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Free-breathing Functional Pulmonary MRI

Posted Sep 30, 2017 Updated Apr 10, 2023
By Dante P.I. Capaldi BSc , Khadija Sheikh PhD , Rachel L. Eddy BEng , Fumin Guo MEng , Sarah Svenningsen PhD , Parameswaran Nair MD PhD FRCP FRCPC , David G. McCormack MD FRCPC , Grace Parraga PhD
16 min read

Rationale and Objectives

Ventilation heterogeneity is a hallmark feature of asthma. Our objective was to evaluate ventilation heterogeneity in patients with severe asthma, both pre- and post-salbutamol, as well as post-methacholine (MCh) challenge using the lung clearance index, free-breathing pulmonary 1 H magnetic resonance imaging (FDMRI), and inhaled-gas MRI ventilation defect percent (VDP).

Materials and Methods

Sixteen severe asthmatics (49 ± 10 years) provided written informed consent to an ethics board-approved protocol. Spirometry, plethysmography, and multiple breath nitrogen washout to measure the lung clearance index were performed during a single visit within 15 minutes of MRI. Inhaled-gas MRI and FDMRI were performed pre- and post-bronchodilator to generate VDP. For asthmatics with forced expiratory volume in 1 second (FEV 1 ) >70% predicted , MRI was also performed before and after MCh challenge. Wilcoxon signed-rank tests, Spearman correlations, and a repeated-measures analysis of variance were performed.

Results

Hyperpolarized 3 He ( P = .02) and FDMRI ( P = .02) VDP significantly improved post-salbutamol and for four asthmatics who could perform MCh ( n = 4). 3 He and FDMRI VDP significantly increased at the provocative concentration of MCh, resulting in a 20% decrease in FEV 1 (PC 20 ) and decreased post-bronchodilator ( P = .02), with a significant difference between methods ( P = .01). FDMRI VDP was moderately correlated with 3 He VDP (ρ = .61, P = .01), but underestimated VDP relative to 3 He VDP (−6 ± 9%). Whereas 3 He MRI VDP was significantly correlated with the lung clearance index, FDMRI was not (ρ = .49, P = .06).

Conclusions

FDMRI VDP generated in free-breathing asthmatic patients was correlated with static inspiratory breath-hold 3 He MRI VDP but underestimated VDP relative to 3 He MRI VDP. Although less sensitive to salbutamol and MCh, FDMRI VDP may be considered for asthma patient evaluations at centers without inhaled-gas MRI.

Introduction

Asthma is a chronic and often debilitating airways disease, characterized by intermittent worsening of breathlessness, cough, chest tightness, and wheeze, and is typically diagnosed based on spirometry measurements of bronchodilator reversibility or response to methacholine (MCh) challenge using the forced expiratory volume in 1 second (FEV 1 ) . Although current asthma therapies were developed based on FEV 1 improvements , this measurement of airflow limitation is relatively insensitive to small airway obstruction , which is believed to be the main site of inflammation and airway remodeling (or premodeling) in asthma . For many children and adults with asthma, disease control remains elusive, and a recent survey identified that over 90% of Canadian asthmatics reported poorly controlled disease and nearly half did not participate in any exercise of any type due to asthma symptoms . This unacceptable disease morbidity and the large and growing number of asthma patients of all ages have motivated the development of pulmonary imaging approaches to generate new and more sensitive biomarkers of small airway dysfunction. To date, however, it has been complex to use such imaging biomarkers in the development of new therapies in clinical trials or to guide therapy decisions in individual patients.

In asthmatics, thoracic computed tomography (CT) can be used to provide asthma biomarkers of gas-trapping , airway remodeling such as airway wall thickening and lumen narrowing , and dynamic changes in ventilation using xenon-enhanced dual-energy CT . Although ultra low-dose CT methods using iterative adaptive reconstruction methods are now under development , because of radiation dose concerns, the clinical use of CT in asthmatics has been limited, especially in mild disease and in children . Other examples include positron emission tomography and single photon emission computed tomography , both of which have been used in the research setting to evaluate regional ventilation heterogeneity in asthmatics .

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Materials and Methods

Study Logistics and Participants

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Spirometry, Plethysmography, and Multiple Breath Nitrogen Washout

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Image Acquisition

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Image Analysis

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Figure 1, FDMRI ventilation map and analysis pipelines. ( a ) Schematic for FDMRI ventilation map generation: (i) coregistered MRI aligned along the time axis; (ii) oscillating signal intensity pattern upon which discrete fast Fourier transforms performed; (iii) magnitude of the frequency of the first ventilation harmonic determined for every voxel; (iv) FDMRI ventilation maps generated. ( b ) Schematic of FDMRI VDP semiautomated segmentation: anatomical 1 H MRI segmented, k-means VDP segmentation, where cluster 1 (C1) = ventilation defects and clusters 2–5 (C2–C5) = hypointense to hyperintense ventilation. FDMRI, Fourier decomposition 1 H magnetic resonance imaging; MRI, magnetic resonance imaging; VDP, ventilation defect percent.

