Comparison of hyperpolarized 3He-MRI, CT based parametric response mapping, and mucus scores in asthmatics

Purpose: The purpose of this study was to anatomically correlate ventilation defects with regions of air trapping by whole lung, lung lobe, and airway segment in the context of airway mucus plugging in asthma.Methods: A total of 34 asthmatics [13M:21F, 13 mild/moderate, median age (range) of 49.5 (3...

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Main Authors: Katherine J. Carey, Peter Hotvedt, David G. Mummy, Kristine E. Lee, Loren C. Denlinger, Mark L. Schiebler, Ronald L. Sorkness, Nizar N. Jarjour, Charles R. Hatt, Craig J. Galban, Sean B. Fain
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-08-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2023.1178339/full
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author Katherine J. Carey
Katherine J. Carey
Katherine J. Carey
Peter Hotvedt
David G. Mummy
David G. Mummy
Kristine E. Lee
Loren C. Denlinger
Mark L. Schiebler
Ronald L. Sorkness
Nizar N. Jarjour
Charles R. Hatt
Charles R. Hatt
Craig J. Galban
Sean B. Fain
author_facet Katherine J. Carey
Katherine J. Carey
Katherine J. Carey
Peter Hotvedt
David G. Mummy
David G. Mummy
Kristine E. Lee
Loren C. Denlinger
Mark L. Schiebler
Ronald L. Sorkness
Nizar N. Jarjour
Charles R. Hatt
Charles R. Hatt
Craig J. Galban
Sean B. Fain
author_sort Katherine J. Carey
collection DOAJ
description Purpose: The purpose of this study was to anatomically correlate ventilation defects with regions of air trapping by whole lung, lung lobe, and airway segment in the context of airway mucus plugging in asthma.Methods: A total of 34 asthmatics [13M:21F, 13 mild/moderate, median age (range) of 49.5 (36.8—53.3) years and 21 severe, 56.1 (47.1—62.6) years] and 4 healthy subjects [1M:3F, 38.5 (26.6—52.2) years] underwent HP 3He MRI and CT imaging. HP 3He MRI was assessed for ventilation defects using a semi-automated k-means clustering algorithm. Inspiratory and expiratory CTs were analyzed using parametric response mapping (PRM) to quantify markers of emphysema and functional small airways disease (fSAD). Segmental and lobar lung masks were obtained from CT and registered to HP 3He MRI in order to localize ventilation defect percent (VDP), at the lobar and segmental level, to regions of fSAD and mucus plugging. Spearman’s correlation was utilized to compare biomarkers on a global and lobar level, and a multivariate analysis was conducted to predict segmental fSAD given segmental VDP (sVDP) and mucus score as variables in order to further understand the functional relationships between regional measures of obstruction.Results: On a global level, fSAD was correlated with whole lung VDP (r = 0.65, p < 0.001), mucus score (r = 0.55, p < 0.01), and moderately correlated (−0.60 ≤ r ≤ −0.56, p < 0.001) to percent predicted (%p) FEV1, FEF25-75 and FEV1/FVC, and more weakly correlated to FVC%p (−0.38 ≤r≤ −0.35, p < 0.001) as expected from previous work. On a regional level, lobar VDP, mucus scores, and fSAD were also moderately correlated (r from 0.45–0.66, p < 0.01). For segmental colocalization, the model of best fit was a piecewise quadratic model, which suggests that sVDP may be increasing due to local airway obstruction that does not manifest as fSAD until more extensive disease is present. sVDP was more sensitive to the presence of a mucus plugs overall, but the prediction of fSAD using multivariate regression showed an interaction in the presence of a mucus plugs when sVDP was between 4% and 10% (p < 0.001).Conclusion: This multi-modality study in asthma confirmed that areas of ventilation defects are spatially correlated with air trapping at the level of the airway segment and suggests VDP and fSAD are sensitive to specific sources of airway obstruction in asthma, including mucus plugs.
