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Pulmonary vascular pruning in smokers with bronchiectasis

Alejandro A. Diaz, Diego J. Maselli, Farbod Rahaghi, Carolyn E. Come, Andrew Yen, Erick S. Maclean, Yuka Okajima, Carlos H. Martinez, Tsuneo Yamashiro, David A. Lynch, Wei Wang, Gregory L. Kinney, George R. Washko, Raúl San José Estépar
ERJ Open Research 2018 4: 00044-2018; DOI: 10.1183/23120541.00044-2018
Alejandro A. Diaz
1Division of Pulmonary and Critical Care Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
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  • For correspondence: ADiaz6@bwh.harvard.edu
Diego J. Maselli
2Division of Pulmonary Diseases and Critical Care, University of Texas Health Science Center, San Antonio, TX, USA
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Farbod Rahaghi
1Division of Pulmonary and Critical Care Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
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Carolyn E. Come
1Division of Pulmonary and Critical Care Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
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Andrew Yen
3Dept of Radiology, University of California, San Diego, CA, USA
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Erick S. Maclean
1Division of Pulmonary and Critical Care Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
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Yuka Okajima
1Division of Pulmonary and Critical Care Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
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Carlos H. Martinez
4Division of Pulmonary and Critical Care Medicine, University of Michigan Health System, Ann Arbor, MI, USA
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Tsuneo Yamashiro
5Dept of Radiology, Graduate School of Medical Science, University of the Ryukyus, Nishihara, Japan
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David A. Lynch
6Dept of Radiology, National Jewish Health, Denver, CO, USA
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Wei Wang
7Division of Sleep Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
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Gregory L. Kinney
8Colorado School of Public Health, University of Colorado Denver, Aurora, CO, USA
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  • ORCID record for Gregory L. Kinney
George R. Washko
1Division of Pulmonary and Critical Care Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
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Raúl San José Estépar
9Dept of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA
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  • FIGURE 1
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    FIGURE 1

    Illustration of intraparenchymal pulmonary vascular pruning in bronchiectasis. Axial computed tomography images of the right lower lobe (RLL) from subjects a) without and b) with bronchiectasis. c and d) Three-dimensional reconstructions of the intraparenchymal pulmonary vascular tree of the right lung from the same subjects. Note the lack of pulmonary vessels in the RLL from the subject with bronchiectasis (d). e) Plot of RLL blood vessel volume to the vessel size for both subjects. Note a lower peak in blood vessel volume of small, distal pulmonary vessels in the RLL of bronchiectatic lung compared with nonbronchiectatic lung.

  • FIGURE 2
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    FIGURE 2

    a) Forced expiratory volume in 1 s (FEV1) and b) 6-min walk test (6MWT) distance by bronchiectasis in any lobe/vascular pruning in the lower lobes groups (n=485). Group 0: bronchiectasis−/vascular pruning− (n=187); group 1: bronchiectasis+/vascular pruning− (n=82); group 2: bronchiectasis−/vascular pruning+ (n=143); group 3: bronchiectasis+/vascular pruning+ (n=73). Note that group 3 had lower FEV1 and 6MWT distance than group 1. p-values are from univariate models. See the main text for the results of the adjusted models. One subject was excluded from these analyses because of a missing right lower lobe ratio of blood vessel volume in vessels <5 mm2 in cross-section to total blood vessel volume, leaving a sample size of 485. The 6MWT distance measurement was missing in two additional subjects.

Tables

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  • TABLE 1

    Demographic and clinical characteristics of the subjects by bronchiectasis status

    Subjects without bronchiectasisSubjects with bronchiectasisp-value
    Subjects331155
    Age years60±964±9<0.0001
    Females57%68%0.02
    Non-Hispanic white race78%78%0.98
    Height cm168±9166±80.009
    Body mass index kg·m−229±629±60.86
    Current smoking status41%37%0.33
    Smoking history pack-years45±2545±230.93
    Chronic heart failure1.8%0.7%0.44
    Coronary artery disease10%15%0.12
    FEV1 L2.2±0.82.0±0.80.006
    FEV1 % predicted77±2477±260.73
    FVC L3.3±0.93.0±0.90.002
    FVC % predicted88±1788±190.84
    TLCCT L5.5±1.45.3±1.20.29
    TLCCT % predicted97±1799±140.32
    6-min walk test distance m428±119403±1170.03
    Resting SaO2 %96±396±30.32
    Spirometric COPD47%50%0.52
    Whole-lung TBV mL277±61275±590.68
    Whole-lung BV5 mL167±41164±390.46
    Whole-lung BV5/TBV %60±660±70.45
    Whole-lung %LAA−950 %6.9±9.87.3±9.00.72
    Upper-lobe %LAA−950 %7.8±10.87.9±9.30.90
    Lower-lobe %LAA−950 %5.5±8.06.3±8.80.31

    Data are presented as mean±sd, unless otherwise stated. Missing data: total lung capacity determined by computed tomography (TLCCT), n=4; TLCCT % predicted, n=4; 6-min walk test, n=2; whole-lung percentage of low-attenuation areas below −950 Hounsfield units (%LAA−950), n=4; %LAA−950 of the upper and lower lobes, n=4. FEV1: forced expiratory volume in 1 s; FVC: forced vital capacity; SaO2: arterial oxygen saturation; COPD: chronic obstructive pulmonary disease; TBV: total blood vessel volume; BV5: blood vessel volume in vessels <5 mm2 in cross-section.

