilatation (tubular=1, varicose=2 and cystic=3). The maximum score is 18, and the minimum score is 1 for a patient with airway dilatation. Patients without airway dilatation were scored as 0. The boxes represent the interquartile range with a median (the horizontal line). BO: bronchiolitis obliterans; Pbm: perimeter of the basement membrane. *p<0.05.

Tables

  • Figures
  • TABLE 1

    Patient characteristics at registration for lung transplantation

    Airway dilatation−
    n=16
    Airway dilatation+
    n=22
    p-value
    Male9 (56)9 (41)0.35
    Age, years33 (14–47)25 (15–42)0.43
    Height, cm158 (141–169)159 (143–164)0.89
    Weight, kg39.3 (25.7–50.6)40.0 (28.9–49.6)0.70
    Ex-smokers1 (6)3 (14)0.46
    Causes of BO
     HSCT14 (88)20 (91)0.74
     Lung transplantation2 (13)2 (9)
      Bilateral/right/left0 (0)/1 (6)/1 (6)2 (9)/0 (0)/0 (0)
    BO with prominent fibrosis3 (19)1 (5)0.16
     Prednisolone use11 (69)19 (86)0.19
      Dose, mg·day−115 (7.5–15)8 (4.0–12.5)0.13
    Immunosuppressive agent use6 (38)12 (55)0.30
    Inhaled corticosteroid use10 (63)12 (55)0.62
    Time from the causes of BO to diagnosis of BO, year2.3 (0.8–5.2)1.3 (0.7–2.9)0.17
    Time from the diagnosis of BO to registration, years1.5 (0.6–4.1)2.8 (1.1–6.0)0.15
    Age at diagnosis of BO, years31 (13–44)21 (12–37)0.31
    Time from registration to lung transplantation#, months2.4 (0.6–18.8)1.5 (1.2–17.3)0.73
    Pulmonary function test¶
     FVC, % of predicted48.3 (16.3–68.4)46.5 (38.9–50.8)1.00
     FEV1, % of predicted20.1 (16.7–44.0)22.0 (18.3–23.0)0.76
     FEV1/FVC, %68.5 (35.0–96.1)42.7 (34.5–50.1)0.15
     RV, % of predicted87.0 (54.6–166.2)176.8 (131.7–236.1)0.03
     RV/TLC, %46.4 (41.9–50.8)53.2 (46.9–58.9)0.12
    Pneumonia within the previous year6 (38)8 (36)0.94
    Reiff score07 (4–10)–

    BO: bronchiolitis obliterans; HSCT: hematopoietic stem-cell transplantation; FVC: forced vital capacity; FEV1: forced expiratory volume in 1 s; RV: residual volume; TLC: total lung capacity. All values are expressed as median (interquartile range) except categorical variables, which are expressed as n (%).

    #29 patients received living-donor lung transplantation.

    ¶Available for 21 patients (airway dilatation+ n=12, airway dilatation− n=9).

    • TABLE 2

      Bacterial culture of the sputum at registration

      Airway dilatation−
      n=14
      Airway dilatation+
      n=18
      p-value
      Streptococcus ssp.0 (0)1 (6)0.37
      Staphylococcus ssp.0 (0)2 (11)0.20
      Pseudomonas aeruginosa0 (0)7 (39)0.01
      Other gram-negative bacilli2 (14)3 (17)0.85
       Haemophilus influenzae1 (7)0
       Klebsiella oxytoca1 (7)0
       Escherichia coli02 (11)
       Stenotrophomonas maltophilia01 (6)
      Normal flora only12 (86)8 (44)0.02
      No growth0 (0)1 (6)0.37

      All values are expressed as n (%).

      • TABLE 3

        Quantitative analysis for inspiratory CT (A) and paired inspiratory and expiratory CT (B) among patients with and without airway dilatation

        A
        Airway dilatation−
        n=10
        Airway dilatation+
        n=14
        p-value
        CT-TLV/pred TLC, %42.0 (21.3–58.9)69.7 (56.7–97.0)0.009
        LAV−950%, %15.3 (5.7–25.1)29.3 (15.1–41.7)0.050
        B
        Airway dilatation−
        n=7
        Airway dilatation+
        n=10
        p-value
        LAV−856%, %46.3 (0.6–57.2)66.5 (54.1–72.6)0.036
        fSAD, %10.0 (0.2–33.9)34.7 (28.3–36.4)0.057

        CT-TLV: total lung capacity calculated on inspiratory CT; pred TLC: predicted total lung capacity; LAV−950%: low attenuation volume <−950 Hounsfield units (HU) at end inspiration; LAV−856%: low attenuation volume <−856 HU at end expiration; fSAD: functional small airway disease. All values are expressed as median (interquartile range).

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        The importance of central airway dilatation in patients with bronchiolitis obliterans
        Mariko Kogo, Hisako Matsumoto, Naoya Tanabe, Toyofumi F. Chen-Yoshikawa, Naoki Nakajima, Akihiko Yoshizawa, Tsuyoshi Oguma, Susumu Sato, Natsuko Nomura, Chie Morimoto, Hironobu Sunadome, Shimpei Gotoh, Akihiro Ohsumi, Hiroshi Date, Toyohiro Hirai
        ERJ Open Research Oct 2021, 7 (4) 00123-2021; DOI: 10.1183/23120541.00123-2021

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        The importance of central airway dilatation in patients with bronchiolitis obliterans
        Mariko Kogo, Hisako Matsumoto, Naoya Tanabe, Toyofumi F. Chen-Yoshikawa, Naoki Nakajima, Akihiko Yoshizawa, Tsuyoshi Oguma, Susumu Sato, Natsuko Nomura, Chie Morimoto, Hironobu Sunadome, Shimpei Gotoh, Akihiro Ohsumi, Hiroshi Date, Toyohiro Hirai
        ERJ Open Research Oct 2021, 7 (4) 00123-2021; DOI: 10.1183/23120541.00123-2021
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