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spelling doaj.art-113a354c8fa14727b192ab7f6ef47bdf2023-08-01T15:44:25ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2023-08-011410.3389/fphys.2023.11783391178339Comparison of hyperpolarized 3He-MRI, CT based parametric response mapping, and mucus scores in asthmaticsKatherine J. Carey0Katherine J. Carey1Katherine J. Carey2Peter Hotvedt3David G. Mummy4David G. Mummy5Kristine E. Lee6Loren C. Denlinger7Mark L. Schiebler8Ronald L. Sorkness9Nizar N. Jarjour10Charles R. Hatt11Charles R. Hatt12Craig J. Galban13Sean B. Fain14Department of Medical Physics, University of Wisconsin—Madison, Madison, WI, United StatesDepartment of Radiology, University of Wisconsin—Madison, Madison, WI, United StatesImbio LLC, Minneapolis, MN, United StatesDepartment of Nuclear Engineering, University of Michigan—Ann Arbor, Ann Arbor, MI, United StatesCenter for In Vivo Microscopy, Department of Radiology, Duke University, Durham, NC, United StatesCenter for In Vivo Microscopy, Duke University, Durham, NC, United StatesDepartment of Biostatistics, University of Wisconsin—Madison, Madison, WI, United StatesDivision of Allergy, Pulmonary, and Critical Care Medicine, University of Wisconsin—Madison, Madison, WI, United StatesDepartment of Radiology, University of Wisconsin—Madison, Madison, WI, United StatesSchool of Pharmacy, University of Wisconsin—Madison, Madison, WI, United StatesDivision of Allergy, Pulmonary, and Critical Care Medicine, University of Wisconsin—Madison, Madison, WI, United StatesImbio LLC, Minneapolis, MN, United States0Department of Radiology, University of Michigan, Ann Arbor, MI, United States0Department of Radiology, University of Michigan, Ann Arbor, MI, United States1Department of Radiology, University of Iowa, Iowa City, IA, United StatesPurpose: The purpose of this study was to anatomically correlate ventilation defects with regions of air trapping by whole lung, lung lobe, and airway segment in the context of airway mucus plugging in asthma.Methods: A total of 34 asthmatics [13M:21F, 13 mild/moderate, median age (range) of 49.5 (36.8—53.3) years and 21 severe, 56.1 (47.1—62.6) years] and 4 healthy subjects [1M:3F, 38.5 (26.6—52.2) years] underwent HP 3He MRI and CT imaging. HP 3He MRI was assessed for ventilation defects using a semi-automated k-means clustering algorithm. Inspiratory and expiratory CTs were analyzed using parametric response mapping (PRM) to quantify markers of emphysema and functional small airways disease (fSAD). Segmental and lobar lung masks were obtained from CT and registered to HP 3He MRI in order to localize ventilation defect percent (VDP), at the lobar and segmental level, to regions of fSAD and mucus plugging. Spearman’s correlation was utilized to compare biomarkers on a global and lobar level, and a multivariate analysis was conducted to predict segmental fSAD given segmental VDP (sVDP) and mucus score as variables in order to further understand the functional relationships between regional measures of obstruction.Results: On a global level, fSAD was correlated with whole lung VDP (r = 0.65, p < 0.001), mucus score (r = 0.55, p < 0.01), and moderately correlated (−0.60 ≤ r ≤ −0.56, p < 0.001) to percent predicted (%p) FEV1, FEF25-75 and FEV1/FVC, and more weakly correlated to FVC%p (−0.38 ≤r≤ −0.35, p < 0.001) as expected from previous work. On a regional level, lobar VDP, mucus scores, and fSAD were also moderately correlated (r from 0.45–0.66, p < 0.01). For segmental colocalization, the model of best fit was a piecewise quadratic model, which suggests that sVDP may be increasing due to local airway obstruction that does not manifest as fSAD until more extensive disease is present. sVDP was more sensitive to the presence of a mucus plugs overall, but the prediction of fSAD using multivariate regression showed an interaction in the presence of a mucus plugs when sVDP was between 4% and 10% (p < 0.001).Conclusion: This multi-modality study in asthma confirmed that areas of ventilation defects are spatially correlated with air trapping at the level of the airway segment and suggests VDP and fSAD are sensitive to specific sources of airway obstruction in asthma, including mucus plugs.https://www.frontiersin.org/articles/10.3389/fphys.2023.1178339/fullasthmaMRICTgas trappinghyperpolarized He-3parametric response mapping (PRM)
spellingShingle Katherine J. Carey
Katherine J. Carey
Katherine J. Carey
Peter Hotvedt
David G. Mummy
David G. Mummy
Kristine E. Lee
Loren C. Denlinger
Mark L. Schiebler
Ronald L. Sorkness
Nizar N. Jarjour
Charles R. Hatt
Charles R. Hatt
Craig J. Galban
Sean B. Fain
Comparison of hyperpolarized 3He-MRI, CT based parametric response mapping, and mucus scores in asthmatics
Frontiers in Physiology
asthma
MRI
CT
gas trapping
hyperpolarized He-3
parametric response mapping (PRM)
title Comparison of hyperpolarized 3He-MRI, CT based parametric response mapping, and mucus scores in asthmatics
title_full Comparison of hyperpolarized 3He-MRI, CT based parametric response mapping, and mucus scores in asthmatics
title_fullStr Comparison of hyperpolarized 3He-MRI, CT based parametric response mapping, and mucus scores in asthmatics
title_full_unstemmed Comparison of hyperpolarized 3He-MRI, CT based parametric response mapping, and mucus scores in asthmatics
title_short Comparison of hyperpolarized 3He-MRI, CT based parametric response mapping, and mucus scores in asthmatics
title_sort comparison of hyperpolarized 3he mri ct based parametric response mapping and mucus scores in asthmatics
topic asthma
MRI
CT
gas trapping
hyperpolarized He-3
parametric response mapping (PRM)
url https://www.frontiersin.org/articles/10.3389/fphys.2023.1178339/full
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