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Statistics

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Results

Participant Characteristics

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TABLE 1

Asthma Demographics, Medication, Control, and Pulmonary Function Tests

Mean (±SD) Asthma All ( n = 16) Severe ( n = 7) Severe Uncontrolled ( n = 9) Age (y) 49 (10) 50 (10) 49 (11) Male, n 6 2 4 BMI, kg ⋅ m −2 28 (4) 28 (5) 28 (4) FEV 1 % pred 66 (24) 64 (19) 68 (28) FVC % pred 84 (14) 85 (12) 83 (16) FEV 1 /FVC % 61 (15) 59 (14) 63 (17) RV % pred 140 (35) 142 (27) 139 (42) TLC % pred 106 (13) 104 (13) 108 (14) RV/TLC % 43 (10) 46 (7) 41 (11) FRC % pred 115 (25) 120 (20) 111 (29) R AW % pred 170 (61) 161 (45) 176 (74) LCI 9.2 (2.6) \* 9.8 (2.6) 8.6 (3.7) † ACQ score 2.0 (1.2) \* 1.2 (0.6) 2.6 (1.2) † AQLQ score 5.0 (1.4) \* 5.8 (0.8) 4.4 (1.5) † mMRC dyspnea score 0.9 (0.7) 0.7 (0.8) 1.0 (0.8) Borg dyspnea 1.4 (1.5) 0.6 (0.7) 2.1 (1.7) ICS, n (%) 16 (100) 7 (100) 9 (100) OCS, n (%) 6 (40) 2 (29) 4 (44) SABA, n (%) 14 (93) 6 (86) 8 (89) LABA, n (%) 16 (100) 7 (100) 9 (100) SAMA, n (%) 3 (20) 1 (14) 2 (22) LAMA, n (%) 4 (27) 1 (14) 3 (33) Anti-IgE, n (%) 3 (20) 1 (14) 2 (22) LTRA, n (%) 7 (47) 3 (43) 4 (44)

% pred , percent of predicted value; ACQ, Asthma Control Questionnaire; anti-IgE, anti-immunoglobulin E; AQLQ, Asthma Quality of Life Questionnaire; BMI, body mass index; FEV 1 , forced expiratory volume in 1 second; FRC, functional residual capacity; FVC, forced vital capacity; ICS, inhaled corticosteroids; LABA, long-acting β2 agonist; LAMA, long-acting anticholinergic; LCI, lung clearance index; LTRA, leukotriene receptor antagonists; mMRC, modified Medical Research Council; OCS, oral corticosteroid; R AW , airways resistance; RV, residual volume; SABA, short-acting β2 agonist; SAMA, short-acting anticholinergic; TLC, total lung capacity.

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Ventilation Response to Salbutamol

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Figure 2, Ventilation MRI for severe and severe uncontrolled asthmatics. ( a ) Hyperpolarized inhaled gas ( cyan ) and FDMRI ( magenta ) for a representative severe asthmatic (female, age = 57 years, baseline FEV 1 = 52% pred , post-salbutamol FEV 1 = 60% pred ) and severe uncontrolled asthmatic (male, age = 56 years, baseline FEV 1 = 37% pred , post-salbutamol FEV 1 = 36% pred ) at baseline and post-salbutamol. Yellow arrows show ventilation defect spatial relationships. ( b ) Box and whisker plot (box = 25th–75th percentile; whiskers = minimum to maximum) for VDP baseline and post-salbutamol for 3 He MRI ( n = 12; baseline VDP = 11.1 ± 10.1%, post-salbutamol VDP = 8.1 ± 7.6%; P = .02) and FDMRI ( n = 12; baseline VDP = 3.9 ± 3.0%, post-salbutamol VDP = 2.8 ± 2.1%; P = .02). FDMRI, Fourier decomposition 1 H magnetic resonance imaging; FEV 1 , forced expiratory volume in 1 second; MRI, magnetic resonance imaging; VDP, ventilation defect percent.

TABLE 2

Subject Listing of Hyperpolarized Inhaled-gas MRI, FDMRI and Multiple Breath Gas Washout Measurements for Each Time Point