    • TABLE 2

      Description of the computed tomography (CT) findings in subjects with bronchiectasis (n=155)

      Bronchiectasis type
       Cylindric146 (94%)
       Varicose8 (5)%
       Cystic1 (1%)
      Bronchiectasis location#
       Right upper lobe19 (12%)
       Right middle lobe97 (63%)
       Right lower lobe81 (52%)
       Left upper lobe53 (34%)
       Left lower lobe62 (40%)
      Number of lobes with bronchiectasis¶
       162 (40%)
       238 (25%)
       326 (17%)
       ≥429 (19%)
      CT bronchiectasis score median (IQR)3 (2.0–5.0)

      IQR: interquartile range. #: percentages do not sum to 100% as some subjects had more than one lobe involved; ¶: percentages do not sum to 100% due to rounding.

      • TABLE 3

        Ratio of blood vessel volume in vessels <5 mm2 in cross-section (BV5) to total blood vessel volume (TBV) by lung lobe and bronchiectasis status

        Lung lobeSubjects without bronchiectasisSubjects with bronchiectasisp-value
        Right upper lobe64±765±80.90
        Right middle lobe54±954±100.91
        Right lower lobe58±755±90.004
        Left upper lobe62±761±70.87
        Left lower lobe55±951±100.0008

        Data are presented as mean±sd, unless otherwise stated. Results are from univariate comparisons of BV5/TBV×100 between subjects with bronchiectasis in a specific lobe only and those without bronchiectasis in any lobe. Missing values: one subject had no lobar vascular measurements and one subject had no vascular measurement in the right middle lobe.

        • TABLE 4

          Multivariable analysis for the differences in the ratio of blood vessel volume in vessels <5 mm2 in cross-section (BV5) to total blood vessel volume (TBV) between subjects with lower-lobe bronchiectasis and without bronchiectasis

          Cohort/subcohortDifference in lower-lobe BV5/TBVsep-value
          Entire cohort−1.50.35<0.0001
          Emphysema status subcohort
           Subjects with emphysema−1.80.520.0008
           Subjects without emphysema−1.60.460.0005

          The differences in lower-lobe BV5/TBV×100 are from a multivariable regression model where the presence of lower lobes bronchiectasis is the main predictor. Analyses were adjusted for age, sex, race, pack-years smoked, forced expiratory volume in 1 s % predicted, total lung capacity determined by computed tomography % predicted, resting arterial oxygen saturation, percentage of low-attenuation areas below −950 Hounsfield units (%LAA−950) of the lower lobes and coronary artery disease. For the analysis stratified by emphysema of the lower lobes, %LAA−950 was omitted as a covariate.

          • TABLE 5

            Multivariable analysis for the differences in the ratio of blood vessel volume in vessels <5 mm2 in cross-section (BV5) to total blood vessel volume (TBV) between subjects with lower lobes bronchiectasis and without bronchiectasis using alternate definitions of the disease

            Alternate definitionDifference in lower-lobe BV5/TBVsep-value
            1) Two or more bronchial paths involved
             Entire cohort−1.80.40<0.0001
             Emphysema status subcohort
              Subjects with emphysema−1.80.570.002
              Subjects without emphysema−1.30.490.009
            2) Lack of airway lumen tapering+airway seen within 1 cm of the pleura
             Entire cohort−2.10.580.0003
             Emphysema status subcohort
              Subjects with emphysema−1.90.770.01
              Subjects without emphysema−2.40.800.003

            The differences in lower-lobe BV5/TBV×100 are from a multivariable regression model where the presence of bronchiectasis in the lower lobes is the main predictor. Analyses were adjusted for age, sex, race, pack-years smoked, forced expiratory volume in 1 s % predicted, total lung capacity determined by computed tomography % predicted, resting arterial oxygen saturation, percentage of low-attenuation areas below −950 Hounsfield units (%LAA−950) of the lower lobes and coronary artery disease. For the analysis stratified by emphysema of the lower lobes, %LAA−950 was omitted as a covariate.

            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.

              TABLE E1 Reading for bronchiectasis on 486 baseline CT scans 00044-2018_tableE1

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            Pulmonary vascular pruning in smokers with bronchiectasis
            Alejandro A. Diaz, Diego J. Maselli, Farbod Rahaghi, Carolyn E. Come, Andrew Yen, Erick S. Maclean, Yuka Okajima, Carlos H. Martinez, Tsuneo Yamashiro, David A. Lynch, Wei Wang, Gregory L. Kinney, George R. Washko, Raúl San José Estépar
            ERJ Open Research Oct 2018, 4 (4) 00044-2018; DOI: 10.1183/23120541.00044-2018

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            Pulmonary vascular pruning in smokers with bronchiectasis
            Alejandro A. Diaz, Diego J. Maselli, Farbod Rahaghi, Carolyn E. Come, Andrew Yen, Erick S. Maclean, Yuka Okajima, Carlos H. Martinez, Tsuneo Yamashiro, David A. Lynch, Wei Wang, Gregory L. Kinney, George R. Washko, Raúl San José Estépar
            ERJ Open Research Oct 2018, 4 (4) 00044-2018; DOI: 10.1183/23120541.00044-2018
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