Pre-salbutamol PC 20 Post-salbutamol 3 He FDMRI LCI 3 He FDMRI LCI 3 He FDMRI LCI VDP (%) VDP (%) VDP (%) Severe S1 3.6 0.7 7.7 5.2 1.6 – 2.6 1.5 7.3 S2 7.0 7.6 9.5 – – – 3.3 5.5 10.1 S3 2.2 0.6 6.7 – – – 2.4 1.7 6.1 S4 9.1 4.9 13.5 – – – 7.4 2.6 13.2 S5 17.0 1.6 11.7 – – – 17.5 1.2 9.7 S6 10.3 2.3 11.9 – – – 9.6 1.3 10.8 S7 1.0 0.6 7.4 – – – 0.5 0.7 7.7 Mean ± SD 7.2 2.6 9.8 5.2 1.6 – 6.2 2.1 9.3 5.6 2.7 2.6 – – – 5.9 1.6 2.4 Severe uncontrolled S8 27.7 7.9 17.5 – – – 24.2 5.4 15.5 S9 5.2 0.2 8.6 6.0 8.1 – 7.0 1.5 8.2 S10 1.9 0.2 7.1 8.0 5.3 – 1.8 1.5 7.7 S11 2.9 4.9 7.1 – – – 2.4 3.3 6.6 S12 2.1 1.2 6.2 15.8 5.9 – 1.2 0.2 6.5 S13 3.2 1.5 6.4 – – – 3.1 0.7 6.4 S14 32.1 4.7 – – – – 17.2 5.1 – S15 5.7 9.0 7.5 – – – 5.7 6.1 7.4 S16 14.6 1.6 8.7 – – – 3.5 0.3 8.8 Mean ± SD 10.6 3.5 8.6 10.0 6.4 – 7.4 2.7 8.4 11.6 3.3 3.7 5.1 1.5 – 8.0 2.3 3.0

FDMRI, Fourier decomposition 1 H magnetic resonance imaging; LCI, lung clearance index; PC 20 , provocative concentration that decreased the forced expiratory volume in 1 second (FEV 1 ) by 20%; SD, standard deviation; VDP, ventilation defect percent.

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Ventilation Response to MCh Challenge and Salbutamol Rescue

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Figure 3, Methacholine challenge. ( a ) Representative severe asthmatic center coronal slice 3 He ( cyan ) MRI and FDMRI ( magenta ) (female, age = 45 years), baseline FEV 1 = 95% pred , PC 20 = 0.123 mg/mL, post-salbutamol FEV 1 = 101% pred at baseline ( 3 He VDP = 3.6%, FDMRI VDP = 0.7%), post-MCh ( 3 He VDP = 5.2%, FDMRI VDP = 1.6%), and post-salbutamol ( 3 He VDP = 2.6%, FDMRI VDP = 1.5%). ( b ) Box and whisker plot (box = 25th–75th percentile; whiskers = minimum to maximum) for 3 He MRI VDP and FDMRI VDP at baseline ( n = 4; 3 He VDP = 3.2 ± 0.8%, FDMRI VDP = 0.6 ± 0.2%), post-MCh ( n = 4; 3 He VDP = 8.8 ± 2.4%, FDMRI VDP = 5.1 ± 1.5%), and post-salbutamol ( n = 4; 3 He VDP = 3.1 ± 1.3%, FDMRI VDP = 1.2 ± 0.7%). FDMRI, Fourier decomposition 1 H magnetic resonance imaging; FEV 1 , forced expiratory volume in 1 second; MCh, methacholine; MRI, magnetic resonance imaging; VDP, ventilation defect percent.

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Relationships and Agreement

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Figure 4, Relationships for FDMRI with 3 He MRI. ( a ) FDMRI VDP was significantly correlated with 3 He MRI VDP ( n = 16, ρ = .61, P = .01, y = 0.1×+1.9). ( b ) Bland-Altman analysis of agreement for FDMRI with 3 He MRI VDP ( n = 16, bias = −6.0 ± 8.6%, lower limit = −22.9%, upper limit = 10.8%). Dotted lines indicate the 95% confidence intervals. FDMRI, Fourier decomposition 1 H magnetic resonance imaging; MRI, magnetic resonance imaging; VDP, ventilation defect percent.

TABLE 3

Relationship of Hyperpolarized Inhaled-gas MRI and FDMRI with Pulmonary Function and LCI

Spearman ρ ( P ) 3 He MRI VDP % FDMRI VDP % ( n = 16) ( n = 16) FEV 1 % pred −.78 (.0006) −.45 (.08) FVC % pred −.53 (.03) −.43 (.09) FEV 1 /FVC %−.75 (.001) -.38 (.1) RV % pred .45 (.08).51 (.04) TLC % pred .19 (.5) .35 (.2) RV/TLC % .46 (.07) .28 (.3) FRC % pred .72 (.002).61 (.01) R AW % pred .80 (.0004).57 (.02) LCI.85 (.0001) \* .49 (.06) \* 3 He MRI VDP % –.61 (.01) FDMRI VDP %.61 (.01) –

ρ, Spearman correlation coefficients; % pred , percent of predicted value; FDMRI, Fourier decomposition 1 H magnetic resonance imaging; FEV 1 , forced expiratory volume in 1 second; FRC, functional residual capacity; FVC, forced vital capacity; LCI, lung clearance index; MRI, magnetic resonance imaging; R AW , airways resistance; RV, residual volume; TLC, total lung capacity; VDP, ventilation defect percent.

Bold text indicates significant relationships.

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Discussion

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Acknowledgments

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Academic Radiology, Volume 24, Issue 10
Journals General Radiology
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